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  • 1051.
    Stångberg, Josefine
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    The evolution of sexual dimorphism in life history traits2017Report (Other academic)
    Abstract [en]

    Many dioecious organisms exhibit some level of sexual dimorphism; the sexes can differ in phenotype, and can have different fitness optima for certain traits and have different reproductive strategies. Sex-specific selection, thus, can be highly diverging in both magnitude and direction. When selection for a trait differs in direction we have antagonistic selection; this often leads to sexual conflicts since the two sexes share most of their genetic architecture. Sexual dimorphism is often seen as a resolution to sexual conflict, a way to decouple the genetic basis of traits under conflict and allow sex-specific expression. One way to better understand the evolution of sexual dimorphism is using a life history theory framework; where traits linked to growth, reproduction and survival are studied and quantified. These quantitative traits, their genetic architecture and how they covary within and between the two sexes, can be further studied using a quantitative genetics approach – G and B matrices. These are essentially genetic variance-covariance matrices of all traits measured, pairwise comparisons that give a picture of how these traits coevolve within an individual (G), but also how different traits covary between the sexes (B). These tools allow us to understand the underlying genetic architecture of life history traits, and also how these traits change under different and sex-specific selection pressures. This, in turn, will aid our understanding of how sexual dimorphism evolves. I end this review by focusing on a particular model species for studying these questions; the nematode Caenorhabditis remanei. 

  • 1052. Sudyka, J.
    et al.
    Arct, A.
    Drobniak, S.
    Dubiec, A.
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Cichon, M.
    Experimentally increased reproductive effort alters telomere length in the blue tit (Cyanistes caeruleus)2014In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 27, no 10, p. 2258-2264Article in journal (Refereed)
    Abstract [en]

    Telomeres have recently been suggested to play important role in ageing and are considered to be a reliable ageing biomarkers. The life history theory predicts that costs of reproduction should be expressed in terms of accelerated senescence, and some empirical studies do confirm such presumption. Thus, a link between reproductive effort and telomere dynamics should be anticipated. Recent studies have indeed demonstrated that reproduction may trigger telomere loss, but actual impact of reproductive effort has not received adequate attention in experimental studies. Here, we experimentally manipulated reproductive effort by increasing the brood size in the wild blue tit (Cyanistes caeruleus). We show that parents attending enlarged broods experienced larger yearly telomere decay in comparison to control birds attending unaltered broods. In addition, we demonstrate that the change in telomere length differs between sexes, but this effect was independent from our treatment. To our knowledge, this is the first experimental study in the wild revealing that telomere dynamics may be linked to reproductive effort. Thus, telomere shortening may constitute one of the potential proximate mechanisms mediating the costs of reproduction.

  • 1053.
    Sudyka, Joanna
    et al.
    Univ Warsaw, Ctr New Technol, Banacha 2c, PL-02097 Warsaw, Poland;Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Arct, Aneta
    Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Drobniak, Szymon M.
    Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Cichon, Mariusz
    Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Birds with high lifetime reproductive success experience increased telomere loss2019In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 15, no 1, article id 20180637Article in journal (Refereed)
    Abstract [en]

    Lifetime reproductive success (LRS) is what counts in terms of evolution, but investments in reproduction entail costs for an organism. The idea that telomere dynamics may be shaped in response to such costs is already established; however, we still lack information on whether this relation translates to overall fitness. Here, we quantified LRS (number of fledged young) and longitudinal telomere dynamics of small passerine birds-the blue tits (Cyanistes caeruleus). We found that individual telomere erosion rate was positively associated with lifetime fledgling number. Birds with more fledged young experienced increased telomere attrition. We show that telomere attrition rate, but not telomere length, is related to individual fitness and suggest that telomere dynamics may underlie reproductive costs experienced by animals as a consequence of prioritizing their lifetime fitness. This is the first study, to our knowledge, to provide evidence that more pronounced telomere erosion is associated with higher fitness gain.

  • 1054.
    Sudyka, Joanna
    et al.
    Univ Warsaw, Ctr New Technol, Banacha 2c, PL-02097 Warsaw, Poland;Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Podmokla, Edyta
    Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Drobniak, Szymon M.
    Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Dubiec, Anna
    Polish Acad Sci, Museum & Inst Zool, Ul Wilcza 64, PL-00679 Warsaw, Poland.
    Arct, Aneta
    Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Cichon, Mariusz
    Jagiellonian Univ, Inst Environm Sci, Gronostajowa 7, PL-30387 Krakow, Poland.
    Sex-specific effects of parasites on telomere dynamics in a short-lived passerinethe blue tit2019In: The Science of Nature: Naturwissenschaften, ISSN 0028-1042, E-ISSN 1432-1904, Vol. 106, no 1-2, article id 6Article in journal (Refereed)
    Abstract [en]

    Parasitic infections potentially drive host's life-histories since they can have detrimental effects on host's fitness. Telomere dynamics is a candidate mechanism to underlie life-history trade-offs and as such may correlate with observed fitness reduction in infected animals. We examined the relationship of chronic infection with two genera of haemosporidians causing avian malaria and malaria-like disease with host's telomere length (TL) in a longitudinal study of free-ranging blue tits. The observed overall infection prevalence was 80% and increased with age, constituting a potentially serious selective pressure in our population. We found longer telomeres in individuals infected with a parasite causing lesser blood pathologies i.e. Haemoproteus compared to Plasmodium genus, but this only held true among males. Female TL was independent of the infection type. Our results indicate that parasitic infections could bring about other types of costs to females than to males with respect to TL. Additionally, we detected linear telomere loss with age, however a random regression analysis did not confirm significant heterogeneity in TL of first breeders and telomere shortening rates in further life.

  • 1055.
    Suh, Alexander
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Genome Size Evolution: Small Transposons with Large Consequences2019In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 29, no 7, p. R241-R243Article in journal (Refereed)
    Abstract [en]

    Transposable elements (TEs) heavily influence genome size variation between organisms. A new study on larvacean tunicates now shows that even non-autonomous TEs - small TEs that parasitize the enzymatic machinery of large, autonomous TEs - can have a large impact on genome size.

  • 1056.
    Suh, Alexander
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    The phylogenomic forest of bird trees contains a hard polytomy at the root of Neoaves2016In: Zoologica Scripta, ISSN 0300-3256, E-ISSN 1463-6409, Vol. 45, p. 50-62Article, review/survey (Refereed)
    Abstract [en]

    Birds have arguably been the most intensely studied animal group for their phylogenetic relationships. However, the recent advent of genome-scale phylogenomics has made the forest of bird phylogenies even more complex and confusing. Here, in this perspective piece, I show that most parts of the avian Tree of Life are now firmly established as reproducible phylogenetic hypotheses. This is to the exception of the deepest relationships among Neoaves. Using phylogenetic networks and simulations, I argue that the very onset of the super-rapid neoavian radiation is irresolvable because of eight near-simultaneous speciation events. Such a hard polytomy of nine taxa translates into 2 027 025 possible rooted bifurcating trees. Accordingly, recent genome-scale phylogenies show extremely complex conflicts in this (and only this) part of the avian Tree of Life. I predict that the upcoming years of avian phylogenomics will witness many more, highly conflicting tree topologies regarding the early neoavian polytomy. I further caution against bootstrapping in the era of genomics and suggest to instead use reproducibility (e.g. independent methods or data types) as support for phylogenetic hypotheses. The early neoavian polytomy coincides with the Cretaceous-Paleogene (K-Pg) mass extinction and is, to my knowledge, the first empirical example of a hard polytomy.

  • 1057.
    Suh, Alexander
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    The Specific Requirements for CR1 Retrotransposition Explain the Scarcity of Retrogenes in Birds2015In: Journal of Molecular Evolution, ISSN 0022-2844, E-ISSN 1432-1432, Vol. 81, no 1-2, p. 18-20Article in journal (Refereed)
    Abstract [en]

    Chicken repeat 1 (CR1) retroposons are the most abundant superfamily of transposable elements in the genomes of birds, crocodilians, and turtles. However, CR1 mobilization remains poorly understood. In this article, I document that the diverse CR1 lineages of land vertebrates share a highly conserved hairpin structure and an octamer microsatellite motif at their very 3' ends. Together with the presence of these same motifs in the tails of CR1-mobilized short interspersed elements, this suggests that the minimum requirement for CR1 transcript recognition and retrotransposition is a complex > 50-nt structure. Such a highly specific recognition sequence readily explains why CR1-dominated genomes generally contain very few retrogenes. Conversely, the mammalian richness in retrogenes results from CR1 extinction in their early evolution and subsequent establishment of L1 dominance.

  • 1058.
    Suh, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. University of Münster, Institute of Experimental Pathology (ZMBE).
    Bachg, Sandra
    University of Münster, Institute of Experimental Pathology (ZMBE).
    Donnellan, Stephen
    South Australian Museum, Adelaide; The University of Adelaide, School of Biological Sciences.
    Joseph, Leo
    National Research Collections Australia, CSIRO, Australian National Wildlife Collection.
    Brosius, Jürgen
    University of Münster, Institute of Experimental Pathology (ZMBE); Brandenburg Medical School (MHB).
    Kriegs, Jan Ole
    University of Münster, Institute of Experimental Pathology (ZMBE); Westfälisches Landesmuseum mit Planetarium, LWL-Museum für Naturkunde.
    Schmitz, Jürgen
    University of Münster, Institute of Experimental Pathology (ZMBE).
    De-novo emergence of SINE retroposons during the early evolution of passerine birds2017In: Mobile DNA, ISSN 1759-8753, E-ISSN 1759-8753, Vol. 8, article id 21Article in journal (Refereed)
    Abstract [en]

    Background: Passeriformes ("perching birds" or passerines) make up more than half of all extant bird species. The genome of the zebra finch, a passerine model organism for vocal learning, was noted previously to contain thousands of short interspersed elements (SINEs), a group of retroposons that is abundant in mammalian genomes but considered largely inactive in avian genomes.

    Results: Here we resolve the deep phylogenetic relationships of passerines using presence/absence patterns of SINEs. The resultant retroposon-based phylogeny provides a powerful and independent corroboration of previous sequence-based analyses. Notably, SINE activity began in the common ancestor of Eupasseres (passerines excluding the New Zealand wrens Acanthisittidae) and ceased before the rapid diversification of oscine passerines (suborder Passeri - songbirds). Furthermore, we find evidence for very recent SINE activity within suboscine passerines (suborder Tyranni), following the emergence of a SINE via acquisition of a different tRNA head as we suggest through template switching.

    Conclusions: We propose that the early evolution of passerines was unusual among birds in that it was accompanied by de-novo emergence and activity of SINEs. Their genomic and transcriptomic impact warrants further study in the light of the massive diversification of passerines.

  • 1059.
    Suh, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Churakov, Gennady
    Ramakodi, Meganathan P.
    Platt, Roy N., II
    Jurka, Jerzy
    Kojima, Kenji K.
    Caballero, Juan
    Smit, Arian F.
    Vliet, Kent A.
    Hoffmann, Federico G.
    Brosius, Juergen
    Green, Richard E.
    Braun, Edward L.
    Ray, David A.
    Schmitz, Juergen
    Multiple Lineages of Ancient CR1 Retroposons Shaped the Early Genome Evolution of Amniotes2015In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 7, no 1, p. 205-217Article in journal (Refereed)
    Abstract [en]

    Chicken repeat 1 (CR1) retroposons are long interspersed elements (LINEs) that are ubiquitous within amniote genomes and constitute the most abundant family of transposed elements in birds, crocodilians, turtles, and snakes. They are also present in mammalian genomes, where they reside as numerous relics of ancient retroposition events. Yet, despite their relevance for understanding amniote genome evolution, the diversity and evolution of CR1 elements has never been studied on an amniote-wide level. We reconstruct the temporal and quantitative activity of CR1 subfamilies via presence/absence analyses across crocodilian phylogeny and comparative analyses of 12 crocodilian genomes, revealing relative genomic stasis of retroposition during genome evolution of extant Crocodylia. Our large-scale phylogenetic analysis of amniote CR1 subfamilies suggests the presence of at least seven ancient CR1 lineages in the amniote ancestor; and amniote-wide analyses of CR1 successions and quantities reveal differential retention (presence of ancient relics or recent activity) of these CR1 lineages across amniote genome evolution. Interestingly, birds and lepidosaurs retained the fewest ancient CR1 lineages among amniotes and also exhibit smaller genome sizes. Our study is the first to analyze CR1 evolution in a genome-wide and amniote-wide context and the data strongly suggest that the ancestral amniote genome contained myriad CR1 elements from multiple ancient lineages, and remnants of these are still detectable in the relatively stable genomes of crocodilians and turtles. Early mammalian genome evolution was thus characterized by a drastic shift from CR1 prevalence to dominance and hyperactivity of L2 LINEs in monotremes and L1 LINEs in therians.

  • 1060.
    Suh, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Smeds, Linnea
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Abundant recent activity of retrovirus-like retrotransposons within and among flycatcher species implies a rich source of structural variation in songbird genomes2018In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, no 1, p. 99-111Article in journal (Refereed)
    Abstract [en]

    Transposable elements (TEs) are genomic parasites capable of inserting virtually anywhere in the host genome, with manifold consequences for gene expression, DNA methylation and genomic stability. Notably, they can contribute to phenotypic variation and hence be associated with, for example, local adaptation and speciation. However, some organisms such as birds have been widely noted for the low densities of TEs in their genomes and this has been attributed to a potential dearth in transposition during their evolution. Here, we show that avian evolution witnessed diverse and abundant transposition on very recent timescales. First, we made an in-depth repeat annotation of the collared flycatcher genome, including identification of 23 new, retrovirus-like LTR retrotransposon families. Then, using whole-genome resequencing data from 200 Ficedula flycatchers, we detected 11,888 polymorphic TE insertions (TE presence/absence variations, TEVs) that segregated within and among species. The density of TEVs was one every 1.5-2.5Mb per individual, with heterozygosities of 0.12-0.16. The majority of TEVs belonged to some 10 different LTR families, most of which are specific to the flycatcher lineage. TEVs were validated by tracing the segregation of hundreds of TEVs across a three-generation pedigree of collared flycatchers and also by their utility as markers recapitulating the phylogenetic relationships among flycatcher species. Our results suggest frequent germline invasions of songbird genomes by novel retroviruses as a rich source of structural variation, which may have had underappreciated phenotypic consequences for the diversification of this species-rich group of birds.

  • 1061.
    Suh, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Smeds, Linnea
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    The Dynamics of Incomplete Lineage Sorting across the Ancient Adaptive Radiation of Neoavian Birds2015In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 13, no 8, article id e1002224Article in journal (Refereed)
    Abstract [en]

    The diversification of neoavian birds is one of the most rapid adaptive radiations of extant organisms. Recent whole-genome sequence analyses have much improved the resolution of the neoavian radiation and suggest concurrence with the Cretaceous-Paleogene (K-Pg) boundary, yet the causes of the remaining genome-level irresolvabilities appear unclear. Here we show that genome-level analyses of 2,118 retrotransposon presence/absence markers converge at a largely consistent Neoaves phylogeny and detect a highly differential temporal prevalence of incomplete lineage sorting (ILS), i.e., the persistence of ancestral genetic variation as polymorphisms during speciation events. We found that ILS-derived incongruences are spread over the genome and involve 35% and 34% of the analyzed loci on the autosomes and the Z chromosome, respectively. Surprisingly, Neoaves diversification comprises three adaptive radiations, an initial near-K-Pg super-radiation with highly discordant phylogenetic signals from near-simultaneous speciation events, followed by two post-K-Pg radiations of core landbirds and core waterbirds with much less pronounced ILS. We provide evidence that, given the extreme level of up to 100% ILS per branch in super-radiations, particularly rapid speciation events may neither resemble a fully bifurcating tree nor are they resolvable as such. As a consequence, their complex demographic history is more accurately represented as local networks within a species tree.

