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  • 151.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    En omöjlig logik2009In: Humanisten, Vol. 1Article in journal (Other (popular science, discussion, etc.))
  • 152.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Evolution, phylogeny, sexual dimorphism and mating system in the grackles (Quiscalus spp, Icterinae)1991In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 45, p. 608-621Article in journal (Refereed)
  • 153.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Evoluutiobiologia2008Book (Other academic)
  • 154.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Introduccion a la Ecologia Evolutiva1998In: Etologuia, Vol. 6, p. 11-20Article in journal (Refereed)
  • 155.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Optimal choice in a neural network2002In: Journal of Theoretical Biology, ISSN 0022-5193, E-ISSN 1095-8541, Vol. 218, p. 149-154Article in journal (Refereed)
  • 156.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Patterns of morphological variation among Cardueline finches (Fringillidae, Carduelinae)1991In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 43, p. 239-248Article in journal (Refereed)
  • 157.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Phenotypic variation in growth trajectories in finches1993In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 47, p. 1506-1514Article in journal (Refereed)
  • 158.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Processes generating macroevolutionary patterns of morphological variation in birds1994In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 7, p. 727-742Article in journal (Refereed)
  • 159.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Selection of bill size proportions in the common rosefinch (Carpodacus erythrinus)1992In: The AUK: A Quarterly Journal of Ornithology, ISSN 0004-8038, E-ISSN 1938-4254, Vol. 109, p. 637-642Article in journal (Refereed)
  • 160.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Similarity of growth among great tits (Parus major) and blue tits (P. caeruleus)1996In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 58, p. 343-355Article in journal (Refereed)
  • 161.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Speciation in birds - a complete picture2002In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 15, p. 1095-1096Article, book review (Other academic)
  • 162.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Species selection on organismal integration1994In: Journal of Theoretical Biology, ISSN 0022-5193, E-ISSN 1095-8541, Vol. 171, p. 427-430Article in journal (Refereed)
  • 163.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    The effect of male presence on nestling growth and fluctuating asymmetry in the Blue Tit1996In: The Condor, ISSN 0010-5422, E-ISSN 1938-5129, Vol. 98, p. 172-175Article in journal (Refereed)
  • 164.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    The importance of evolutionary constraints in ecological time scales1996In: Evolutionary Ecology, ISSN 0269-7653, E-ISSN 1573-8477, p. 423-431Article in journal (Refereed)
  • 165.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    The independent contrast method in comparative biology1994In: Cladistics, ISSN 0748-3007, E-ISSN 1096-0031, p. 425-433Article in journal (Refereed)
  • 166.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Variation in growth in the Blue tit (Parus caeruleus)1997In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 10, p. 139-155Article in journal (Refereed)
  • 167.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Why some measures of fluctuating asymmetry are so sensitive to measurement error1997In: Acta Zoologica Fennica, ISSN 0001-7299, Vol. 34, p. 133-137Article in journal (Refereed)
  • 168.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Aho, Teija
    Behrmann-Godel, Jasminca
    Isolation over 35 years in a heated biotest basin causes selection on MHC class II beta genes in the European perch (Perca fluviatilis L.)2015In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 5, no 7, p. 1440-1455Article in journal (Refereed)
    Abstract [en]

    Genes that play key roles in host immunity such as the major histocompatibility complex (MHC) in vertebrates are expected to be major targets of selection. It is well known that environmental conditions can have an effect on host-parasite interactions and may thus influence the selection on MHC. We analyzed MHC class II ss variability over 35years in a population of perch (Perca fluviatilis) from the Baltic Sea that was split into two populations separated from each other. One population was subjected to heating from cooling water of a nuclear power plant and was isolated from the surrounding environment in an artificial lake, while the other population was not subjected to any change in water temperature (control). The isolated population experienced a change of the allelic composition and a decrease in allelic richness of MHC genes compared to the control population. The two most common MHC alleles showed cyclic patterns indicating ongoing parasite-host coevolution in both populations, but the alleles that showed a cyclic behavior differed between the two populations. No such patterns were observed at alleles from nine microsatellite loci, and no genetic differentiation was found between populations. We found no indications for a genetic bottleneck in the isolated population during the 35years. Additionally, differences in parasitism of the current perch populations suggest that a change of the parasite communities has occurred over the isolation period, although the evidence in form of in-depth knowledge of the change of the parasite community over time is lacking. Our results are consistent with the hypothesis of a selective sweep imposed by a change in the parasite community.