  • 1062.
    Suh, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Witt, Christopher C.
    Univ New Mexico, Dept Biol, Albuquerque, NM 87131 USA.;Univ New Mexico, Museum Southwestern Biol, Albuquerque, NM 87131 USA..
    Menger, Juliana
    UFZ Helmholtz Ctr Environm Res, Dept Conservat Biol, D-04318 Leipzig, Germany.;Univ Leipzig, Inst Biol, Mol Evolut & Systemat Anim, D-04103 Leipzig, Germany.;INPA, BR-69067375 Manaus, Amazonas, Brazil..
    Sadanandan, Keren R.
    Natl Univ Singapore, Dept Biol Sci, Singapore 117543, Singapore..
    Podsiadlowski, Lars
    Univ Bonn, Inst Evolutionary Biol & Ecol, D-53121 Bonn, Germany..
    Gerth, Michael
    Univ Leipzig, Inst Biol, Mol Evolut & Systemat Anim, D-04103 Leipzig, Germany.;Univ Liverpool, Inst Integrat Biol, Liverpool L69 7ZB, Merseyside, England..
    Weigert, Anne
    Univ Leipzig, Inst Biol, Mol Evolut & Systemat Anim, D-04103 Leipzig, Germany.;Max Planck Inst Evolutionary Anthropol, D-04103 Leipzig, Germany..
    McGuire, Jimmy A.
    Univ Calif Berkeley, Museum Vertebrate Zool, Berkeley, CA 94720 USA.;Univ Calif Berkeley, Dept Integrat Biol, Berkeley, CA 94720 USA..
    Mudge, Joann
    Natl Ctr Genome Resources, Santa Fe, NM 87505 USA..
    Edwards, Scott V.
    Harvard Univ, Dept Organism & Evolutionary Biol, Cambridge, MA 02138 USA..
    Rheindt, Frank E.
    Natl Univ Singapore, Dept Biol Sci, Singapore 117543, Singapore..
    Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes2016In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 7, article id 11396Article in journal (Refereed)
    Abstract [en]

    Parasite host switches may trigger disease emergence, but prehistoric host ranges are often unknowable. Lymphatic filariasis and loiasis are major human diseases caused by the insect-borne filarial nematodes Brugia, Wuchereria and Loa. Here we show that the genomes of these nematodes and seven tropical bird lineages exclusively share a novel retrotransposon, AviRTE, resulting from horizontal transfer (HT). AviRTE subfamilies exhibit 83-99% nucleotide identity between genomes, and their phylogenetic distribution, paleobiogeography and invasion times suggest that HTs involved filarial nematodes. The HTs between bird and nematode genomes took place in two pantropical waves, >25-22 million years ago (Myr ago) involving the Brugia/Wuchereria lineage and >20-17 Myr ago involving the Loa lineage. Contrary to the expectation from the mammal-dominated host range of filarial nematodes, we hypothesize that these major human pathogens may have independently evolved from bird endoparasites that formerly infected the global breadth of avian biodiversity.

  • 1063.
    Sulej, Tomasz
    et al.
    PAS, Inst Paleobiol, Twarda 51-55, PL-00818 Warsaw, Poland.
    Niedzwiedzki, Grzegorz
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    An elephant-sized Late Triassic synapsid with erect limbs2019In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 363, no 6422, p. 78-80Article in journal (Refereed)
    Abstract [en]

    Here, we describe the dicynodont Lisowicia bojani, from the Late Triassic of Poland, a gigantic synapsid with seemingly upright subcursorial limbs that reached an estimated length of more than 4.5 meters, height of 2.6 meters, and body mass of 9 tons. Lisowicia is the youngest undisputed dicynodont and the largest nondinosaurian terrestrial tetrapod from the Triassic. The lack of lines of arrested growth and the highly remodeled cortex of its limb bones suggest permanently rapid growth and recalls that of dinosaurs and mammals. The discovery of Lisowicia overturns the established picture of the Triassic megaherbivore radiation as a phenomenon restricted to dinosaurs and shows that stem-group mammals were capable of reaching body sizes that were not attained again in mammalian evolution until the latest Eocene.

  • 1064.
    Sun, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Genome Evolution of Neurospora tetrasperma2013Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    In this thesis work, I have used a comparative genomics approach to study a fungal model organism, Neurospora tetrasperma. My specific focus has been on genomic introgression, intron evolution, chromosomal structural rearrangements and codon usage. All of the studies are based on large-scale dataset generated by next-generation sequencing technology (NGS), combined with other techniques, such as Optical Mapping. In the introgression study, we detected large-scale introgression tracts in three N. tetrasperma lineages, and the introgression showed allele-specific and chromosomal-specific pattern. In the study of introns, we found indications of mRNA mediated intron loss and non-homologous end joining (NHEJ) mediated intron gains in N. tetrasperma. We found that selection is involved in shaping intron gains and losses, and associated with intron position, intron phase and GC content. In the study of chromosomal structural rearrangements, we found a lineage specific chromosomal inversion pattern in N. tetrasperma, which indicates that inversions are unlikely to associate with the origin of the suppressed recombination and the mating system transition in N. tetrasperma. The result suggests inversions are the consequences, rather than the causes, of suppressed recombination on the mating-type chromosome of N. tetrasperma. In the final study, analyses of codon usage indicated that the region of suppressed recombination in N. tetrasperma is subjected to genomic degeneration, and selection efficiency has been much reduced in this region.

    List of papers
    1. Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma
    Open this publication in new window or tab >>Large-Scale Introgression Shapes the Evolution of the Mating-Type Chromosomes of the Filamentous Ascomycete Neurospora tetrasperma
    Show others...
    2012 (English)In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 8, no 7, p. e1002820-Article in journal (Refereed) Published
    Abstract [en]

    The significance of introgression as an evolutionary force shaping natural populations is well established, especially in animal and plant systems. However, the abundance and size of introgression tracts, and to what degree interspecific gene flow is the result of adaptive processes, are largely unknown. In this study, we present medium coverage genomic data from species of the filamentous ascomycete Neurospora, and we use comparative genomics to investigate the introgression landscape at the genomic level in this model genus. We revealed one large introgression tract in each of the three investigated phylogenetic lineages of Neurospora tetrasperma (sizes of 5.6 Mbp, 5.2 Mbp, and 4.1 Mbp, respectively). The tract is located on the chromosome containing the locus conferring sexual identity, the mating-type (mat) chromosome. The region of introgression is confined to the region of suppressed recombination and is found on one of the two mat chromosomes (mat a). We used Bayesian concordance analyses to exclude incomplete lineage sorting as the cause for the observed pattern, and multilocus genealogies from additional species of Neurospora show that the introgression likely originates from two closely related, freely recombining, heterothallic species (N. hispaniola and N. crassa/N. perkinsii). Finally, we investigated patterns of molecular evolution of the mat chromosome in Neurospora, and we show that introgression is correlated with reduced level of molecular degeneration, consistent with a shorter time of recombination suppression. The chromosome specific (mat) and allele specific (mat a) introgression reported herein comprise the largest introgression tracts reported to date from natural populations. Furthermore, our data contradicts theoretical predictions that introgression should be less likely on sex-determining chromosomes. Taken together, the data presented herein advance our general understanding of introgression as a force shaping eukaryotic genomes.

    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-181143 (URN)10.1371/journal.pgen.1002820 (DOI)000306840400034 ()
    Available from: 2012-09-18 Created: 2012-09-17 Last updated: 2017-12-07Bibliographically approved
    2. Intron Evolution in Neurospora: the role of mutational bias and selection
    Open this publication in new window or tab >>Intron Evolution in Neurospora: the role of mutational bias and selection
    2015 (English)In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 25, no 1, p. 100-110Article in journal (Refereed) Published
    Abstract [en]

    We used comparative and population genomics to study intron evolutionary dynamics in the fungal model genus Neurospora. For our investigation, we used well-annotated genomes of N. crassa, N. discreta, and N. tetrasperma, and 92 resequenced genomes of N. tetrasperma from natural populations. By analyzing the four well-annotated genomes, we identified 9495 intron sites in 7619 orthologous genes. Our data supports nonhomologous end joining (NHEJ) and tandem duplication as mechanisms for intron gains in the genus and the RT-mRNA process as a mechanism for intron loss. We found a moderate intron gain rate (5.78-6.89x10(-13) intron gains per nucleotide site per year) and a high intron loss rate (7.53-13.76x10(-10) intron losses per intron sites per year) as compared to other eukaryotes. The derived intron gains and losses are skewed to high frequencies, relative to neutral SNPs, in natural populations of N. tetrasperma, suggesting that selection is involved in maintaining a high intron turnover. Furthermore, our analyses of the association between intron population-level frequency and genomic features suggest that selection is involved in shaping a 5' intron position bias and a low intron GC content. However, intron sequence analyses suggest that the gained introns were not exposed to recent selective sweeps. Taken together, this work contributes to our understanding of the importance of mutational bias and selection in shaping the intron distribution in eukaryotic genomes.

    National Category
    Evolutionary Biology Genetics
    Research subject
    Biology with specialization in Evolutionary Genetics
    Identifiers
    urn:nbn:se:uu:diva-207325 (URN)10.1101/gr.175653.114 (DOI)000347373200009 ()25342722 (PubMedID)
    Available from: 2013-09-12 Created: 2013-09-12 Last updated: 2017-12-06Bibliographically approved
    3. Lineage-specific chromosomal inversions in Neurospora tetrasperma
    Open this publication in new window or tab >>Lineage-specific chromosomal inversions in Neurospora tetrasperma
    Show others...
    (English)Manuscript (preprint) (Other academic)
    National Category
    Evolutionary Biology Genetics
    Research subject
    Biology with specialization in Evolutionary Genetics
    Identifiers
    urn:nbn:se:uu:diva-207328 (URN)
    Available from: 2013-09-12 Created: 2013-09-12 Last updated: 2014-01-23
    4. Degeneration in Codon Usage within the Region of Suppressed Recombination in the Mating-Type Chromosomes of Neurospora tetrasperma
    Open this publication in new window or tab >>Degeneration in Codon Usage within the Region of Suppressed Recombination in the Mating-Type Chromosomes of Neurospora tetrasperma
    2011 (English)In: Eukaryotic Cell, ISSN 1535-9778, E-ISSN 1535-9786, Vol. 10, no 4, p. 594-603Article in journal (Refereed) Published
    Abstract [en]

    The origin and early evolution of sex chromosomes are currently poorly understood. The Neurospora tetrasperma mating-type (mat) chromosomes have recently emerged as a model system for the study of early sex chromosome evolution, since they contain a young (< 6 million years ago [Mya]), large (> 6.6-Mb) region of suppressed recombination. Here we examined preferred-codon usage in 290 genes (121,831 codon positions) in order to test for early signs of genomic degeneration in N. tetrasperma mat chromosomes. We report several key findings about codon usage in the region of recombination suppression, including the following: (i) this region has been subjected to marked and largely independent degeneration among gene alleles; (ii) the level of degeneration is magnified over longer periods of recombination suppression; and (iii) both mat a and mat A chromosomes have been subjected to deterioration. The frequency of shifts from preferred codons to nonpreferred codons is greater for shorter genes than for longer genes, suggesting that short genes play an especially significant role in early sex chromosome evolution. Furthermore, we show that these degenerative changes in codon usage are best explained by altered selection efficiency in the recombinationally suppressed region. These findings demonstrate that the fungus N. tetrasperma provides an effective system for the study of degenerative genomic changes in young regions of recombination suppression in sex-regulating chromosomes.

    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-152908 (URN)10.1128/EC.00284-10 (DOI)000289408900015 ()21335530 (PubMedID)
    Available from: 2011-05-03 Created: 2011-05-03 Last updated: 2017-12-11Bibliographically approved
  • 1065.
    Sun, Yu
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Corcoran, Pádraic
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Åslin, Matilda
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Lao, Zhiqin
    Beijing Genomic Institute.
    Li, Li
    Beijing Genomic Institute.
    Wang, Weilin
    Beijing Genomic Institute.
    Andersson, Siv
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Lineage-specific chromosomal inversions in Neurospora tetraspermaManuscript (preprint) (Other academic)
  • 1066.
    Sun, Yu
    et al.
    South China Agr Univ, Coll Life Sci, Guangdong Prov Key Lab Prot Funct & Regulat Agr O, Guangzhou 510642, Guangdong, Peoples R China..
    Svedberg, Jesper
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Hiltunen, Markus
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Corcoran, Padraic
    Univ Sheffield, Dept Anim & Plant Sci, Sheffield S10 2TN, S Yorkshire, England..
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Large-scale suppression of recombination predates genomic rearrangements in Neurospora tetrasperma2017In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 8, article id 1140Article in journal (Refereed)
    Abstract [en]

    A common feature of eukaryote genomes is large chromosomal regions where recombination is absent or strongly reduced, but the factors that cause this reduction are not well understood. Genomic rearrangements have often been implicated, but they may also be a consequence of recombination suppression rather than a cause. In this study, we generate eight high-quality genomic data sets of the filamentous ascomycete Neurospora tetrasperma, a fungus that lacks recombination over most of its largest chromosome. The genomes surprisingly reveal collinearity of the non-recombining regions and although large inversions are enriched in these regions, we conclude these inversions to be derived and not the cause of the suppression. To our knowledge, this is the first time that non-recombining, genic regions as large as 86% of a full chromosome (or 8 Mbp), are shown to be collinear. These findings are of significant interest for our understanding of the evolution of sex chromosomes and other supergene complexes.

  • 1067. Sun, Yu
    et al.
    Svedberg, Jesper
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Hiltunen, Markus
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Corcoran, Pádraic
    Johannesson, Hanna
    Large-scale suppression of recombination predates genomic rearrangements in Neurospora tetrasperma2017In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723Article in journal (Refereed)
    Abstract [en]

    A common feature of eukaryote genomes is large chromosomal regions where recombination is absent or strongly reduced, but the factors that cause this reduction are not well understood. Genomic rearrangements have often been implicated, but they may also be a consequence of recombination suppression rather than a cause. In this study, we generate eight high-quality genomic datasets of N. tetrasperma, a fungus that lacks recombination over most of its largest chromosome. The genomes surprisingly reveal collinearity of the non-recombining regions and although large inversions are enriched in these regions, we conclude these inversions to be derived and not the cause of the suppression. To our knowledge, this is the first time that non-recombining, genic regions as large as 86% of a full chromosome (or 8 Mbp), are shown to be collinear. These findings are of significant interest for our understanding of the evolution of sex chromosomes and other supergene complexes.

  • 1068.
    Sun, Yu
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Tamarit, Daniel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Andersson, Siv
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Switches in Genomic GC Content Drive Shifts of Optimal Codons under Sustained Selection on Synonymous Sites2017In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 9, no 10, p. 2560-2579Article in journal (Refereed)
    Abstract [en]

    The major codon preference model suggests that codons read by tRNAs in high concentrations are preferentially utilized in highly expressed genes. However, the identity of the optimal codons differs between species although the forces driving such changes are poorly understood. We suggest that these questions can be tackled by placing codon usage studies in a phylogenetic framework and that bacterial genomes with extreme nucleotide composition biases provide informative model systems. Switches in the background substitution biases from GC to AT have occurred in Gardnerella vaginalis (GC = 32%), and from AT to GC in Lactobacillus delbrueckii (GC=62%) and Lactobacillus fermentum (GC = 63%). We show that despite the large effects on codon usage patterns by these switches, all three species evolve under selection on synonymous sites. In G. vaginalis, the dramatic codon frequency changes coincide with shifts of optimal codons. In contrast, the optimal codons have not shifted in the two Lactobacillus genomes despite an increased fraction of GC-ending codons. We suggest that all three species are in different phases of an on-going shift of optimal codons, and attribute the difference to a stronger background substitution bias and/or longer time since the switch in G. vaginalis. We show that comparative and correlative methods for optimal codon identification yield conflicting results for genomes in flux and discuss possible reasons for the mispredictions. We conclude that switches in the direction of the background substitution biases can drive major shifts in codon preference patterns even under sustained selection on synonymous codon sites.