  • 169.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Subtle but ubiquitous selection on body size in a natural population of collared flycatchers over 33years2017In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 30, no 7, p. 1386-1399Article in journal (Refereed)
    Abstract [en]

    Understanding the magnitude and long-term patterns of selection in natural populations is of importance, for example, when analysing the evolutionary impact of climate change. We estimated univariate and multivariate directional, quadratic and correlational selection on four morphological traits (adult wing, tarsus and tail length, body mass) over a time period of 33years (approximate to 19000 observations) in a nest-box breeding population of collared flycatchers (Ficedula albicollis). In general, selection was weak in both males and females over the years regardless of fitness measure (fledged young, recruits and survival) with only few cases with statistically significant selection. When data were analysed in a multivariate context and as time series, a number of patterns emerged; there was a consistent, but weak, selection for longer wings in both sexes, selection was stronger on females when the number of fledged young was used as a fitness measure, there were no indications of sexually antagonistic selection, and we found a negative correlation between selection on tarsus and wing length in both sexes but using different fitness measures. Uni- and multivariate selection gradients were correlated only for wing length and mass. Multivariate selection gradient vectors were longer than corresponding vector of univariate gradients and had more constrained direction. Correlational selection had little importance. Overall, the fitness surface was more or less flat with few cases of significant curvature, indicating that the adaptive peak with regard to body size in this species is broader than the phenotypic distribution, which has resulted in weak estimates of selection.

  • 170.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Linden, Mats
    Sexual size dimorphism in the Great tit (Parus major) in relation to history and current selection1993In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 6, p. 397-415Article in journal (Refereed)
  • 171.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Merilä, Juha
    Fluctuating asymmetry and measurement error1995In: Systematic Biology, ISSN 1063-5157, E-ISSN 1076-836X, Vol. 44, p. 97-101Article in journal (Refereed)
  • 172.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Merilä, Juha
    Morphological differentiation in Carduelis finches1993In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 6, p. 359-373Article in journal (Refereed)
  • 173.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Merilä, Juha
    Population divergence and morphometric integration in the greenfinch (Carduelis chloris)- evolution against the trajectory of least resistance1999In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 12, p. 103-112Article in journal (Refereed)
  • 174.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Merilä, Juha
    Baker, Alan J
    Historical demography and present day population structure of the Greenfinch (Carduelis chloris) - an analysis of mtDNA control-region sequences1997In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 51, p. 946-956Article in journal (Refereed)
  • 175.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Merilä, Juha
    Bennet, GF
    Geographic and individual variation on haematozoan infections in the greenfinch, Carduelis chloris1995In: Canadian Journal of Zoology, ISSN 0008-4301, E-ISSN 1480-3283, Vol. 73, p. 1798-1804Article in journal (Refereed)
  • 176.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Merilä, Juha
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Evolution of morphological differences with moderate genetic correlations among traits as exemplified by two flycatcher species (Ficedula, Muscicapidae)1994In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 52, p. 19-30Article in journal (Refereed)
  • 177.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ranta, Esa
    Kaitala, Veijo
    Lundberg, Per
    Bach, Lars
    Stenseth, Nils Christian
    Environmental forcing and genetic differentiation in subdivided populations2008In: Evolutionary Ecology Research, ISSN 1522-0613, E-ISSN 1937-3791, Vol. 10, p. 1-9Article in journal (Refereed)
  • 178.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Senar, Juan Carlos
    Sex differences in survival selection in serins (Carduelis serinus)2001In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 14, p. 841-849Article in journal (Refereed)
  • 179.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Spong, Göran
    Creel, Scott
    Stone, Jon
    Genetic structure of a population of lions (Panthera leo) in the Selous Game Reserve: implications for the evolution of sociality2002In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 15, p. 945-953-Article in journal (Refereed)
  • 180.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Spong, Göran
    Johansson, Malin
    High genetic variation in leopards indicates large and long-term stable effective population size2000In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 9, p. 1773-1782Article in journal (Refereed)
  • 181.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Stone, Jon
    Delayed prezygotic isolating mechansims: evolution with a twist2002In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 269, p. 861-865Article in journal (Refereed)
  • 182.
    Björklund, Mats
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Stone, Jon
    Delrious: a computer program designed to analyse molecular maraker data and calculate delta and relatedness esimtaes with confidence2001In: Molecular Ecology Notes, ISSN 1471-8278, E-ISSN 1471-8286, Vol. 1, p. 209-214Article in journal (Refereed)
  • 183. Blackburn, Tim
    et al.
    Monroe, Melanie
    Lawson, Becki
    Phill, Cassey
    Ewen, John
    Body size changes in passerine birds introduced to New Zealand from the UK2013In: NeoBiota, ISSN 1619-0033, E-ISSN 1314-2488, Vol. 17, p. 1-18Article in journal (Refereed)
  • 184.
    Blair, Matthew W.
    et al.
    Department of Plant Breeding and Genetics, Cornell University.
    Cortés, Andres J.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Penmetsa, R.Varma
    University of California, Davis.
    Farmer, Andrew
    National Center for Genomic Research, Albuquerque.
    Carrasquilla-Garcia, Noelia
    University of California, Davis.
    Cook, Doug R.
    University of California, Davis.
    A high-throughput SNP marker system for parental polymorphism screening, and diversity analysis in common bean (Phaseolus vulgaris L.)2013In: Theoretical and Applied Genetics, ISSN 0040-5752, E-ISSN 1432-2242, Vol. 126, no 2, p. 535-548Article in journal (Refereed)
    Abstract [en]