  • 1069.
    Sun, Yu
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Whittle, Carrie-Ann
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Corcoran, Pádraic
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Intron Evolution in Neurospora: the role of mutational bias and selection2015In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 25, no 1, p. 100-110Article in journal (Refereed)
    Abstract [en]

    We used comparative and population genomics to study intron evolutionary dynamics in the fungal model genus Neurospora. For our investigation, we used well-annotated genomes of N. crassa, N. discreta, and N. tetrasperma, and 92 resequenced genomes of N. tetrasperma from natural populations. By analyzing the four well-annotated genomes, we identified 9495 intron sites in 7619 orthologous genes. Our data supports nonhomologous end joining (NHEJ) and tandem duplication as mechanisms for intron gains in the genus and the RT-mRNA process as a mechanism for intron loss. We found a moderate intron gain rate (5.78-6.89x10(-13) intron gains per nucleotide site per year) and a high intron loss rate (7.53-13.76x10(-10) intron losses per intron sites per year) as compared to other eukaryotes. The derived intron gains and losses are skewed to high frequencies, relative to neutral SNPs, in natural populations of N. tetrasperma, suggesting that selection is involved in maintaining a high intron turnover. Furthermore, our analyses of the association between intron population-level frequency and genomic features suggest that selection is involved in shaping a 5' intron position bias and a low intron GC content. However, intron sequence analyses suggest that the gained introns were not exposed to recent selective sweeps. Taken together, this work contributes to our understanding of the importance of mutational bias and selection in shaping the intron distribution in eukaryotic genomes.

  • 1070.
    Sundberg, Henrik
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Contributions to the understanding of diversity and evolution in the genus Coreomyces2018Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    The Laboulbeniales is an order of enigmatic ascomycete fungi that are obligate microscopic parasites of arthropods, which are usually non-detrimental. They typically display a high degree of host specificity, and the genus Coreomyces, which is the recurring theme of this thesis, is no exception. Coreomyces is a small aquatic genus parasitising water boatmen (Corixidae). Members in this genus present something that is unique for Laboulbeniales, position specificity. This means that a parasite is restricted to a specific position on the host. This thesis aims at elucidating the patterns of host and position specificity present in the genus Coreomyces by the use of molecular markers. A second aim is to describe new taxa encountered during the course of the project. Finally we wanted to reveal what mating system is present in a member of the Laboulbeniales, something that has never been done before. Understanding the mode of sexual reproduction and to get insights into mating type organisation can give important clues to how the species patterns we observe may have evolved. To achieve these goals we first had to develop a robust and simple molecular methodology that made use of as little material as possible, preferably a single thallus. Our results showed that position specificity indeed exists in this genus, but that it is not as strict as previously presumed, all species we analysed occupied more than one position. Further we were able to show that thalli found in the same position on different hosts constitute the same species, and also that two sister species utilise the same position. We conclude that, in most cases, growth position is more important than host species or host sex in species delimitation. We confirmed the presence of four discrete taxa, two of which were described as new species, Coreomyces confusus H. Sundb. et al. and C. dextrorsus H. Sundb. et al. Finally we were able to show that C. macropus and C. confusus are likely to display a homothallic breeding system.

    List of papers
    1. A crush on small fungi: An efficient and quick method for obtaining DNA from minute ascomycetes
    Open this publication in new window or tab >>A crush on small fungi: An efficient and quick method for obtaining DNA from minute ascomycetes
    2018 (English)In: Methods in Ecology and Evolution, ISSN 2041-210X, E-ISSN 2041-210X, Vol. 9, no 1, p. 148-158Article in journal (Refereed) Published
    Abstract [en]

    We have developed a reliable technique for extracting DNA from single microscopic fungal thalli, including efficient cell disruption and transfer of cell content for subsequent polymerase chain reaction (PCR). The technique was primarily developed for members of the ascomycete order Laboulbeniales, which are minute fungi with tough cell walls that are exceedingly difficult to disrupt with standard extraction techniques. Our method makes routine amplification of DNA from single thalli possible, even from small species or poorly developed individuals. DNA release is accomplished in an entirely mechanical manner using an arbor press fitted with custom-made components. This approach has eliminated additional treatment such as laborious freeze-thaw cycles, enzymes, or lysing agents. The overall PCR success rate of 89% is comparable to or better than alternative protocols that make use of substantially larger amounts of fungal tissue. From 97% of the successful PCRs a total of 156 sequences from four gene regions were produced. Being able to restrict DNA extractions to a single thallus is critical to all genetic studies requiring data at the level of individual, e.g. population genetics. As all researchers working with minute uncultivable organisms in many respects face the same problems (effective handling of the material, small quantities of DNA etc.), the methodology described here has a potential to be widely applicable. Necessary custom-made components can be manufactured at fairly low cost by any precision-tool workshop using our detail drawings.

    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-334516 (URN)10.1111/2041-210X.12850 (DOI)000419821200015 ()
    Funder
    Helge Ax:son Johnsons stiftelse
    Available from: 2017-11-23 Created: 2017-11-23 Last updated: 2018-08-16Bibliographically approved
    2. Position specificity in the genus Coreomyces (Laboulbeniomycetes, Ascomycota)
    Open this publication in new window or tab >>Position specificity in the genus Coreomyces (Laboulbeniomycetes, Ascomycota)
    2018 (English)In: Fungal Systematics and Evolution, ISSN 2589-3823, Vol. 1, no 1, p. 217-228Article in journal (Refereed) Published
    Abstract [en]

    To study position specificity in the insect-parasitic fungal genus Coreomyces (Laboulbeniaceae, Laboulbeniales), we sampled corixid hosts (Corixidae, Heteroptera) in southern Scandinavia. We detected Coreomyces thalli in five different positions on the hosts. Thalli from the various positions grouped in four distinct clusters in the resulting gene trees, distinctly so in the ITS and LSU of the nuclear ribosomal DNA, less so in the SSU of the nuclear ribosomal DNA and the mitochondrial ribosomal DNA. Thalli from the left side of abdomen grouped in a single cluster, and so did thalli from the ventral right side. Thalli in the mid-ventral position turned out to be a mix of three clades, while thalli growing dorsally grouped with thalli from the left and right abdominal clades. The mid-ventral and dorsal positions were found in male hosts only. The position on the left hemelytron was shared by members from two sister clades. Statistical analyses demonstrate a significant positive correlation between clade and position on the host, but also a weak correlation between host sex and clade membership. These results indicate that sex-of-host specificity may be a non-existent extreme in a continuum, where instead weak preferences for one host sex may turn out to be frequent.

    Keywords
    CORIXIDAE, DNA, FUNGI, HOST-SPECIFICITY, INSECT, PHYLOGENY
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-357103 (URN)10.3114/fuse.2018.01.09 (DOI)
    Funder
    Helge Ax:son Johnsons stiftelse
    Available from: 2018-08-11 Created: 2018-08-11 Last updated: 2018-08-16Bibliographically approved
    3. Two new species in the genus Coreomyces Thaxt. from Europe
    Open this publication in new window or tab >>Two new species in the genus Coreomyces Thaxt. from Europe
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Coreomyces is a small insect-parasitic genus that belongs to the ascomycete order Laboulbeniales. In this study we describe two new species: Coreomyces confusus sp. nov and Coreomyces dextrorsum sp. nov. We have also found C. macropus Thaxt. and C. corixae Thaxt. Thalli congruent in both morphology and position on host integument with C. arcuatus sensu Majewski have been shown to be a morphotype of C. macropus. Infected corixids have been sampled from Sweden and Turkey. Our records have been verified with molecular data (ITS and nrLSU rDNA).

    National Category
    Biological Systematics
    Research subject
    Biology; Biology with specialization in Systematics
    Identifiers
    urn:nbn:se:uu:diva-357105 (URN)
    Available from: 2018-08-11 Created: 2018-08-11 Last updated: 2018-08-16
    4. Mating types in the genus Coreomyces
    Open this publication in new window or tab >>Mating types in the genus Coreomyces
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    The aim of this study was to uncover the mating system in members of the monoecious genus Coremyces (Laboulbeniales, Ascomycota). We retrieved genome sequences from five individuals using NGS methods and looked for mating type genes as well as flanking genes. The genomes represent two species, Coreomyces macropus Thaxt. (four genomes) and C. confusus H. Sundb. et al. (one genome). Our results indicate that the two species of Coreomyces are homothallic. We found both MAT1-1 and MAT1-2 in long scaffolds with high sequencing depth in four out of five genomes (MAT1-2 was not encountered in one of the genomes). The flanking SLA2 gene was observed in all five genomes, whereas APN2 was encountered only in two genomes of C. macropus. Homothallism, combined with the earlier observations that archegonia and antheridia appear in close physical proximity and that spermatia generally disperse only over very short distances, suggest that intrahaploid mating may be the norm in Coreomyces and confers an evolutionary advantage.

    Keywords
    Ascomycota, Fungi, Laboulbeniomycetes, MDA, reproduction, selfing, index switching
    National Category
    Evolutionary Biology Genetics
    Research subject
    Biology with specialization in Evolutionary Organismal Biology
    Identifiers
    urn:nbn:se:uu:diva-357108 (URN)
    Available from: 2018-08-11 Created: 2018-08-11 Last updated: 2018-08-16
  • 1071.
    Sundberg, Henrik
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Kruys, Åsa
    Uppsala University, Music and Museums, Museum of Evolution.
    Bergsten, Johannes
    Naturhistoriska riksmuseet.
    Ekman, Stefan
    Uppsala University, Music and Museums, Museum of Evolution.
    Mating types in the genus CoreomycesManuscript (preprint) (Other academic)
    Abstract [en]

    The aim of this study was to uncover the mating system in members of the monoecious genus Coremyces (Laboulbeniales, Ascomycota). We retrieved genome sequences from five individuals using NGS methods and looked for mating type genes as well as flanking genes. The genomes represent two species, Coreomyces macropus Thaxt. (four genomes) and C. confusus H. Sundb. et al. (one genome). Our results indicate that the two species of Coreomyces are homothallic. We found both MAT1-1 and MAT1-2 in long scaffolds with high sequencing depth in four out of five genomes (MAT1-2 was not encountered in one of the genomes). The flanking SLA2 gene was observed in all five genomes, whereas APN2 was encountered only in two genomes of C. macropus. Homothallism, combined with the earlier observations that archegonia and antheridia appear in close physical proximity and that spermatia generally disperse only over very short distances, suggest that intrahaploid mating may be the norm in Coreomyces and confers an evolutionary advantage.

  • 1072.
    Sundberg, Henrik
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Kruys, Åsa
    Uppsala University, Music and Museums, Museum of Evolution.
    Bergsten, Johannes
    Naturhistoriska riksmuseet, Stockholm, Sweden.
    Ekman, Stefan
    Uppsala University, Music and Museums, Museum of Evolution.
    Position specificity in the genus Coreomyces (Laboulbeniomycetes, Ascomycota)2018In: Fungal Systematics and Evolution, ISSN 2589-3823, Vol. 1, no 1, p. 217-228Article in journal (Refereed)
    Abstract [en]

    To study position specificity in the insect-parasitic fungal genus Coreomyces (Laboulbeniaceae, Laboulbeniales), we sampled corixid hosts (Corixidae, Heteroptera) in southern Scandinavia. We detected Coreomyces thalli in five different positions on the hosts. Thalli from the various positions grouped in four distinct clusters in the resulting gene trees, distinctly so in the ITS and LSU of the nuclear ribosomal DNA, less so in the SSU of the nuclear ribosomal DNA and the mitochondrial ribosomal DNA. Thalli from the left side of abdomen grouped in a single cluster, and so did thalli from the ventral right side. Thalli in the mid-ventral position turned out to be a mix of three clades, while thalli growing dorsally grouped with thalli from the left and right abdominal clades. The mid-ventral and dorsal positions were found in male hosts only. The position on the left hemelytron was shared by members from two sister clades. Statistical analyses demonstrate a significant positive correlation between clade and position on the host, but also a weak correlation between host sex and clade membership. These results indicate that sex-of-host specificity may be a non-existent extreme in a continuum, where instead weak preferences for one host sex may turn out to be frequent.

  • 1073.
    Supraha, Luka
    Uppsala University, Disciplinary Domain of Science and Technology, Earth Sciences, Department of Earth Sciences, Palaeobiology.
    Phenotypic variation and adaptive strategies in calcifying marine phytoplankton (Coccolithophores)2015Licentiate thesis, comprehensive summary (Other academic)
    List of papers
    1. Eco-physiological adaptation shapes the response of calcifying algae to nutrient limitation
    Open this publication in new window or tab >>Eco-physiological adaptation shapes the response of calcifying algae to nutrient limitation
    2015 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 5, article id 16499Article in journal (Refereed) Published
    Abstract [en]

    The steady increase in global ocean temperature will most likely lead to nutrient limitation in the photic zone. This will impact the physiology of marine algae, including the globally important calcifying coccolithophores. Understanding their adaptive patterns is essential for modelling carbon production in a low-nutrient ocean. We investigated the physiology of Helicosphaera carteri, a representative of the abundant but under-investigated flagellated functional group of coccolithophores. Two strains isolated from contrasting nutrient regimes (South Atlantic and Mediterranean Sea) were grown in phosphorus-replete and phosphorus-limited batch cultures. While growing exponentially in a phosphorus-replete medium, the Mediterranean strain exhibited on average 24% lower growth rate, 36% larger coccosphere volume and 21% lower particulate inorganic carbon (PIC) production than the Atlantic strain. Under phosphorus limitation, the same strain was capable of reaching a 2.6 times higher cell density than the Atlantic strain due to lower phosphorus requirements. These results suggest that local physiological adaptation can define the performance of this species under nutrient limitation.

    National Category
    Ecology Cell Biology Evolutionary Biology Earth and Related Environmental Sciences
    Identifiers
    urn:nbn:se:uu:diva-253354 (URN)10.1038/srep16499 (DOI)000364487200001 ()26560531 (PubMedID)
    Funder
    Knut and Alice Wallenberg FoundationThe Royal Swedish Academy of Sciences
    Available from: 2015-05-26 Created: 2015-05-26 Last updated: 2017-12-04Bibliographically approved
    2. High temperature decreases the PIC/POC ratio and increases phosphorus requirements in Coccolithus pelagicus (Haptophyta)
    Open this publication in new window or tab >>High temperature decreases the PIC/POC ratio and increases phosphorus requirements in Coccolithus pelagicus (Haptophyta)
    Show others...
    2014 (English)In: Biogeosciences, ISSN 1726-4170, E-ISSN 1726-4189, Vol. 11, p. 3531-3545Article in journal (Refereed) Published
    Abstract [en]

    Rising ocean temperatures will likely increase stratification of the water column and reduce nutrient input into the photic zone. This will increase the likelihood of nutrient limitation in marine microalgae, leading to changes in the abundance and composition of phytoplankton communities, which in turn will affect global biogeochemical cycles. Calcifying algae, such as coccolithophores, influence the carbon cycle by fixing CO2 into particulate organic carbon through photosynthesis (POC production) and into particulate inorganic carbon through calcification (PIC production). As calcification produces a net release of CO2, the ratio of PIC to POC production determines whether coccolithophores act as a source (high PIC / POC) or a sink (low PIC / POC) of atmospheric CO2. We studied the effect of phosphorus (P-) limitation and high temperature on the physiology and the PIC / POC ratio of two subspecies of Coccolithus pelagicus. This large and heavily calcified species is a major contributor to calcite export from the photic zone into deep-sea reservoirs. Phosphorus limitation did not influence exponential growth rates in either subspecies, but P-limited cells had significantly lower cellular P-content. One of the subspecies was subjected to a 5 °C temperature increase from 10 °C to 15 °C, which did not affect exponential growth rates either, but nearly doubled cellular P-content under both high and low phosphate availability. This temperature increase reduced the PIC / POC ratio by 40–60%, whereas the PIC / POC ratio did not differ between P-limited and nutrient-replete cultures when the subspecies were grown near their respective isolation temperature. Both P-limitation and elevated temperature significantly increased coccolith malformations. Our results suggest that a temperature increase may intensify P-limitation due to a higher P-requirement to maintain growth and POC production rates, possibly reducing abundances in a warmer ocean. Under such a scenario C. pelagicus may decrease its calcification rate relative to photosynthesis, thus favouring CO2 sequestration over release. It seems unlikely that P-limitation by itself causes changes in the PIC / POC ratio in this species.