    Single nucleotide polymorphism (SNP) detection has become a marker system of choice, because of the high abundance of source polymorphisms and the ease with which allele calls are automated. Various technologies exist for the evaluation of SNP loci and previously we validated two medium throughput technologies. In this study, our goal was to utilize a 768 feature, Illumina GoldenGate assay for common bean (Phaseolus vulgaris L.) developed from conserved legume gene sequences and to use the new technology for (1) the evaluation of parental polymorphisms in a mini-core set of common bean accessions and (2) the analysis of genetic diversity in the crop. A total of 736 SNPs were scored on 236 diverse common bean genotypes with the GoldenGate array. Missing data and heterozygosity levels were low and 94 % of the SNPs were scorable. With the evaluation of the parental polymorphism genotypes, we estimated the utility of the SNP markers in mapping for inter-genepool and intra-genepool populations, the latter being of lower polymorphism than the former. When we performed the diversity analysis with the diverse genotypes, we found Illumina GoldenGate SNPs to provide equivalent evaluations as previous gene-based SNP markers, but less fine-distinctions than with previous microsatellite marker analysis. We did find, however, that the gene-based SNPs in the GoldenGate array had some utility in race structure analysis despite the low polymorphism. Furthermore the SNPs detected high heterozygosity in wild accessions which was probably a reflection of ascertainment bias. The Illumina SNPs were shown to be effective in distinguishing between the genepools, and therefore were most useful in saturation of inter-genepool genetic maps. The implications of these results for breeding in common bean are discussed as well as the advantages and disadvantages of the GoldenGate system for SNP detection.

  • 185.
    Bloch, Natasha, I
    et al.
    UCL, Dept Genet Evolut & Environm, London, England.
    Corral-Lopez, Alberto
    Stockholm Univ, Dept Zool Ethol, Stockholm, Sweden.
    Buechel, Severine D.
    Stockholm Univ, Dept Zool Ethol, Stockholm, Sweden.
    Kotrschal, Alexander
    Stockholm Univ, Dept Zool Ethol, Stockholm, Sweden.
    Kolm, Niclas
    Stockholm Univ, Dept Zool Ethol, Stockholm, Sweden.
    Mank, Judith E.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology. UCL, Dept Genet Evolut & Environm, London, England.
    Early neurogenomic response associated with variation in guppy female mate preference2018In: Nature Ecology & Evolution, E-ISSN 2397-334X, Vol. 2, no 11, p. 1772-1781Article in journal (Refereed)
    Abstract [en]

    Understanding the evolution of mate choice requires dissecting the mechanisms of female preference, particularly how these differ among social contexts and preference phenotypes. Here, we studied the female neurogenomic response after only 10 min of mate exposure in both a sensory component (optic tectum) and a decision-making component (telencephalon) of the brain. By comparing the transcriptional response between females with and without preferences for colourful males, we identified unique neurogenomic elements associated with the female preference phenotype that are not present in females without preference. A network analysis revealed different properties for this response at the sensory-processing and the decision-making levels, and we show that this response is highly centralized in the telencephalon. Furthermore, we identified an additional set of genes that vary in expression across social contexts, beyond mate evaluation. We show that transcription factors among these loci are predicted to regulate the transcriptional response of the genes we found to be associated with female preference.