    Keywords
    coccolithophores, culture experiments, phosphate limitation, calcification
    National Category
    Natural Sciences
    Research subject
    Biology; Earth Science with specialization in Environmental Analysis
    Identifiers
    urn:nbn:se:uu:diva-220830 (URN)10.5194/bg-11-3531-2014 (DOI)000339265800008 ()
    Available from: 2014-03-20 Created: 2014-03-20 Last updated: 2017-12-05Bibliographically approved
    3. Observations on the life cycle and ecology of Acanthoica quattrospina Lohmann from a Mediterranean estuary
    Open this publication in new window or tab >>Observations on the life cycle and ecology of Acanthoica quattrospina Lohmann from a Mediterranean estuary
    2014 (English)In: Journal of Nannoplankton Research, ISSN 1210-8049, Vol. 34, no SI, p. 49-56Article in journal (Refereed) Published
    National Category
    Ecology Biological Systematics
    Identifiers
    urn:nbn:se:uu:diva-253353 (URN)
    Conference
    INA Workshop on Extant Coccolithophores research
    Available from: 2015-05-26 Created: 2015-05-26 Last updated: 2016-09-13Bibliographically approved
  • 1074.
    Supraha, Luka
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Earth Sciences, Department of Earth Sciences, Palaeobiology.
    Ljubesic, Zrinka
    Univ Zagreb, Fac Sci, Dept Biol, Rooseveltov Trg 6, Zagreb 10000, Croatia.
    Henderiks, Jorijntje
    Uppsala University, Disciplinary Domain of Science and Technology, Earth Sciences, Department of Earth Sciences, Palaeobiology. Univ Oslo, Dept Biosci, CEES, POB 1066, N-0316 Oslo, Norway.
    Combination coccospheres from the Eastern Adriatic coast: New, verified and possible life-cycle associations2018In: Marine Micropaleontology, ISSN 0377-8398, E-ISSN 1872-6186, Vol. 141, p. 23-30Article in journal (Refereed)
    Abstract [en]

    Coccolithophore life cycles involve the alternation between morphologically distinct life-cycle phases. This often leads to taxonomic issues where the life-cycle phases of the same species are described as distinct taxa. This issue can be resolved by the observation of combination coccospheres, i.e. cells bearing the coccoliths of both life-cycle phases. This study presents new observations on combination coccospheres from the highly diverse and ecologically important coccolithophore order Syracosphaerales and the genus Alisphaera. New life-cycle associations are revealed between Syracosphaera hirsuta and Corisphaera strigilis, and between Alisphaera unicornis and a nannolith-producing Polycrater galapagensis. The life-cycle association of Syracosphaera marginiporata Anthosphaera sp. type B is verified. A possible association between Rhabdosphaera xiphos and an unidentified holococcolith-bearing morphotype is proposed and needs to be verified in future investigations. The appropriate taxonomic revisions are conducted following the taxonomic principle of priority and recommended practices for naming the coccolithophore life-cycle phases.

  • 1075.
    Svanbäck, Richard
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Johansson, Frank
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Predation selects for smaller eye size in a vertebrate: effects of environmental conditions and sex2019In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 286, no 1897, article id 20182625Article in journal (Refereed)
    Abstract [en]

    Increased eye size in animals results in a larger retinal image and thus improves visual acuity. Thus, larger eyes should aid both in finding food as well as detecting predators. On the other hand, eyes are usually very conspicuous and several studies have suggested that eye size is associated with predation risk. However, experimental evidence is scant. In this study, we address how predation affects variation in eye size by performing two experiments using Eurasian perch juveniles as prey and either larger perch or pike as predators. First, we used large outdoor tanks to compare selection due to predators on relative eye size in open and artificial vegetated habitats. Second, we studied the effects of both predation risk and resource levels on phenotypic plasticity in relative eye size in indoor aquaria experiments. In the first experiment, we found that habitat altered selection due to predators, since predators selected for smaller eye size in a non-vegetated habitat, but not in a vegetated habitat. In the plasticity experiment, we found that fish predators induced smaller eye size in males, but not in females, while resource levels had no effect on eye size plasticity. Our experiments provide evidence that predation risk could be one of the driving factors behind variation in eye size within species.

  • 1076.
    Svanbäck, Richard
    et al.
    Biodiversity Research Centre and Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada.
    Schluter, Dolph
    Biodiversity Research Centre and Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada.
    Niche Specialization Influences Adaptive Phenotypic Plasticity in the Threespine Stickleback2012In: American Naturalist, ISSN 0003-0147, E-ISSN 1537-5323, Vol. 180, no 1, p. 50-59Article in journal (Refereed)
    Abstract [en]

    Phenotypic plasticity may be favored in generalist populations if it increases niche width, even in temporally constant environments. Phenotypic plasticity can increase the frequency of extreme phenotypes in a population and thus allow it to make use of a wide resource spectrum. Here we test the prediction that generalist populations should be more plastic than specialists. In a common-garden experiment, we show that solitary, generalist populations of threespine sticklebacks inhabiting small coastal lakes of British Columbia have a higher degree of morphological plasticity than the more specialized sympatric limnetic and benthic species. The ancestral marine stickleback showed low levels of plasticity similar to those of sympatric sticklebacks, implying that the greater plasticity of the generalist population has evolved recently. Measurements of wild populations show that those with mean trait values intermediate between the benthic and limnetic values indeed have higher morphological variation. Our data indicate that plasticity can evolve rapidly after colonization of a new environment in response to changing niche use.

  • 1077.
    Svedberg, Jesper
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Catching the Spore killers: Genomic conflict and genome evolution in Neurospora2017Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    A genome is shaped by many different forces. Recombination can for instance both create and maintain genetic diversity, but the need to locally reduce recombination rates will also leave specific signatures. Genetic elements can act selfishly and spreading at the expense of the rest of the genome can leave marks of their activity, as can mechanisms that suppresses them, in a phenomenon known as genomic conflict. In this thesis, I have studied the forces driving genome evolution, using modern genome sequencing techniques and with a special focus on a class of selfish genetic elements known as Spore killers found in the fungus Neurospora. First, we show novel findings on large-scale suppression of recombination by non-structural means in the N. tetrasperma genomes. In contrary, in the genomic region harbouring the spore killer elements Sk-2 and Sk-3 of N. intermedia, a dense set of inversions that are interspersed with transposable elements have accumulated. The inversions are unique for each killer type, showing that they have a long separated evolutionary history and likely have established themselves independently. For the Sk-2 haplotype, where we have polymorphism data, we see signs of relaxed selection, which is consistent with the hypothesis that recombination suppression reduces the efficacy of selection in this region. These results show the strong effects the divergent selective forces of genomic conflicts can have on chromosome architecture. Furthermore, we investigate the hypothesis that spore killing can drive reproductive isolation, by comparing the fertility of crosses between N. metzenbergii and either killer or non-killer N. intermedia strains. We show that crosses with spore killer strains have lower fertility, which cannot be explained by the killing itself, but is potentially caused by an incompatibility gene captured in the non-recombining region. Finally, we identified the genetic element responsible for causing spore killing in the Sk-1 spore killer strains found in N. sitophila. Unlike the Sk-2 and Sk-3 elements, Sk-1 is not connected to a large, non-recombining region, but is caused by a single locus, and we also find indications that this locus was introgressed from N. hispaniola.

    List of papers
    1. Large-scale suppression of recombination predates genomic rearrangements in Neurospora tetrasperma
    Open this publication in new window or tab >>Large-scale suppression of recombination predates genomic rearrangements in Neurospora tetrasperma
    Show others...
    2017 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723Article in journal (Refereed) In press
    Abstract [en]

    A common feature of eukaryote genomes is large chromosomal regions where recombination is absent or strongly reduced, but the factors that cause this reduction are not well understood. Genomic rearrangements have often been implicated, but they may also be a consequence of recombination suppression rather than a cause. In this study, we generate eight high-quality genomic datasets of N. tetrasperma, a fungus that lacks recombination over most of its largest chromosome. The genomes surprisingly reveal collinearity of the non-recombining regions and although large inversions are enriched in these regions, we conclude these inversions to be derived and not the cause of the suppression. To our knowledge, this is the first time that non-recombining, genic regions as large as 86% of a full chromosome (or 8 Mbp), are shown to be collinear. These findings are of significant interest for our understanding of the evolution of sex chromosomes and other supergene complexes.

    Keywords
    Genome evolution, recombination, suppression of recombination, inversions, Neurospora tetrasperma
    National Category
    Evolutionary Biology
    Research subject
    Biology with specialization in Evolutionary Genetics
    Identifiers
    urn:nbn:se:uu:diva-329496 (URN)
    Available from: 2017-09-17 Created: 2017-09-17 Last updated: 2017-11-29
    2. The effect of genomic conflict on genome evolution in Neurospora intermedia
    Open this publication in new window or tab >>The effect of genomic conflict on genome evolution in Neurospora intermedia
    Show others...
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Genomic conflicts are predicted to have a major influence on genome evolution, but empirical data is needed in order to confirm or refute this prediction. In this study, we used a genomic approach to address the influence of genomic conflicts, caused by selfish genetic elements, on genome evolution in the model fungus Neurospora intermedia. We gathered high-quality genomic data from sixteen strains of Neurospora by using the PacBio RSII long-read sequencing platform. Six of these strains carry the meiotic drive element Sk-2 or Sk-3, which are multigene systems of killer and resistance loci linked together in haplotypes. We show that in the N. intermedia genomes, in which an array of protective mechanisms act to limit the negative effects of selfish DNA, both the Sk-2 and Sk-3 haplotypes have accumulated a dense set of inversions that are interspersed with transposable elements. The inversions are unique for each killer type, showing that they have a long separated evolutionary history and likely have established themselves as meiotic drivers independently. For the Sk-2 haplotype, for which we have polymorphism-data, we see signs of relaxed selection, which is consistent with the hypothesis that recombination suppression reduces the efficacy of selection in this region. Thus, our data indicates that albeit N. intermedia possesses an active genome defence system, selfish genetic elements have worked in concert and significantly affected the evolutionary trajectory of chromosome 3 in this species.

    Keywords
    Genomics, genomic conflict, mieotic drive, spore killer, Neurospora
    National Category
    Evolutionary Biology
    Research subject
    Biology with specialization in Evolutionary Genetics
    Identifiers
    urn:nbn:se:uu:diva-329493 (URN)
    Available from: 2017-09-17 Created: 2017-09-17 Last updated: 2017-09-17
    3. A single gene causes meiotic drive in Neurospora sitophila
    Open this publication in new window or tab >>A single gene causes meiotic drive in Neurospora sitophila
    Show others...
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Meiotic drive in Neurospora was first identified in Neurospora sitophila over forty years ago. Since drive in this fungus results in “spore killing”, the drive was designated Sk-1. The locus responsible for killing has until now been unknown. Here we sequenced 56 N. sitophila strains from natural populations, using paired-end sequencing on the Illumina HiSeq platform, and used this population genomic data to identify a locus on chromosome VI that significantly associates with the killing phenotypewe have used Illumina technology to generate whole genome sequence data for 56 wild N. sitophila strains. Using a genome wide association test we have identified the locus responsible for the Sk-1 phenotype on chromosome VI. We call the locus nkl1. By using the PacBio RSII platform, we generated high quality genome assemblies of four N. sitophila strains (two Sk-1 killers and two sensitives) and verified that no structural rearrangements were found in this region or on other chromosomes. We verified by laboratory crosses that the allelic variants of nkl1 show segregation distortion, and generated deletion mutants to demonstrate that the locus is responsible both for killing and resistance. We show demonstrate that the element is likely to have been introgressed from the closely related species, N. hispaniola. We identified three subclades in N. sitophila is split up into three subclades, in one of which Sk-1 is fixed for Sk-1, one another where Sk-1 is absent, and a third where killers and sensitives appear to intermix. This indicates that Sk-1 is currently invading N. sitophila through matings between diverged lineages.

    Keywords
    Genomics, genomic conflict, mieotic drive, spore killer, Sk-1, Neurospora sitophila
    National Category
    Evolutionary Biology
    Research subject
    Biology with specialization in Evolutionary Genetics
    Identifiers
    urn:nbn:se:uu:diva-329494 (URN)
    Available from: 2017-09-17 Created: 2017-09-17 Last updated: 2017-09-17
    4. Meiotic drive is associated with reproductive isolation in Neurospora
    Open this publication in new window or tab >>Meiotic drive is associated with reproductive isolation in Neurospora
    (English)Manuscript (preprint) (Other academic)
    Keywords
    Genomic conflict, repoductive isolation, speciation, meiotic drive, spore killer, Neurospora
    National Category
    Evolutionary Biology
    Research subject
    Biology
    Identifiers
    urn:nbn:se:uu:diva-329495 (URN)
    Available from: 2017-09-17 Created: 2017-09-17 Last updated: 2017-09-17
  • 1078.
    Svedberg, Jesper
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Hosseini, Sara
    Chen, Jun
    Mozgova, Iva
    Hennig, Lars
    Manitchotpisit, Pennapa
    Hammond, Thomas M.
    Lascoux, Martin
    Johannesson, Hanna
    The effect of genomic conflict on genome evolution in Neurospora intermediaManuscript (preprint) (Other academic)
    Abstract [en]

    Genomic conflicts are predicted to have a major influence on genome evolution, but empirical data is needed in order to confirm or refute this prediction. In this study, we used a genomic approach to address the influence of genomic conflicts, caused by selfish genetic elements, on genome evolution in the model fungus Neurospora intermedia. We gathered high-quality genomic data from sixteen strains of Neurospora by using the PacBio RSII long-read sequencing platform. Six of these strains carry the meiotic drive element Sk-2 or Sk-3, which are multigene systems of killer and resistance loci linked together in haplotypes. We show that in the N. intermedia genomes, in which an array of protective mechanisms act to limit the negative effects of selfish DNA, both the Sk-2 and Sk-3 haplotypes have accumulated a dense set of inversions that are interspersed with transposable elements. The inversions are unique for each killer type, showing that they have a long separated evolutionary history and likely have established themselves as meiotic drivers independently. For the Sk-2 haplotype, for which we have polymorphism-data, we see signs of relaxed selection, which is consistent with the hypothesis that recombination suppression reduces the efficacy of selection in this region. Thus, our data indicates that albeit N. intermedia possesses an active genome defence system, selfish genetic elements have worked in concert and significantly affected the evolutionary trajectory of chromosome 3 in this species.

  • 1079.
    Svedberg, Jesper
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Hosseini, Sara
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Chen, Jun
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Vogan, Aaron A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Mozgova, Iva
    Swedish Univ Agr Sci, Dept Plant Biol, POB 7080, SE-75007 Uppsala, Sweden;Swedish Univ Agr Sci, Linnean Ctr Plant Biol, POB 7080, SE-75007 Uppsala, Sweden;Czech Acad Sci, Inst Microbiol, Ctr Algatech, CZ-37981 Trebon, Czech Republic.
    Hennig, Lars
    Swedish Univ Agr Sci, Dept Plant Biol, POB 7080, SE-75007 Uppsala, Sweden;Swedish Univ Agr Sci, Linnean Ctr Plant Biol, POB 7080, SE-75007 Uppsala, Sweden.
    Manitchotpisit, Pennapa
    Illinois State Univ, Sch Biol Sci, Normal, IL 61790 USA.
    Abusharekh, Anna
    Illinois State Univ, Sch Biol Sci, Normal, IL 61790 USA.
    Hammond, Thomas M.
    Illinois State Univ, Sch Biol Sci, Normal, IL 61790 USA.
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Johannesson, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Convergent evolution of complex genomic rearrangements in two fungal meiotic drive elements2018In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 4242Article in journal (Refereed)
    Abstract [en]

    Meiotic drive is widespread in nature. The conflict it generates is expected to be an important motor for evolutionary change and innovation. In this study, we investigated the genomic consequences of two large multi-gene meiotic drive elements, Sk-2 and Sk-3, found in the filamentous ascomycete Neurospora intermedia. Using long-read sequencing, we generated the first complete and well-annotated genome assemblies of large, highly diverged, non-recombining regions associated with meiotic drive elements. Phylogenetic analysis shows that, even though Sk-2 and Sk-3 are located in the same chromosomal region, they do not form sister clades, suggesting independent origins or at least a long evolutionary separation. We conclude that they have in a convergent manner accumulated similar patterns of tandem inversions and dense repeat clusters, presumably in response to similar needs to create linkage between genes causing drive and resistance.

  • 1080.
    Svedberg, Jesper
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.
    Vogan, Aaron
    Rhoades, Nicholas A.
    Sarmarajeewa, Dilini
    Hammond, Thomas M.
    Lascoux, Martin
    Johannesson, Hanna
    A single gene causes meiotic drive in Neurospora sitophilaManuscript (preprint) (Other academic)
    Abstract [en]

    Meiotic drive in Neurospora was first identified in Neurospora sitophila over forty years ago. Since drive in this fungus results in “spore killing”, the drive was designated Sk-1. The locus responsible for killing has until now been unknown. Here we sequenced 56 N. sitophila strains from natural populations, using paired-end sequencing on the Illumina HiSeq platform, and used this population genomic data to identify a locus on chromosome VI that significantly associates with the killing phenotypewe have used Illumina technology to generate whole genome sequence data for 56 wild N. sitophila strains. Using a genome wide association test we have identified the locus responsible for the Sk-1 phenotype on chromosome VI. We call the locus nkl1. By using the PacBio RSII platform, we generated high quality genome assemblies of four N. sitophila strains (two Sk-1 killers and two sensitives) and verified that no structural rearrangements were found in this region or on other chromosomes. We verified by laboratory crosses that the allelic variants of nkl1 show segregation distortion, and generated deletion mutants to demonstrate that the locus is responsible both for killing and resistance. We show demonstrate that the element is likely to have been introgressed from the closely related species, N. hispaniola. We identified three subclades in N. sitophila is split up into three subclades, in one of which Sk-1 is fixed for Sk-1, one another where Sk-1 is absent, and a third where killers and sensitives appear to intermix. This indicates that Sk-1 is currently invading N. sitophila through matings between diverged lineages.

  • 1081.
    Svensson, Erik, I
    et al.
    Lund Univ, Dept Biol, SE-22362 Lund, Sweden.
    Berger, David
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    The Role of Mutation Bias in Adaptive Evolution2019In: Trends in Ecology & Evolution, ISSN 0169-5347, E-ISSN 1872-8383, Vol. 34, no 5, p. 422-434Article, review/survey (Refereed)
    Abstract [en]

    Mutational input is the ultimate source of genetic variation, but mutations are not thought to affect the direction of adaptive evolution. Recently, critics of standard evolutionary theory have questioned the random and non-directional nature of mutations, claiming that the mutational process can be adaptive in its own right. We discuss here mutation bias in adaptive evolution. We find little support for mutation bias as an independent force in adaptive evolution, although it can interact with selection under conditions of small population size and when standing genetic variation is limited, entirely consistent with standard evolutionary theory. We further emphasize that natural selection can shape the phenotypic effects of mutations, giving the false impression that directed mutations are driving adaptive evolution.

  • 1082.
    Svensson, Erik I.
    et al.
    Lund Univ, Dept Biol, S-22362 Lund, Sweden.
    Goedert, Debora
    Dartmouth Coll, Dept Biol Sci, Hanover, NH 03755 USA.
    Gomez-Llano, Miguel A.
    Lund Univ, Dept Biol, S-22362 Lund, Sweden.
    Spagopoulou, Foteini
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Nava-Bolanos, Angela
    Univ Nacl Autonoma Mexico, Inst Ecol, Dept Ecol Evolut, Apdo Postal 70-275,Ciudad Univ, Mexico City 04510, DF, Mexico;Univ Nacl Autonoma Mexico, Fac Ciencias, Secret Educ Abierta & Continua, CU, Ave Univ 3000, Mexico City 04510, DF, Mexico.
    Booksmythe, Isobel
    Monash Univ, Sch Biol Sci, Clayton, Vic 3800, Australia.
    Sex differences in local adaptation: what can we learn from reciprocal transplant experiments?2018In: Philosophical Transactions of the Royal Society of London. Biological Sciences, ISSN 0962-8436, E-ISSN 1471-2970, Vol. 373, no 1757, article id 20170420Article, review/survey (Refereed)
    Abstract [en]

    Local adaptation is of fundamental interest to evolutionary biologists. Traditionally, local adaptation has been studied using reciprocal transplant experiments to quantify fitness differences between residents and immigrants in pairwise transplants between study populations. Previous studies have detected local adaptation in some cases, but others have shown lack of adaptation or even maladaptation. Recently, the importance of different fitness components, such as survival and fecundity, to local adaptation have been emphasized. Here, we address another neglected aspect in studies of local adaptation: sex differences. Given the ubiquity of sexual dimorphism in life histories and phenotypic traits, this neglect is surprising, but may be partly explained by differences in research traditions and terminology in the fields of local adaptation and sexual selection. Studies that investigate differences in mating success between resident and immigrants across populations tend to be framed in terms of reproductive and behavioural isolation, rather than local adaptation. We briefly review the published literature that bridges these areas and suggest that reciprocal transplant experiments could benefit from quantifying both male and female fitness components. Such a more integrative research approach could clarify the role of sex differences in the evolution of local adaptations. 

  • 1083.
    Sverrisdóttir, Oddný Ósk
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Daskalaki, Evangelia
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Skoglund, Pontus
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Valdiosera, Cristina E.
    La Trobe University.
    Carretero, José M.
    Facultad de Humanidades, Departamento Históricas y Geografía.
    Arsuaga Ferreras, Juan Luis
    Facultad de Ciencias Geológicas.
    Jakobsson, Mattias
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Götherström, Anders
    Stockholm University.
    A late Neolithic Iberian farmer exhibits genetic affinity to Neolithic Scandinavian farmers and a Bronze Age central European  farmerManuscript (preprint) (Other academic)
  • 1084. Szrek, Piotr
    et al.
    Dec, Marek
    Niedzwiedzki, Grzegorz
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    The first placoderm fish from the Lower Devonian of Poland2015In: Journal of Vertebrate Paleontology, ISSN 0272-4634, E-ISSN 1937-2809, Vol. 35, no 3, article id e930471Article in journal (Refereed)
  • 1085.
    Szrek, Piotr
    et al.
    Polish Geol Inst, Natl Res Inst, Rakowiecka 4 St, PL-00075 Warsaw, Poland. Polish Geol Inst, Natl Res Inst, Holy Cross Mt Branch, Zgoda 21 St, PL-00075 Kielce, Poland..
    Salwa, Sylwester
    Holy Cross Mountains Branch of the Polish Geological Institute—National Research Institute, Zgoda 21 Street, 00-075 Kielce, Poland.
    Niedzwiedzki, Grzegorz
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Dec, Marek
    Polish Acad Sci, Inst Paleobiol, Twarda 51-55, PL-00818 Warsaw, Poland..
    Ahlberg, Per E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Uchman, Alfred
    Jagiellonian Univ, Inst Geol Sci, Oleandry 2a, PL-30063 Krakow, Poland..
    A glimpse of a fish face: An exceptional fish feeding trace fossil from the Lower Devonian of the Holy Cross Mountains, Poland2016In: Palaeogeography, Palaeoclimatology, Palaeoecology, ISSN 0031-0182, E-ISSN 1872-616X, Vol. 454, p. 113-124Article in journal (Refereed)
    Abstract [en]

    An exceptionally well-preserved assemblage of numerous invertebrate and vertebrate trace fossils is described from the Lower Devonian of the Holy Cross Mountains, southern Poland. Two trace-bearing horizons occur in the shallow-marine sequence that is exposed in a small outcrop near Ujazd village. One of the trace fossils is preserved as a bilobate, generally elliptical, epichnial pit is described as Osculichnus tarnowskae isp. nov. and interpreted as a unique example of praedichnia. Neoichnologic experiments and observations indicate that the ichnogenus Osculichnus was produced by feeding fish. The fish producing O. tarnowskae probably hunted bivalves, polychaetes and arthropods, which are represented by invertebrate trace fossils in the same horizons. The overall shape and morphological details of O. tarnowskae suggest that it was made by a lungfish broadly similar to Dipnorhynchus. The trace provides the first direct evidence for Devonian lungfish feeding behaviour, as well as the first record of three-dimensional soft-tissue morphology of the snout area of an Emsian representative of this group. The trace fossils from Ujazd provide new insight into the palaeoecology and taphonomy of the Lower Devonian of the Holy Cross Mountains.

  • 1086.
    Sällman Almén, Markus
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Functional Pharmacology.
    The Membrane Proteome: Evolution, Characteristics and Classification2012Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Membrane proteins are found in all kingdoms of life and are essential for cellular interactions with the environment. Although a large research effort have been put into this group many membrane proteins remains uncharacterized, both in terms of function and evolutionary history. We have estimated the component of α-helical membrane proteins within the human proteome; the membrane proteome. We found that the human membrane proteome make up 27% of all protein, which we could classify the majority of into 234 families and further into three major functional groups: receptors, transporters or enzymes. We extended this analysis by determining the membrane proteome of 24 organisms that covers all major groups of eukaryotes. This comprehensive membrane protein catalog of over 100,000 proteins was utilized to determine the evolutionary history of all membrane protein families throughout eukaryotes.  We also investigated the evolutionary history across eukaryotes of the antiviral Interferon induced transmembrane proteins (IFITM) and the G protein-coupled receptor (GPCR) superfamily in detail.  We identified ten novel human homologs to the IFITM proteins, which together with the known IFITMs forms a family that we call the Dispanins. Using phylogenetic analysis we show that the Dispanins first emerged in eukaryotes in a common ancestor of choanoflagellates and animals, and that the family later expanded in vertebrates into four subfamilies. The GPCR superfamily was mined across eukaryotic species and we present evidence for a common origin for four of the five main human GPCR families; Rhodopsin, Frizzled, Adhesion and Secretin in the cAMP receptor family that was found in non-metazoans and invertebrates, but has been lost in vertebrates. Here we present the first accurate estimation of the human proteome together with comprehensive functional and evolutionary classification and extend it to organisms that represents all major eukaryotic groups. Moreover, we identify a novel protein family, the Dispanins, which has an evolutionary history that has been formed by horizontal gene transfer from bacteria followed by expansions in the animal lineage. We also study the evolution of the GPCR superfamily throughout eukaryotic evolution and provide a comprehensive model of the evolution and relationship of these receptors.

    List of papers
    1. Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin
    Open this publication in new window or tab >>Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin
    2009 (English)In: BMC Biology, ISSN 1741-7007, E-ISSN 1741-7007, Vol. 7, p. 50-Article in journal (Refereed) Published
    Abstract [en]

    BACKGROUND: Membrane proteins form key nodes in mediating the cell's interaction with the surroundings, which is one of the main reasons why the majority of drug targets are membrane proteins. RESULTS: Here we mined the human proteome and identified the membrane proteome subset using three prediction tools for alpha-helices: Phobius, TMHMM, and SOSUI. This dataset was reduced to a non-redundant set by aligning it to the human genome and then clustered with our own interactive implementation of the ISODATA algorithm. The genes were classified and each protein group was manually curated, virtually evaluating each sequence of the clusters, applying systematic comparisons with a range of databases and other resources. We identified 6,718 human membrane proteins and classified the majority of them into 234 families of which 151 belong to the three major functional groups: receptors (63 groups, 1,352 members), transporters (89 groups, 817 members) or enzymes (7 groups, 533 members). Also, 74 miscellaneous groups with 697 members were determined. Interestingly, we find that 41% of the membrane proteins are singlets with no apparent affiliation or identity to any human protein family. Our results identify major differences between the human membrane proteome and the ones in unicellular organisms and we also show a strong bias towards certain membrane topologies for different functional classes: 77% of all transporters have more than six helices while 60% of proteins with an enzymatic function and 88% receptors, that are not GPCRs, have only one single membrane spanning alpha-helix. Further, we have identified and characterized new gene families and novel members of existing families. CONCLUSION: Here we present the most detailed roadmap of gene numbers and families to our knowledge, which is an important step towards an overall classification of the entire human proteome. We estimate that 27% of the total human proteome are alpha-helical transmembrane proteins and provide an extended classification together with in-depth investigations of the membrane proteome's functional, structural, and evolutionary features.

    National Category
    Medical and Health Sciences
    Identifiers
    urn:nbn:se:uu:diva-121692 (URN)10.1186/1741-7007-7-50 (DOI)000270292300001 ()19678920 (PubMedID)
    Available from: 2010-03-27 Created: 2010-03-27 Last updated: 2017-12-12Bibliographically approved
    2. Evolution and characteristics of the membrane proteome
    Open this publication in new window or tab >>Evolution and characteristics of the membrane proteome
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Membrane proteins are found in all kingdoms of life and have a diverse set of functions and occupy key roles in many biological systems.  The majority of integral membrane proteins span the membrane with one or more transmembrane alpha helices, which both anchors the protein in the membrane and is crucial for their role in cell-cell interactions and signaling over the membrane. Herein, we have determined all alpha helical transmembrane proteins from 24 complete eukaryotic proteomes, which spans the four eukaryotic super groups chromalveolates, plants, excavates and unikonts. Hence, for the first time we are able to investigate the evolutionary history of the membrane proteome. In total we identify 100 955 membrane proteins among the more than 400 000 investigated proteins. We are able to place 91% of the membrane proteins into candidate families using Markov clustering based on sequence similarity and Pfam protein family affiliation. We provide evidence that most of the transporter and enzyme family repertoire of present eukaryotes was present already in the last common ancestor of all eukaryotes. Moreover, we discuss the functional nature of loss and gain of membrane protein families across eukaryotes and provide a comprehensive resource of the evolutionary history of the human membrane proteome.

    Keywords
    Membrane proteins, membrane proteome, comparative genomics
    National Category
    Bioinformatics and Systems Biology Evolutionary Biology Biochemistry and Molecular Biology
    Identifiers
    urn:nbn:se:uu:diva-181981 (URN)
    Available from: 2012-10-02 Created: 2012-10-02 Last updated: 2013-01-23
    3. The Dispanins: A Novel Gene Family of Ancient Origin That Contains 14 Human Members
    Open this publication in new window or tab >>The Dispanins: A Novel Gene Family of Ancient Origin That Contains 14 Human Members
    2012 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 7, no 2, p. e31961-Article in journal (Refereed) Published
    Abstract [en]

    The Interferon induced transmembrane proteins (IFITM) are a family of transmembrane proteins that is known to inhibit cell invasion of viruses such as HIV-1 and influenza. We show that the IFITM genes are a subfamily in a larger family of transmembrane (TM) proteins that we call Dispanins, which refers to a common 2TM structure. We mined the Dispanins in 36 eukaryotic species, covering all major eukaryotic groups, and investigated their evolutionary history using Bayesian and maximum likelihood approaches to infer a phylogenetic tree. We identified ten human genes that together with the known IFITM genes form the Dispanin family. We show that the Dispanins first emerged in eukaryotes in a common ancestor of choanoflagellates and metazoa, and that the family later expanded in vertebrates where it forms four subfamilies (A-D). Interestingly, we also find that the family is found in several different phyla of bacteria and propose that it was horizontally transferred to eukaryotes from bacteria in the common ancestor of choanoflagellates and metazoa. The bacterial and eukaryotic sequences have a considerably conserved protein structure. In conclusion, we introduce a novel family, the Dispanins, together with a nomenclature based on the evolutionary origin.