  • 186.
    Blom, Henning
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Jerve, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Qu, Qin Ming
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Chen, Dong Lei
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Märss, Tiiu
    Tallinn University of Technology.
    Dupret, Vincent
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Sanchez, Sophie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Ahlberg, Per
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Affinities of Lophosteus and the origin of the osteichthyan body plan2011In: / [ed] Streng, Kear, 2011, p. 3-4Conference paper (Refereed)
  • 187.
    Blom, Henning
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Jerve, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Qu, Qinming
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Chen, Dong Lei
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Märss, Tiiu
    Tallinn University of Technology.
    Dupret, Vincent
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Sanchez, Sophie
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    Ahlberg, Per
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
    The affinity of Lophosteus  and the evolution of osteichthyan characters2011Conference paper (Refereed)
  • 188.
    Bodare, Sofia
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Functional Genomics. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Stocks, Michael
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Yang, J-C
    Taiwan Forestry Research Institute.
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Origin and demographic history of the endemic Taiwan spruce (Picea morrisonicola)2013In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 3, no 10, p. 3320-3333Article in journal (Refereed)
    Abstract [en]

    Taiwan spruce (Picea morrisonicola) is a vulnerable conifer species endemic to the island of Taiwan. A warming climate and competition from subtropical tree species has limited the range of Taiwan spruce to the higher altitudes of the island. Using seeds sampled from an area in the central mountain range of Taiwan, 15 nuclear loci were sequenced in order to measure genetic variation and to assess the long-term genetic stability of the species. Genetic diversity is low and comparable to other spruce species with limited ranges such as Picea breweriana, Picea chihuahuana, and Picea schrenkiana. Importantly, analysis using approximate Bayesian computation (ABC) provides evidence for a drastic decline in the effective population size approximately 0.3–0.5 million years ago (mya). We used simulations to show that this is unlikely to be a false-positive result due to the limited sample used here. To investigate the phylogenetic origin of Taiwan spruce, additional sequencing was performed in the Chinese spruce Picea wilsonii and combined with previously published data for three other mainland China species, Picea purpurea, Picea likiangensis, and P. schrenkiana. Analysis of population structure revealed that P. morrisonicola clusters most closely with P. wilsonii, and coalescent analyses using the program MIMAR dated the split to 4–8 mya, coincidental to the formation of Taiwan. Considering the population decrease that occurred after the split, however, led to a much more recent origin.

  • 189.
    Bogusz, Marcin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Evolutionary Approaches to Sequence Alignment2018Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Molecular evolutionary biology allows us to look into the past by analyzing sequences of amino acids or nucleotides. These analyses can be very complex, often involving advanced statistical models of sequence evolution to construct phylogenetic trees, study the patterns of natural selection and perform a number of other evolutionary studies. In many cases, these evolutionary studies require a prerequisite of multiple sequence alignment (MSA) - a technique, which aims at grouping the characters that share a common ancestor, or homology, into columns. This information regarding shared homology is needed by statistical models to describe the process of substitutions in order to perform evolutionary inference. Sequence alignment, however, is difficult and MSAs often contain whole regions of wrongly aligned characters, which impact downstream analyses.

    In this thesis I use two broad groups of approaches to avoid errors in the alignment. The first group addresses the analysis methods without sequence alignment by explicitly modelling the processes of substitutions, and insertions and deletions (indels) between pairs of sequences using pair hidden Markov models. I describe an accurate tree inference method that uses a neighbor joining clustering approach to construct a tree from a matrix of model-based evolutionary distances.

    Next, I develop a pairwise method of modelling how natural selection acts on substitutions and indels. I further show the relationship between the constraints acting on these two evolutionary forces to show that natural selection affects them in a similar way.

    The second group of approaches deals with errors in existing alignments. I use a statistical model-based approach to evaluate the quality of multiple sequence alignments.

    First, I provide a graph-based tool for removing wrongly aligned pairs of residues by splitting them apart. This approach tends to produce better results when compared to standard column-based filtering.

    Second, I provide a way to compare MSAs using a probabilistic framework. I propose new ways of scoring of sequence alignments and show that popular methods produce similar results.

    The overall purpose of this work is to facilitate more accurate evolutionary analyses by addressing the problem of sequence alignment in a statistically rigorous manner.