    National Category
    Pharmacology and Toxicology
    Identifiers
    urn:nbn:se:uu:diva-174788 (URN)10.1371/journal.pone.0031961 (DOI)000302871500098 ()
    Available from: 2012-05-29 Created: 2012-05-28 Last updated: 2018-01-12Bibliographically approved
    4. Independent HHsearch, Needleman-Wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families
    Open this publication in new window or tab >>Independent HHsearch, Needleman-Wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families
    Show others...
    2011 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 28, no 9, p. 2471-2480Article in journal (Refereed) Published
    Abstract [en]

    Several families of G protein-coupled receptors (GPCR) show no significant sequence similarities and it has been debated which groups of GPCRs that share a common origin. We developed and performed integrated independent HHsearch, Needleman-Wunsch-based and motif analyses on almost 7000 unique GPCRs from twelve species. Moreover, we mined the evolutionary important Trichoplax adhaerens, Nematostella vectensis, Thalassiosira pseudonana and Strongylocentrotus purpuratus genomes, revealing remarkably rich vertebrate-like repertoires already in the early Metazoan species. We found strong evidence for that the Adhesion and Frizzled families are children to the cAMP family with HHsearch homology probabilities of 99.8% and 99.4%, respectively, also supported by the Needleman-Wunsch analysis and several motifs. We also found that the large Rhodopsin family is likely a child of the cAMP family with a HHsearch homology probability of 99.4% and conserved motifs. Therefore, we suggest that the Adhesion and Frizzled families originated from the cAMP family in an event close to that which gave rise to the Rhodopsin family. We also found convincing evidence that the Rhodopsin family is parent to the important sensory Taste 2, Vomeronasal type 1 and Nematode chemoreceptor families. The insect odorant, gustatory and Trehalose receptors, frequently referred to as GPCRs, form a separate cluster without relationship to the other families and we speculate, based on these and other’s results, that these families are ligand-gated ion channels rather than GPCRs. Overall, we suggest common descent of at least 97% of the GPCRs sequences found in humans, including all the main families.

    Keywords
    evolution, GPCR, GPCRs, G-protein, 7TM, Rhodopsin
    National Category
    Medical and Health Sciences
    Identifiers
    urn:nbn:se:uu:diva-121694 (URN)10.1093/molbev/msr061 (DOI)000294552700009 ()
    Available from: 2010-03-27 Created: 2010-03-27 Last updated: 2017-12-12Bibliographically approved
    5. The Origin of GPCRs: Identification of Mammalian like Rhodopsin, Adhesion, Glutamate and Frizzled GPCRs in Fungi
    Open this publication in new window or tab >>The Origin of GPCRs: Identification of Mammalian like Rhodopsin, Adhesion, Glutamate and Frizzled GPCRs in Fungi
    2012 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 7, no 1, p. e29817-Article in journal (Refereed) Published
    Abstract [en]

    G protein-coupled receptors (GPCRs) in humans are classified into the five main families named Glutamate, Rhodopsin, Adhesion, Frizzled and Secretin according to the GRAFS classification. Previous results show that these mammalian GRAFS families are well represented in the Metazoan lineages, but they have not been shown to be present in Fungi. Here, we systematically mined 79 fungal genomes and provide the first evidence that four of the five main mammalian families of GPCRs, namely Rhodopsin, Adhesion, Glutamate and Frizzled, are present in Fungi and found 142 novel sequences between them. Significantly, we provide strong evidence that the Rhodopsin family emerged from the cAMP receptor family in an event close to the split of Opisthokonts and not in Placozoa, as earlier assumed. The Rhodopsin family then expanded greatly in Metazoans while the cAMP receptor family is found in 3 invertebrate species and lost in the vertebrates. We estimate that the Adhesion and Frizzled families evolved before the split of Unikonts from a common ancestor of all major eukaryotic lineages. Also, the study highlights that the fungal Adhesion receptors do not have N-terminal domains whereas the fungal Glutamate receptors have a broad repertoire of mammalian-like N-terminal domains. Further, mining of the close unicellular relatives of the Metazoan lineage, Salpingoeca rosetta and Capsaspora owczarzaki, obtained a rich group of both the Adhesion and Glutamate families, which in particular provided insight to the early emergence of the N-terminal domains of the Adhesion family. We identified 619 Fungi specific GPCRs across 79 genomes and revealed that Blastocladiomycota and Chytridiomycota phylum have Metazoan-like GPCRs rather than the GPCRs specific for Fungi. Overall, this study provides the first evidence of the presence of four of the five main GRAFS families in Fungi and clarifies the early evolutionary history of the GPCR superfamily.

    National Category
    Medical and Health Sciences
    Identifiers
    urn:nbn:se:uu:diva-172159 (URN)10.1371/journal.pone.0029817 (DOI)000301070200052 ()
    Available from: 2012-04-03 Created: 2012-04-02 Last updated: 2017-12-07Bibliographically approved
  • 1087.
    Sällman Almén, Markus
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Functional Pharmacology.
    Fredriksson, Robert
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Functional Pharmacology.
    Schiöth, Helgi
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Functional Pharmacology.
    Evolution and characteristics of the membrane proteomeManuscript (preprint) (Other academic)
    Abstract [en]

    Membrane proteins are found in all kingdoms of life and have a diverse set of functions and occupy key roles in many biological systems.  The majority of integral membrane proteins span the membrane with one or more transmembrane alpha helices, which both anchors the protein in the membrane and is crucial for their role in cell-cell interactions and signaling over the membrane. Herein, we have determined all alpha helical transmembrane proteins from 24 complete eukaryotic proteomes, which spans the four eukaryotic super groups chromalveolates, plants, excavates and unikonts. Hence, for the first time we are able to investigate the evolutionary history of the membrane proteome. In total we identify 100 955 membrane proteins among the more than 400 000 investigated proteins. We are able to place 91% of the membrane proteins into candidate families using Markov clustering based on sequence similarity and Pfam protein family affiliation. We provide evidence that most of the transporter and enzyme family repertoire of present eukaryotes was present already in the last common ancestor of all eukaryotes. Moreover, we discuss the functional nature of loss and gain of membrane protein families across eukaryotes and provide a comprehensive resource of the evolutionary history of the human membrane proteome.

  • 1088.
    Söderberg, Axel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Biology Education Centre.
    Song recognition in nestling Ficedula Flycatchers2016Independent thesis Basic level (degree of Bachelor), 20 credits / 30 HE creditsStudent thesis
  • 1089.
    Tahir, Daniah
    Uppsala University, Disciplinary Domain of Science and Technology, Mathematics and Computer Science, Department of Mathematics.
    Multi-trait Branching Models with Applications to Species Evolution2019Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    This thesis provides an analysis of the evolution of discrete traits and their effect on the birth and survival of species using the theory of supercritical, continuous time Markov branching processes. We present a branching modeling framework that incorporates multi-trait diversification processes associated with the emergence of new species, death of existing species, and transition of species carrying one type of a trait to another. The trait-dependent speciation, extinction, and transition help in interpreting the relationships between traits on one hand, and linking together the diversification process with molecular evolution on the other. Various multitype species branching models are applied in order to examine the evolutionary patterns in known data sets, such as the impact of outcrossing and selfing mating systems on the diversification rates of species, and the analysis of virulent behavior of pathogenic bacterial strains in different environments. Stochastic equations and limit theorems for branching processes help scrutinize the long time asymptotics of the models under an asymmetry in change of types, and under various schemes of rescaling. In addition, we explore diversity-dependent processes in which, instead of allowing supercritical growth of population sizes, the increase in species numbers is regulated by modifying the species branching rates. The use of probabilistic methods in a setting of population genetics leads to an analogy between biallelic frequency models and binary trait species tree models. To obtain an approximation for a Markov branching process of species evolution over a long geological time scale, we methodically utilize the theory of diffusion processes. Overall, our results show that branching models can be effectively used to seek to comprehend the diversification patterns in species during the process of evolution.

    List of papers
    1. Modeling a trait-dependent diversification process coupled with molecular evolution on a random species tree
    Open this publication in new window or tab >>Modeling a trait-dependent diversification process coupled with molecular evolution on a random species tree
    2019 (English)In: Journal of Theoretical Biology, ISSN 0022-5193, E-ISSN 1095-8541, Vol. 461, p. 189-203Article in journal (Refereed) Published
    Abstract [en]

    Understanding the evolution of binary traits, which affects the birth and survival of species and also the rate of molecular evolution, remains challenging. In this work, we present a probabilistic modeling framework for binary trait, random species trees, in which the number of species and their traits are represented by an asymmetric, two-type, continuous time Markov branching process. The model involves a number of different parameters describing both character and molecular evolution on the so-called 'reduced' tree, consisting of only extant species at the time of observation. We expand our model by considering the impact of binary traits on dN/dS, the normalized ratio of nonsynonymous to synonymous substitutions. We also develop mechanisms which enable us to understand the substitution rates on a phylogenetic tree with regards to the observed traits. The properties obtained from the model are illustrated with a phylogeny of outcrossing and selfing plant species, which allows us to investigate not only the branching tree rates, but also the molecular rates and the intensity of selection.

    Keywords
    Branching processes, Irreversible transitions, Binary traits, Phylogenetic trees, Mutation rates
    National Category
    Evolutionary Biology Probability Theory and Statistics
    Identifiers
    urn:nbn:se:uu:diva-372749 (URN)10.1016/j.jtbi.2018.10.032 (DOI)000452245900018 ()30340056 (PubMedID)
    Available from: 2019-01-15 Created: 2019-01-15 Last updated: 2019-04-25
    2. Using multitype branching models to analyze bacterial pathogenicity
    Open this publication in new window or tab >>Using multitype branching models to analyze bacterial pathogenicity
    Show others...
    (English)In: Article in journal (Refereed) Submitted
    Abstract [en]

    We apply multitype, continuous time Markov branching models to study pathogenicity in E. coli, a bacterium belonging to the genus Escherichia. First, we examine briefly the properties of multitype branching processes and we also survey some fundamental limit theorems regarding the behavior of such models under various conditions. These theorems are then applied to discrete, state dependent models in order to analyze pathogenicity in a published clinical data set consisting of 251 strains of E. coli. We use well established methods, incorporating maximum likelihood techniques, to estimate speciation rates as well as the rates of transition between different states of the models. From the analysis, we not only derive new results, we also verify some preexisting notions about virulent behavior in bacterial strains.

    Keywords
    Markov models, branching processes, limit theorems, virulence factors, E. coli strains.
    National Category
    Mathematics Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-380966 (URN)
    Available from: 2019-04-02 Created: 2019-04-02 Last updated: 2019-04-25
    3. Stochastic equations and limit results for some two-type branching models
    Open this publication in new window or tab >>Stochastic equations and limit results for some two-type branching models
    2019 (English)In: Statistics and Probability Letters, ISSN 0167-7152, E-ISSN 1879-2103, Vol. 150, p. 35-46Article in journal (Refereed) Published
    Abstract [en]

    A class of binary state, asymmetric, continuous time Markov branching processes are analyzed under supercritical conditions. Stochastic equations are provided, and limit results for the long time asymptotics as well as for the behavior of the model under rescaling are reviewed. Extensions are presented for model variations, such as population size dependence, with the purpose of promoting further use of these models for applications.

    Keywords
    Continuous time branching process, Asymmetric model, Population size dependence, Functional limit theory, Central limit theory
    National Category
    Probability Theory and Statistics
    Identifiers
    urn:nbn:se:uu:diva-380960 (URN)10.1016/j.spl.2019.02.011 (DOI)000466623900006 ()
    Available from: 2019-04-02 Created: 2019-04-02 Last updated: 2019-06-25Bibliographically approved
    4. Analysis of diversity-dependent species evolution using concepts in population genetics
    Open this publication in new window or tab >>Analysis of diversity-dependent species evolution using concepts in population genetics
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    In this work, we consider a two-type species model with trait dependent speciation, extinction and transition rates under an evolutionary time scale. The scaling approach and the diffusion approximation techniques which are widely used in mathematical population genetics provide background and tools to assist in the study of species dynamics, and help explore the analogy between trait dependent species diversication and the evolution of allele frequencies in the population genetics setting. The analytical framework specied is then applied to models incorporating diversity-dependence, in order to infer effective results from processes in which the net growth of species depends on their current population sizes.

    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-380961 (URN)
    Available from: 2019-04-02 Created: 2019-04-02 Last updated: 2019-04-25
  • 1090.
    Tahir, Daniah
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Mathematics and Computer Science, Department of Mathematics.
    Glemin, Sylvain
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. University of Montpellier, CNRS, IRD, EPHE, ISEM, UMR 5554, Montpellier 5, France.
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Kaj, Ingemar
    Uppsala University, Disciplinary Domain of Science and Technology, Mathematics and Computer Science, Department of Mathematics, Analysis and Probability Theory.
    Modeling a trait-dependent diversification process coupled with molecular evolution on a random species tree2019In: Journal of Theoretical Biology, ISSN 0022-5193, E-ISSN 1095-8541, Vol. 461, p. 189-203Article in journal (Refereed)
    Abstract [en]

    Understanding the evolution of binary traits, which affects the birth and survival of species and also the rate of molecular evolution, remains challenging. In this work, we present a probabilistic modeling framework for binary trait, random species trees, in which the number of species and their traits are represented by an asymmetric, two-type, continuous time Markov branching process. The model involves a number of different parameters describing both character and molecular evolution on the so-called 'reduced' tree, consisting of only extant species at the time of observation. We expand our model by considering the impact of binary traits on dN/dS, the normalized ratio of nonsynonymous to synonymous substitutions. We also develop mechanisms which enable us to understand the substitution rates on a phylogenetic tree with regards to the observed traits. The properties obtained from the model are illustrated with a phylogeny of outcrossing and selfing plant species, which allows us to investigate not only the branching tree rates, but also the molecular rates and the intensity of selection.

  • 1091.
    Talavera, David
    et al.
    Univ Manchester, Fac Life Sci, Manchester, Lancs, England..
    Lovell, Simon C.
    Univ Manchester, Fac Life Sci, Manchester, Lancs, England..
    Whelan, Simon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ Manchester, Fac Life Sci, Manchester, Lancs, England..
    Covariation Is a Poor Measure of Molecular Coevolution2015In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 32, no 9, p. 2456-2468Article in journal (Refereed)
    Abstract [en]

    Recent developments in the analysis of amino acid covariation are leading to breakthroughs in protein structure prediction, protein design, and prediction of the interactome. It is assumed that observed patterns of covariation are caused by molecular coevolution, where substitutions at one site affect the evolutionary forces acting at neighboring sites. Our theoretical and empirical results cast doubt on this assumption. We demonstrate that the strongest coevolutionary signal is a decrease in evolutionary rate and that unfeasibly long times are required to produce coordinated substitutions. We find that covarying substitutions are mostly found on different branches of the phylogenetic tree, indicating that they are independent events that may or may not be attributable to coevolution. These observations undermine the hypothesis that molecular coevolution is the primary cause of the covariation signal. In contrast, we find that the pairs of residues with the strongest covariation signal tend to have low evolutionary rates, and that it is this low rate that gives rise to the covariation signal. Slowly evolving residue pairs are disproportionately located in the protein's core, which explains covariation methods' ability to detect pairs of residues that are close in three dimensions. These observations lead us to propose the "coevolution paradox": The strength of coevolution required to cause coordinated changes means the evolutionary rate is so low that such changes are highly unlikely to occur. As modern covariation methods may lead to breakthroughs in structural genomics, it is critical to recognize their biases and limitations.

  • 1092.
    Talla, Venkat
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University.
    Speciation genetics of recently diverged species: 2018Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Species differentiation can be a consequence of evolutionary forces including natural selection and random genetic drift. Patterns of genomic differentiation vary across the tree of life. This variation seems to be dependent on, for example, differences in genomic architecture and molecular mechanisms. However, the knowledge we currently possess, both regarding the processes driving speciation and the resulting genomic signatures, is from a very small subset of the overall biodiversity that resides on the planet. Therefore, characterization of the architecture of genomic divergence from more organism groups will be important to understand the effects of molecular mechanisms and evolutionary forces driving divergence between lineages. Hence it has not been possible to come to a consensus on the relative importance of genetic drift and natural selection on divergence processes in general. In this thesis, I use genomic approaches to investigate the forces underlying species and population differentiation in the European cryptic wood white butterflies (Leptidea sinapisL. reali and L. juvernica) and two closely related bird species, the chiffchaff (Phylloscopus collybita abietinus) and the Siberian chiffchaff (P. tristis). Both these groups contain recently diverged species, a prerequisite for investigating initial differentiation processes. However, the study systems also differ in several respects, allowing for applying distinct approaches to understand the divergence process in each system.

    In summary, by applying a suite of genomic approaches, my thesis work gives novel insights into the speciation history of wood whites and chiffchaff. I identify candidate genes for local adaptation in both systems and concludes that genome differentiation in wood white butterflies have been driven by a combination of random genetic drift and week directional selection in allopatry. In the chiffchaff, the general differentiation landscape seems to have been shaped by recurrent background selection (and potentially selective sweeps), likely as a consequence of regional variation in the recombination rate which has also been observed in other genome-scans in birds. Potentially, some of the highly differentiated regions contain barriers to gene-flow as these regions are still present in sympatry, where species exchange genetic material at a high rate.

    List of papers
    1. Rapid Increase in Genome Size as a Consequence of Transposable Element Hyperactivity in Wood-White (Leptidea) Butterflies
    Open this publication in new window or tab >>Rapid Increase in Genome Size as a Consequence of Transposable Element Hyperactivity in Wood-White (Leptidea) Butterflies
    Show others...
    2017 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 9, no 10, p. 2491-2505Article in journal (Refereed) Published
    Abstract [en]

    Characterizing and quantifying genome size variation among organisms and understanding if genome size evolves as a consequence of adaptive or stochastic processes have been long-standing goals in evolutionary biology. Here, we investigate genome size variation and association with transposable elements (TEs) across lepidopteran lineages using a novel genome assembly of the common wood-white (Leptidea sinapis) and population re-sequencing data from both L. sinapis and the closely related L. reali and L. juvernica together with 12 previously available lepidopteran genome assemblies. A phylogenetic analysis confirms established relationships among species, but identifies previously unknown intraspecific structure within Leptidea lineages. The genome assembly of L. sinapis is one of the largest of any lepidopteran taxon so far (643Mb) and genome size is correlated with abundance of TEs, both in Lepidoptera in general and within Leptidea where L. juvernica from Kazakhstan has considerably larger genome size than any other Leptidea population. Specific TE subclasses have been active in different Lepidoptera lineages with a pronounced expansion of predominantly LINEs, DNA elements, and unclassified TEs in the Leptidea lineage after the split from other Pieridae. The rate of genome expansion in Leptidea in general has been in the range of four Mb/Million year (My), with an increase in a particular L. juvernica population to 72Mb/My. The considerable differences in accumulation rates of specific TE classes in different lineages indicate that TE activity plays a major role in genome size evolution in butterflies and moths.

    Keywords
    butterfly, Lepidoptera, Leptidea, genome expansion, transposable elements, population
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-341668 (URN)10.1093/gbe/evx163 (DOI)000414778600001 ()28981642 (PubMedID)
    Funder
    Knut and Alice Wallenberg FoundationSwedish Research Council, VR 2013-4508EU, FP7, Seventh Framework Programme, 625997Swedish National Infrastructure for Computing (SNIC), b2014034
    Available from: 2018-02-14 Created: 2018-02-14 Last updated: 2018-08-28Bibliographically approved
    2. Lack of parallelism: lineage-specific directional selection drives genome differentiation across a triplet of cryptic butterfly species
    Open this publication in new window or tab >>Lack of parallelism: lineage-specific directional selection drives genome differentiation across a triplet of cryptic butterfly species
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    (English)Manuscript (preprint) (Other academic)
    Keywords
    Speciation, wood-white butterflies, Leptidea, Lepidoptera, cryptic species, genome-scan
    National Category
    Genetics
    Research subject
    Evolutionary Genetics
    Identifiers
    urn:nbn:se:uu:diva-358288 (URN)
    Available from: 2018-08-27 Created: 2018-08-27 Last updated: 2018-08-28
    3. Heterogeneous Patterns of Genetic Diversity and Differentiation in European and Siberian Chiffchaff (Phylloscopus collybita abietinus/P. tristis)
    Open this publication in new window or tab >>Heterogeneous Patterns of Genetic Diversity and Differentiation in European and Siberian Chiffchaff (Phylloscopus collybita abietinus/P. tristis)
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    2017 (English)In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 7, no 12, p. 3983-3998Article in journal (Refereed) Published
    Abstract [en]

    Identification of candidate genes for trait variation in diverging lineages and characterization of mechanistic underpinnings of genome differentiation are key steps toward understanding the processes underlying the formation of new species. Hybrid zones provide a valuable resource for such investigations, since they allow us to study how genomes evolve as species exchange genetic material and to associate particular genetic regions with phenotypic traits of interest. Here, we use whole-genome resequencing of both allopatric and hybridizing populations of the European (Phylloscopus collybita abietinus) and the Siberian chiffchaff (P. tristis)-two recently diverged species which differ in morphology, plumage, song, habitat, and migration-to quantify the regional variation in genome-wide genetic diversity and differentiation, and to identify candidate regions for trait variation. We find that the levels of diversity, differentiation, and divergence are highly heterogeneous, with significantly reduced global differentiation, and more pronounced differentiation peaks in sympatry than in allopatry. This pattern is consistent with regional differences in effective population size and recurrent background selection or selective sweeps reducing the genetic diversity in specific regions prior to lineage divergence, but the data also suggest that post-divergence selection has resulted in increased differentiation and fixed differences in specific regions. We find that hybridization and backcrossing is common in sympatry, and that phenotype is a poor predictor of the genomic composition of sympatric birds. The combination of a differentiation scan approach with identification of fixed differences pinpoint a handful of candidate regions that might be important for trait variation between the two species.

    Keywords
    chiffchaff, speciation, genome-scan, divergence islands, Z-chromosome, autosomes
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-344216 (URN)10.1534/g3.117.300152 (DOI)000417073900015 ()29054864 (PubMedID)
    Funder
    Swedish Research Council, 2013-4508Swedish National Infrastructure for Computing (SNIC), b2013146
    Available from: 2018-03-06 Created: 2018-03-06 Last updated: 2018-08-28Bibliographically approved
    4. Dissecting the effects of natural selection and mutation on genetic diversity in three recently diverged cryptic butterfly species
    Open this publication in new window or tab >>Dissecting the effects of natural selection and mutation on genetic diversity in three recently diverged cryptic butterfly species
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    (English)Manuscript (preprint) (Other academic)
    Keywords
    Adaptation, speciation, Leptidea, Lepidoptera, cryptic species, selection
    National Category
    Genetics
    Research subject
    Biology with specialization in Evolutionary Genetics
    Identifiers
    urn:nbn:se:uu:diva-358291 (URN)
    Available from: 2018-08-27 Created: 2018-08-27 Last updated: 2018-08-28
    5. Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation
    Open this publication in new window or tab >>Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation
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    2018 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, no 4, p. 935-948Article in journal (Refereed) Published
    Abstract [en]

    In temperate latitudes, many insects enter diapause (dormancy) during the cold season, a period during which developmental processes come to a standstill. The wood white (Leptidea sinapis) is a butterfly species distributed across western Eurasia that shows photoperiod-induced diapause with variation in critical day-length across populations at different latitudes. We assembled transcriptomes and estimated gene expression levels at different developmental stages in experimentally induced directly developing and diapausing cohorts of a single Swedish population of L. sinapis to investigate the regulatory mechanisms underpinning diapause initiation. Different day lengths resulted in expression changes of developmental genes and affected the rate of accumulation of signal molecules, suggesting that diapause induction might be controlled by increased activity of monoamine neurotransmitters in larvae reared under short-day light conditions. Expression differences between light treatment groups of two monoamine regulator genes (DDC and ST) were observed already in instar III larvae. Once developmental pathways were irreversibly set at instar V, a handful of genes related to dopamine production were differentially expressed leading to a significant decrease in expression of global metabolic genes and increase in expression of genes related to fatty acid synthesis and sequestration. This is in line with a time-dependent (hour-glass) model of diapause regulation where a gradual shift in the concentration of monoamine neurotransmitters and their metabolites during development of larvae under short-day conditions leads to increased storage of fat, decreased energy expenditures, and ultimately developmental stasis at the pupal stage.

    Place, publisher, year, edition, pages
    WILEY, 2018
    Keywords
    developmental plasticity, diapause, gene expression, hour-glass model, Lepidoptera, monoamine neurotransmitter
    National Category
    Developmental Biology
    Identifiers
    urn:nbn:se:uu:diva-351766 (URN)10.1111/mec.14501 (DOI)000428797100010 ()29411442 (PubMedID)
    Funder
    Swedish Research Council, 2013-4508]Science for Life Laboratory - a national resource center for high-throughput molecular bioscience, Backstrom_2014Knut and Alice Wallenberg Foundation
    Available from: 2018-06-04 Created: 2018-06-04 Last updated: 2018-08-28Bibliographically approved
  • 1093.
    Talla, Venkat
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Kalsoom, Faheema
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Shipilina, Daria
    Lomonosov Moscow State Univ, Dept Vertebrate Zool, Moscow 119991, Russia..
    Marova, Irina
    Lomonosov Moscow State Univ, Dept Vertebrate Zool, Moscow 119991, Russia..
    Backström, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Heterogeneous Patterns of Genetic Diversity and Differentiation in European and Siberian Chiffchaff (Phylloscopus collybita abietinus/P. tristis)2017In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 7, no 12, p. 3983-3998Article in journal (Refereed)
    Abstract [en]

    Identification of candidate genes for trait variation in diverging lineages and characterization of mechanistic underpinnings of genome differentiation are key steps toward understanding the processes underlying the formation of new species. Hybrid zones provide a valuable resource for such investigations, since they allow us to study how genomes evolve as species exchange genetic material and to associate particular genetic regions with phenotypic traits of interest. Here, we use whole-genome resequencing of both allopatric and hybridizing populations of the European (Phylloscopus collybita abietinus) and the Siberian chiffchaff (P. tristis)-two recently diverged species which differ in morphology, plumage, song, habitat, and migration-to quantify the regional variation in genome-wide genetic diversity and differentiation, and to identify candidate regions for trait variation. We find that the levels of diversity, differentiation, and divergence are highly heterogeneous, with significantly reduced global differentiation, and more pronounced differentiation peaks in sympatry than in allopatry. This pattern is consistent with regional differences in effective population size and recurrent background selection or selective sweeps reducing the genetic diversity in specific regions prior to lineage divergence, but the data also suggest that post-divergence selection has resulted in increased differentiation and fixed differences in specific regions. We find that hybridization and backcrossing is common in sympatry, and that phenotype is a poor predictor of the genomic composition of sympatric birds. The combination of a differentiation scan approach with identification of fixed differences pinpoint a handful of candidate regions that might be important for trait variation between the two species.

  • 1094.
    Talla, Venkat
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Suh, Alexander
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Kalsoom, Faheema
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Dinca, Vlad
    Inst Biol Evolut CSIC UPF, Anim Biodivers & Evolut Program, Barcelona, Spain..
    Vila, Roger
    Inst Biol Evolut CSIC UPF, Anim Biodivers & Evolut Program, Barcelona, Spain..
    Friberg, Magne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Wiklund, Christer
    Stockholm Univ, Div Ecol, Dept Zool, Stockholm, Sweden..
    Backström, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Rapid Increase in Genome Size as a Consequence of Transposable Element Hyperactivity in Wood-White (Leptidea) Butterflies2017In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 9, no 10, p. 2491-2505Article in journal (Refereed)
    Abstract [en]

    Characterizing and quantifying genome size variation among organisms and understanding if genome size evolves as a consequence of adaptive or stochastic processes have been long-standing goals in evolutionary biology. Here, we investigate genome size variation and association with transposable elements (TEs) across lepidopteran lineages using a novel genome assembly of the common wood-white (Leptidea sinapis) and population re-sequencing data from both L. sinapis and the closely related L. reali and L. juvernica together with 12 previously available lepidopteran genome assemblies. A phylogenetic analysis confirms established relationships among species, but identifies previously unknown intraspecific structure within Leptidea lineages. The genome assembly of L. sinapis is one of the largest of any lepidopteran taxon so far (643Mb) and genome size is correlated with abundance of TEs, both in Lepidoptera in general and within Leptidea where L. juvernica from Kazakhstan has considerably larger genome size than any other Leptidea population. Specific TE subclasses have been active in different Lepidoptera lineages with a pronounced expansion of predominantly LINEs, DNA elements, and unclassified TEs in the Leptidea lineage after the split from other Pieridae. The rate of genome expansion in Leptidea in general has been in the range of four Mb/Million year (My), with an increase in a particular L. juvernica population to 72Mb/My. The considerable differences in accumulation rates of specific TE classes in different lineages indicate that TE activity plays a major role in genome size evolution in butterflies and moths.

  • 1095.
    Tamarit, Daniel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Evolution of symbiotic lineages and the origin of new traits2016Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    This thesis focuses on the genomic study of symbionts of two different groups of hymenopterans: bees and ants. Both groups of insects have major ecological impact, and investigating their microbiomes increases our understanding of their health, diversity and evolution.

    The study of the bee gut microbiome, including members of Lactobacillus and Bifidobacterium, revealed genomic processes related to the adaptation to the gut environment, such as the expansion of genes for carbohydrate metabolism and the acquisition of genes for interaction with the host. A broader genomic study of these genera demonstrated that some lineages evolve under strong and opposite substitution biases, leading to extreme GC content values. A comparison of codon usage patterns in these groups revealed ongoing shifts of optimal codons.

    In a separate study we analysed the genomes of several strains of Lactobacillus kunkeei, which inhabits the honey stomach of bees but is not found in their gut. We observed signatures of genome reduction and suggested candidate genes for host-interaction processes. We discovered a novel type of genome architecture where genes for metabolic functions are located in one half of the genome, whereas genes for information processes are located in the other half. This genome organization was also found in other Lactobacillus species, indicating that it was an ancestral feature that has since been retained. We suggest mechanisms and selective forces that may cause the observed organization, and describe processes leading to its loss in several lineages independently.

    We also studied the genome of a species of Rhizobiales bacteria found in ants. We discuss its metabolic capabilities and suggest scenarios for how it may affect the ants’ lifestyle. This genome contained a region with homology to the Bartonella gene transfer agent (GTA), which is a domesticated bacteriophage used to transfer bacterial DNA between cells. We propose that its unique behaviour as a specialist GTA, preferentially transferring host-interaction factors, originated from a generalist GTA that transferred random segments of chromosomal DNA.

    These bioinformatic analyses of previously uncharacterized bacterial lineages have increased our understanding of their physiology and evolution and provided answers to old and new questions in fundamental microbiology.

    List of papers
    1. Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut
    Open this publication in new window or tab >>Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut
    Show others...
    2015 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 16, article id 284Article in journal (Refereed) Published
    Abstract [en]

    Background: In the honeybee Apis mellifera, the bacterial gut community is consistently colonized by eight distinct phylotypes of bacteria. Managed bee colonies are of considerable economic interest and it is therefore important to elucidate the diversity and role of this microbiota in the honeybee. In this study, we have sequenced the genomes of eleven strains of lactobacilli and bifidobacteria isolated from the honey crop of the honeybee Apis mellifera. Results: Single gene phylogenies confirmed that the isolated strains represent the diversity of lactobacilli and bifidobacteria in the gut, as previously identified by 16S rRNA gene sequencing. Core genome phylogenies of the lactobacilli and bifidobacteria further indicated extensive divergence between strains classified as the same phylotype. Phylotype-specific protein families included unique surface proteins. Within phylotypes, we found a remarkably high level of gene content diversity. Carbohydrate metabolism and transport functions contributed up to 45% of the accessory genes, with some genomes having a higher content of genes encoding phosphotransferase systems for the uptake of carbohydrates than any previously sequenced genome. These genes were often located in highly variable genomic segments that also contained genes for enzymes involved in the degradation and modification of sugar residues. Strain-specific gene clusters for the biosynthesis of exopolysaccharides were identified in two phylotypes. The dynamics of these segments contrasted with low recombination frequencies and conserved gene order structures for the core genes. Hits for CRISPR spacers were almost exclusively found within phylotypes, suggesting that the phylotypes are associated with distinct phage populations. Conclusions: The honeybee gut microbiota has been described as consisting of a modest number of phylotypes; however, the genomes sequenced in the current study demonstrated a very high level of gene content diversity within all three described phylotypes of lactobacilli and bifidobacteria, particularly in terms of metabolic functions and surface structures, where many features were strain-specific. Together, these results indicate niche differentiation within phylotypes, suggesting that the honeybee gut microbiota is more complex than previously thought.