    List of papers
    1. Phylogenetic Tree Estimation With and Without Alignment: New Distance Methods and Benchmarking
    Open this publication in new window or tab >>Phylogenetic Tree Estimation With and Without Alignment: New Distance Methods and Benchmarking
    2017 (English)In: Systematic Biology, ISSN 1063-5157, E-ISSN 1076-836X, Vol. 66, no 2, p. 218-231Article in journal (Refereed) Published
    Abstract [en]

    Phylogenetic tree inference is a critical component of many systematic and evolutionary studies. The majority of these studies are based on the two-step process of multiple sequence alignment followed by tree inference, despite persistent evidence that the alignment step can lead to biased results. Here we present a two-part study that first presents PaHMM-Tree, a novel neighbor joining-based method that estimates pairwise distances without assuming a single alignment. We then use simulations to benchmark its performance against a wide-range of other phylogenetic tree inference methods, including the first comparison of alignment-free distance-based methods against more conventional tree estimation methods. Our new method for calculating pairwise distances based on statistical alignment provides distance estimates that are as accurate as those obtained using standard methods based on the true alignment. Pairwise distance estimates based on the two-step process tend to be substantially less accurate. This improved performance carries through to tree inference, where PaHMM-Tree provides more accurate tree estimates than all of the pairwise distance methods assessed. For close to moderately divergent sequence data we find that the two-step methods using statistical inference, where information from all sequences is included in the estimation procedure, tend to perform better than PaHMM-Tree, particularly full statistical alignment, which simultaneously estimates both the tree and the alignment. For deep divergences we find the alignment step becomes so prone to error that our distance-based PaHMM-Tree outperforms all other methods of tree inference. Finally, we find that the accuracy of alignment-free methods tends to decline faster than standard two-step methods in the presence of alignment uncertainty, and identify no conditions where alignment-free methods are equal to or more accurate than standard phylogenetic methods even in the presence of substantial alignment error.

    Keywords
    Alignment-free, distance-based phylogenetics, pair Hidden Markov Models, phylogenetic inference, statistical alignment
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-316533 (URN)10.1093/sysbio/syw074 (DOI)000397703800009 ()27633353 (PubMedID)
    Available from: 2017-03-02 Created: 2017-03-02 Last updated: 2018-09-19Bibliographically approved
    2. Selection acting on indels and substitutions in protein coding sequences
    Open this publication in new window or tab >>Selection acting on indels and substitutions in protein coding sequences
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Patterns of selection acting on an expressed protein act to maintain or adapt its structure and function over time. The most widely used method for studying these selective forces is the ratio of synonymous to non-synonymous substitutions (dN/dS), which helps distinguish between neutral, purifying (negative), and adaptive (positive) selection. This ratio, however, examines only amino acid substitutions and ignores other evolutionary forces like small-scale insertions and deletions (indels) that may affect protein evolution. There are currently no statistically robust methods for studying the forces acting on protein sequence indels, with the few ad hoc solutions highly dependent on the gap patterns produced by alignment and filtering steps. This study broadens our understanding of how selection acts on indels in proteins by explicitly examining the relationship between selective constraint acting on substitutions and indels. We present a probabilistic model that jointly estimates dN/dS and the indel rate through statistical alignment, which removes biases in both parameter estimates caused by alignment error. We apply our method to thousands of genes from human-mouse and human-chicken pairwise analyses, revealing that the indel rate and selection (dN/dS) tends to be related, demonstrating that purifying selection acting in proteins tends to affect non-synonymous mutations and indels in a quantifiably similar way. We also investigate how the selective forces acting on substitutions and indels vary along genes. Our findings and methods offer the opportunity to begin studying the interaction between substitutions and indels, and the first widely applicable tools for understanding how they impact protein evolution.

    Keywords
    Natural Selection, Protein Evolution, Pair hidden Markov models
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-360838 (URN)
    Available from: 2018-09-18 Created: 2018-09-18 Last updated: 2018-09-19
    3. A graph-based approach for improving the homologyinference in multiple sequence alignments
    Open this publication in new window or tab >>A graph-based approach for improving the homologyinference in multiple sequence alignments
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Multiple sequence alignment (MSA) is ubiquitous in evolutionary studies and other areas ofbioinformatics. In nearly all cases MSAs are taken to be a known and xed quantity on which toperform downstream analysis despite extensive evidence that MSA accuracy and uncertainty aectsresults. Mistakes in the MSA are known to cause a wide range of problems for downstream evolutionaryinference, ranging from false inference of positive selection to long branch attraction artifacts. The mostpopular approach to dealing with this problem is to remove (lter) specic columns in the MSA thatare thought to be prone to error, either through proximity to gaps or through some scoring function.Although popular, this approach has had mixed success and several studies have even suggested thatltering might be detrimental to phylogenetic studies. Here we present a dierent approach to dealingwith MSA accuracy and uncertainty through a graph-based approach implemented in the freely availablesoftware Divvier. The aim of Divvier is to identify clusters of characters that have strong statisticalevidence of shared homology, based on the output of a pair hidden Markov model. These clusters canthen be used to either lter characters out the MSA, through a process we call partial ltering, or torepresent each of the clusters in a new column, through a process we call divvying up. We validateour approach through its performance on real and simulated benchmarks, nding Divvier substantiallyoutperforms all other ltering software for treating MSAs by retaining more true positive homology callsand removing more false positive homology calls. We also nd that Divvier, in contrast to other lteringtools, can alleviate long branch attraction artifacts induced by MSA and reduces the variation in treeestimates caused by MSA uncertainty.

    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-360839 (URN)
    Available from: 2018-09-18 Created: 2018-09-18 Last updated: 2018-09-21
    4. Examining sequence alignments using a model-based approach
    Open this publication in new window or tab >>Examining sequence alignments using a model-based approach
    (English)Manuscript (preprint) (Other academic)
    Abstract [en]

    Multiple sequence alignment (MSA) is a commonly performed procedure required for a number of evolutionary and comparative analyses. The common two-step process of sequence alignment followed by statistical phylogenetic inference depends on MSA quality. MSA is computationally difficult and as a result in many cases sequence alignments contain regions of spurious homologies. These errors in the alignment affect downstream results, so choosing an accurate MSA is critical.  Researchers often face the problem of choosing an aligner out of many multiple sequence alignment methods (MSAMs). This choice is often based on the results of benchmarks with various popular methods claiming high accuracy scores. These methods compete to obtain the highest scores in the commonly used sum-of-pairs benchmark—which accounts for a fraction of the true homologies recovered—ignoring the fraction of introduced false positive homologies. Furthermore, these benchmarks do not account for the fact that some homologies are more difficult to recover than the others. We take a probabilistic model-based approach to examine the quality of pairwise homologies returned by four popular MSAMs. We use pair-hidden Markov models to break down alignment columns into pairs and obtain distributions of pairwise posterior scores for these aligners. Basing our results on a structural benchmark and a simulation study, we find that MSAMs appear to return a sample from a confidence set defined by high posterior probabilities. Furthermore, we find that the reference alignment contains low pairwise posterior portions of pairwise homologies which cannot be expected to be recovered by any MSAM. Finally, we look at several possible test statistics, with and without the need for reference alignments, and ultimately suggest using positive predictive value (PPV) and mean posterior probability for MSA evaluation.

    Keywords
    Sequence alignment, alignment accuracy, alignment uncertainty, pair hidden Markov models
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-360840 (URN)
    Available from: 2018-09-19 Created: 2018-09-19 Last updated: 2018-09-21
  • 190.
    Bogusz, Marcin
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ali, Raja Hashim
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Whelan, Simon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Examining sequence alignments using a model-based approachManuscript (preprint) (Other academic)
    Abstract [en]

    Multiple sequence alignment (MSA) is a commonly performed procedure required for a number of evolutionary and comparative analyses. The common two-step process of sequence alignment followed by statistical phylogenetic inference depends on MSA quality. MSA is computationally difficult and as a result in many cases sequence alignments contain regions of spurious homologies. These errors in the alignment affect downstream results, so choosing an accurate MSA is critical.  Researchers often face the problem of choosing an aligner out of many multiple sequence alignment methods (MSAMs). This choice is often based on the results of benchmarks with various popular methods claiming high accuracy scores. These methods compete to obtain the highest scores in the commonly used sum-of-pairs benchmark—which accounts for a fraction of the true homologies recovered—ignoring the fraction of introduced false positive homologies. Furthermore, these benchmarks do not account for the fact that some homologies are more difficult to recover than the others. We take a probabilistic model-based approach to examine the quality of pairwise homologies returned by four popular MSAMs. We use pair-hidden Markov models to break down alignment columns into pairs and obtain distributions of pairwise posterior scores for these aligners. Basing our results on a structural benchmark and a simulation study, we find that MSAMs appear to return a sample from a confidence set defined by high posterior probabilities. Furthermore, we find that the reference alignment contains low pairwise posterior portions of pairwise homologies which cannot be expected to be recovered by any MSAM. Finally, we look at several possible test statistics, with and without the need for reference alignments, and ultimately suggest using positive predictive value (PPV) and mean posterior probability for MSA evaluation.