    Keywords
    Lactic acid bacteria, Lactobacillus spp, Firmicutes, Bifidobacteria, Comparative genomics, Phosphotransferase systems, Niche specialization
    National Category
    Genetics
    Identifiers
    urn:nbn:se:uu:diva-256855 (URN)10.1186/s12864-015-1476-6 (DOI)000355302300001 ()25880915 (PubMedID)
    External cooperation:
    Note

    De två förstaförfattarna delar förstaförfattarskapet.

    Available from: 2015-06-26 Created: 2015-06-26 Last updated: 2017-12-04Bibliographically approved
    2. Functionally Structured Genomes in Lactobacillus kunkeei Colonizing the Honey Crop and Food Products of Honeybees and Stingless Bees
    Open this publication in new window or tab >>Functionally Structured Genomes in Lactobacillus kunkeei Colonizing the Honey Crop and Food Products of Honeybees and Stingless Bees
    Show others...
    2015 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 7, no 6, p. 1455-1473Article in journal (Refereed) Published
    Abstract [en]

    Lactobacillus kunkeei is the most abundant bacterial species in the honey crop and food products of honeybees. The 16 S rRNA-genes of strains isolated from different bee species are nearly identical in sequence and therefore inadequate as markers for studies of coevolutionary patterns. Here, we have compared the 1.5Mb genomes of ten L. kunkeei strains isolated from all recognized Apis species and another two strains from Meliponini species. Agene flux analysis, including previously sequenced Lactobacillus species as outgroups, indicated the influence of reductive evolution. The genome architecture is unique in that vertically inherited core genes are located near the terminus of replication, whereas genes for secreted proteins and putative host-adaptive traits are located near the origin of replication. We suggest that these features have resulted from a genome-wide loss of genes, with integrations of novel genes mostly occurring in regions flanking the origin of replication. The phylogenetic analyses showed that the bacterial topology was incongruent with the host topology, and that strains of the same microcluster have recombined frequently across the host species barriers, arguing against codiversification. Multiple genotypes were recovered in the individual hosts and transfers of mobile elements could be demonstrated for strains isolated from the same host species. Unlike other bacteria with small genomes, short generation times and multiple rRNA operons suggest that L. kunkeei evolves under selection for rapid growth in its natural growth habitat. The results provide an extended framework for reductive genome evolution and functional genome organization in bacteria.

    Keywords
    genome organization, Lactobacillus kunkeei, honeybee, genome reduction, recombination
    National Category
    Biological Sciences
    Identifiers
    urn:nbn:se:uu:diva-261322 (URN)10.1093/gbe/evv079 (DOI)000358800100005 ()25953738 (PubMedID)
    Available from: 2015-09-02 Created: 2015-09-01 Last updated: 2017-12-04Bibliographically approved
    3. Functionally structured genome architectures in Lactobacillus – insights into their variability and evolution
    Open this publication in new window or tab >>Functionally structured genome architectures in Lactobacillus – insights into their variability and evolution
    Show others...
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Bacterial genome architectures evolve in response to selective pressures on the interplay between replication and gene expression. Several genomes contain a higher fraction of genes coding for proteins involved in information processes near the origin of replication, which is thought to be due to selection for rapid growth. We recently described a novel type of genome architecture in Lactobacillus kunkeei (Tamarit, et al. 2015). In this genome, vertically inherited genes encoding proteins with roles in translation and replication have accumulated in the chromosomal half surrounding the terminus of replication, while species-specific genes, and genes encoding proteins with metabolic and transport functions have accumulated in the chromosomal half around the origin of replication. Here, we show that this pattern is present also in the closest relatives of L. kunkeei, and similar but not identical biased genome architectures are present in other groups within the Lactobacillaceae. Thus, the biased genome structure in L. kunkeei has emerged from an ancestral clustering of vertically inherited genes around the terminus of replication, while horizontally acquired genes have been inserted near the origin of replication. The genome bias has been lost independently in several groups due to insertions of mobile elements near the terminus of replication and/or major genome rearrangements. We propose chromosomal structuring in macrodomains in the Lactobacillaceae, and suggest that further exploration of its functional consequences and generality will provide valuable insights into the forces that shape genome organization in bacteria. 

    Keywords
    genome organization, replication axis
    National Category
    Evolutionary Biology
    Research subject
    Biology with specialization in Molecular Evolution
    Identifiers
    urn:nbn:se:uu:diva-301781 (URN)
    External cooperation:
    Available from: 2016-08-25 Created: 2016-08-25 Last updated: 2016-08-31Bibliographically approved
    4. Switches in Genomic GC Content Drive Shifts of Optimal Codons under Sustained Selection on Synonymous Sites
    Open this publication in new window or tab >>Switches in Genomic GC Content Drive Shifts of Optimal Codons under Sustained Selection on Synonymous Sites
    2017 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 9, no 10, p. 2560-2579Article in journal (Refereed) Published
    Abstract [en]

    The major codon preference model suggests that codons read by tRNAs in high concentrations are preferentially utilized in highly expressed genes. However, the identity of the optimal codons differs between species although the forces driving such changes are poorly understood. We suggest that these questions can be tackled by placing codon usage studies in a phylogenetic framework and that bacterial genomes with extreme nucleotide composition biases provide informative model systems. Switches in the background substitution biases from GC to AT have occurred in Gardnerella vaginalis (GC = 32%), and from AT to GC in Lactobacillus delbrueckii (GC=62%) and Lactobacillus fermentum (GC = 63%). We show that despite the large effects on codon usage patterns by these switches, all three species evolve under selection on synonymous sites. In G. vaginalis, the dramatic codon frequency changes coincide with shifts of optimal codons. In contrast, the optimal codons have not shifted in the two Lactobacillus genomes despite an increased fraction of GC-ending codons. We suggest that all three species are in different phases of an on-going shift of optimal codons, and attribute the difference to a stronger background substitution bias and/or longer time since the switch in G. vaginalis. We show that comparative and correlative methods for optimal codon identification yield conflicting results for genomes in flux and discuss possible reasons for the mispredictions. We conclude that switches in the direction of the background substitution biases can drive major shifts in codon preference patterns even under sustained selection on synonymous codon sites.

    Keywords
    Codon Usage, Lactobacillus, Bifidobacterium, GC content
    National Category
    Evolutionary Biology
    Research subject
    Biology with specialization in Molecular Evolution
    Identifiers
    urn:nbn:se:uu:diva-300909 (URN)10.1093/gbe/evw201 (DOI)000414778600006 ()27540085 (PubMedID)
    Funder
    Swedish Research Council, 349-2007-8732 621-2014-4460Knut and Alice Wallenberg Foundation, 2011.0148 2012.0075
    Available from: 2016-08-15 Created: 2016-08-15 Last updated: 2018-02-14Bibliographically approved
    5. The genome of Rhizobiales bacteria in predatory ants indicates a role for urease in lifestyle switches
    Open this publication in new window or tab >>The genome of Rhizobiales bacteria in predatory ants indicates a role for urease in lifestyle switches
    Show others...
    2016 (English)Article in journal (Refereed) Submitted
    Abstract [en]

    Bacterial symbionts provide amino acids to herbivorous ants, but their role in carnivores is a puzzle. The most prevalent bacterial lineage in ants belongs to the order Rhizobiales. Sequence reads with similarity to Bartonella, a member of the Rhizobiales, were identified in the data collected in a genome project of the carnivorous ant Harpegnatos saltator. Here, we present an analysis of the closed 1.86 Mb genome of the Bartonella-like bacterium, here abbreviated Bhsal. A phylogenetic study showed that Bhsal diverged prior to the radiation of the Bartonella species. Uniquely present in the Bhsal genome is a gene for a giant protein of 6,177 amino acids with a repeated domain structure. We also identified genes for a multi- subunit urease protein complex, potentially involved in the hydrolysis of urea into ammonium. We hypothesize that the urease function protects Bhsal from the acidic environment of the ant gut. The urease genes are also present in Brucella, which has a fecal-oral transmission pathway, but they have been lost in Bartonella species, which use blood-borne transmission pathways. Taken together, the results suggest that the urease function has served an important role for transmission strategies and lifestyle changes in the host-associated members of the Rhizobiales.

    Keywords
    symbiosis, genomics, Bartonella
    National Category
    Evolutionary Biology
    Research subject
    Biology with specialization in Molecular Evolution
    Identifiers
    urn:nbn:se:uu:diva-301778 (URN)
    Available from: 2016-08-25 Created: 2016-08-25 Last updated: 2017-01-13Bibliographically approved
    6. Origin and evolution of the Bartonella Gene Transfer Agent
    Open this publication in new window or tab >>Origin and evolution of the Bartonella Gene Transfer Agent
    Show others...
    2018 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 2, p. 451-464Article in journal (Refereed) Published
    Abstract [en]

    Gene transfer agents (GTAs) are domesticated bacteriophages that have evolved into molecular machines for the transferof bacterial DNA. Despite their widespread nature and their biological implications, the mechanisms and selective forcesthat drive the emergence of GTAs are still poorly understood. Two GTAs have been identifiedintheAlphaproteobacteria:the RcGTA, which is widely distributed in a broad range of species; and the BaGTA, which has a restricted host range thatincludes vector-borne intracellular bacteria of the genusBartonella. The RcGTA packages chromosomal DNA randomly,whereas the BaGTA particles contain a relatively higher fraction of genes for host interaction factors that are amplifiedfrom a nearby phage-derived origin of replication. In this study, we compare the BaGTA genes with homologous bac-teriophage genes identified in the genomes ofBartonellaspecies and close relatives. Unlike the BaGTA, the prophagegenes are neither present in all species, nor inserted into homologous genomic sites. Phylogenetic inferences and sub-stitution frequency analyses confirm codivergence of the BaGTA with the host genome, as opposed to multiple integra-tion and recombination events in the prophages. Furthermore, the organizationof segments flanking the BaGTA differsfrom that of the prophages by a few rearrangement events,which have abolished the normal coordination betweenphage genome replication and phage gene expression. Based on the results of our comparative analysis, we propose amodel for how a prophage may be transformed into a GTA that transfers amplified bacterial DNA segments.

    Keywords
    mobile elements, Phage domestication, GTA
    National Category
    Evolutionary Biology
    Research subject
    Biology with specialization in Molecular Evolution
    Identifiers
    urn:nbn:se:uu:diva-301779 (URN)10.1093/molbev/msx299 (DOI)000423713100014 ()29161442 (PubMedID)
    Funder
    Swedish Research Council, 349-2007-8732, 621-2014-4460Knut and Alice Wallenberg Foundation, 2011.0148, 2012.0075
    Available from: 2016-08-25 Created: 2016-08-25 Last updated: 2018-10-23
  • 1096.
    Tamarit, Daniel
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Dyrhage, Karl
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Edblom, Johan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Ås, Joel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Functionally structured genome architectures in Lactobacillus – insights into their variability and evolutionManuscript (preprint) (Other academic)
    Abstract [en]

    Bacterial genome architectures evolve in response to selective pressures on the interplay between replication and gene expression. Several genomes contain a higher fraction of genes coding for proteins involved in information processes near the origin of replication, which is thought to be due to selection for rapid growth. We recently described a novel type of genome architecture in Lactobacillus kunkeei (Tamarit, et al. 2015). In this genome, vertically inherited genes encoding proteins with roles in translation and replication have accumulated in the chromosomal half surrounding the terminus of replication, while species-specific genes, and genes encoding proteins with metabolic and transport functions have accumulated in the chromosomal half around the origin of replication. Here, we show that this pattern is present also in the closest relatives of L. kunkeei, and similar but not identical biased genome architectures are present in other groups within the Lactobacillaceae. Thus, the biased genome structure in L. kunkeei has emerged from an ancestral clustering of vertically inherited genes around the terminus of replication, while horizontally acquired genes have been inserted near the origin of replication. The genome bias has been lost independently in several groups due to insertions of mobile elements near the terminus of replication and/or major genome rearrangements. We propose chromosomal structuring in macrodomains in the Lactobacillaceae, and suggest that further exploration of its functional consequences and generality will provide valuable insights into the forces that shape genome organization in bacteria. 

  • 1097.
    Tamarit, Daniel
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Ellegaard, Kirsten Maren
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Wikander, Johan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Olofsson, Tobias
    Lund University.
    Vásquez, Alejandra
    Lund University.
    Andersson, Siv
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Comparative Genomics of Lactobacillus kunkeii indicates Selection for Rapid Growth in the BeebreadManuscript (preprint) (Other academic)
  • 1098.
    Tamarit, Daniel
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Neuvonen, Minna M.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Engel, Philipp
    University of Lausanne.
    Guy, Lionel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab. Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Andersson, Siv G. E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Origin and evolution of the Bartonella Gene Transfer Agent2018In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 2, p. 451-464Article in journal (Refereed)
    Abstract [en]

    Gene transfer agents (GTAs) are domesticated bacteriophages that have evolved into molecular machines for the transferof bacterial DNA. Despite their widespread nature and their biological implications, the mechanisms and selective forcesthat drive the emergence of GTAs are still poorly understood. Two GTAs have been identifiedintheAlphaproteobacteria:the RcGTA, which is widely distributed in a broad range of species; and the BaGTA, which has a restricted host range thatincludes vector-borne intracellular bacteria of the genusBartonella. The RcGTA packages chromosomal DNA randomly,whereas the BaGTA particles contain a relatively higher fraction of genes for host interaction factors that are amplifiedfrom a nearby phage-derived origin of replication. In this study, we compare the BaGTA genes with homologous bac-teriophage genes identified in the genomes ofBartonellaspecies and close relatives. Unlike the BaGTA, the prophagegenes are neither present in all species, nor inserted into homologous genomic sites. Phylogenetic inferences and sub-stitution frequency analyses confirm codivergence of the BaGTA with the host genome, as opposed to multiple integra-tion and recombination events in the prophages. Furthermore, the organizationof segments flanking the BaGTA differsfrom that of the prophages by a few rearrangement events,which have abolished the normal coordination betweenphage genome replication and phage gene expression. Based on the results of our comparative analysis, we propose amodel for how a prophage may be transformed into a GTA that transfers amplified bacterial DNA segments.

  • 1099. Tamas, I
    et al.
    Klasson, L M
    Sandström, J P
    Andersson, S G
    Mutualists and parasites: how to paint yourself into a (metabolic) corner.2001In: FEBS Letters, ISSN 0014-5793, E-ISSN 1873-3468, Vol. 498, no 2-3, p. 135-9Article in journal (Refereed)
    Abstract [en]

    Eukaryotes have developed an elaborate series of interactions with bacteria that enter their bodies and/or cells. Genome evolution of symbiotic and parasitic bacteria multiplying inside eukaryotic cells results in both convergent and divergent changes. The genome sequences of the symbiotic bacteria of aphids, Buchnera aphidicola, and the parasitic bacteria of body louse and humans, Rickettsia prowazekii, provide insights into these processes. Convergent genome characteristics include reduction in genome sizes and lowered G+C content values. Divergent evolution was recorded for amino acid and cell wall biosynthetic genes. The presence of pseudogenes in both genomes provides examples of recent gene inactivation events and offers clues to the process of genome deterioration and host-cell adaptation.

  • 1100. Tamas, Ivica
    et al.
    Klasson, Lisa
    Canbäck, Björn
    Näslund, A Kristina
    Eriksson, Ann-Sofie
    Wernegreen, Jennifer J
    Sandström, Jonas P
    Moran, Nancy A
    Andersson, Siv G E
    50 million years of genomic stasis in endosymbiotic bacteria.2002In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 296, no 5577, p. 2376-9Article in journal (Refereed)
    Abstract [en]

    Comparison of two fully sequenced genomes of Buchnera aphidicola, the obligate endosymbionts of aphids, reveals the most extreme genome stability to date: no chromosome rearrangements or gene acquisitions have occurred in the past 50 to 70 million years, despite substantial sequence evolution and the inactivation and loss of individual genes. In contrast, the genomes of their closest free-living relatives, Escherichia coli and Salmonella spp., are more than 2000-fold more labile in content and gene order. The genomic stasis of B. aphidicola, likely attributable to the loss of phages, repeated sequences, and recA, indicates that B. aphidicola is no longer a source of ecological innovation for its hosts.

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