  • 191.
    Bogusz, Marcin
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Whelan, Simon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Phylogenetic Tree Estimation With and Without Alignment: New Distance Methods and Benchmarking2017In: Systematic Biology, ISSN 1063-5157, E-ISSN 1076-836X, Vol. 66, no 2, p. 218-231Article in journal (Refereed)
    Abstract [en]

    Phylogenetic tree inference is a critical component of many systematic and evolutionary studies. The majority of these studies are based on the two-step process of multiple sequence alignment followed by tree inference, despite persistent evidence that the alignment step can lead to biased results. Here we present a two-part study that first presents PaHMM-Tree, a novel neighbor joining-based method that estimates pairwise distances without assuming a single alignment. We then use simulations to benchmark its performance against a wide-range of other phylogenetic tree inference methods, including the first comparison of alignment-free distance-based methods against more conventional tree estimation methods. Our new method for calculating pairwise distances based on statistical alignment provides distance estimates that are as accurate as those obtained using standard methods based on the true alignment. Pairwise distance estimates based on the two-step process tend to be substantially less accurate. This improved performance carries through to tree inference, where PaHMM-Tree provides more accurate tree estimates than all of the pairwise distance methods assessed. For close to moderately divergent sequence data we find that the two-step methods using statistical inference, where information from all sequences is included in the estimation procedure, tend to perform better than PaHMM-Tree, particularly full statistical alignment, which simultaneously estimates both the tree and the alignment. For deep divergences we find the alignment step becomes so prone to error that our distance-based PaHMM-Tree outperforms all other methods of tree inference. Finally, we find that the accuracy of alignment-free methods tends to decline faster than standard two-step methods in the presence of alignment uncertainty, and identify no conditions where alignment-free methods are equal to or more accurate than standard phylogenetic methods even in the presence of substantial alignment error.

  • 192.
    Bogusz, Marcin
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Whelan, Simon
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Selection acting on indels and substitutions in protein coding sequencesManuscript (preprint) (Other academic)
    Abstract [en]

    Patterns of selection acting on an expressed protein act to maintain or adapt its structure and function over time. The most widely used method for studying these selective forces is the ratio of synonymous to non-synonymous substitutions (dN/dS), which helps distinguish between neutral, purifying (negative), and adaptive (positive) selection. This ratio, however, examines only amino acid substitutions and ignores other evolutionary forces like small-scale insertions and deletions (indels) that may affect protein evolution. There are currently no statistically robust methods for studying the forces acting on protein sequence indels, with the few ad hoc solutions highly dependent on the gap patterns produced by alignment and filtering steps. This study broadens our understanding of how selection acts on indels in proteins by explicitly examining the relationship between selective constraint acting on substitutions and indels. We present a probabilistic model that jointly estimates dN/dS and the indel rate through statistical alignment, which removes biases in both parameter estimates caused by alignment error. We apply our method to thousands of genes from human-mouse and human-chicken pairwise analyses, revealing that the indel rate and selection (dN/dS) tends to be related, demonstrating that purifying selection acting in proteins tends to affect non-synonymous mutations and indels in a quantifiably similar way. We also investigate how the selective forces acting on substitutions and indels vary along genes. Our findings and methods offer the opportunity to begin studying the interaction between substitutions and indels, and the first widely applicable tools for understanding how they impact protein evolution.

  • 193.
    Bolivar, Paulina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Gueguen, Laurent
    Univ Claude Bernard Lyon 1, CNRS, UMR 5558, Lab Biol & Biometrie Evolut, Lyon, France.
    Duret, Laurent
    Univ Claude Bernard Lyon 1, CNRS, UMR 5558, Lab Biol & Biometrie Evolut, Lyon, France.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Mugal, Carina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    GC-biased gene conversion conceals the prediction of the nearly neutral theory in avian genomes2019In: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 20, article id 5Article in journal (Refereed)
    Abstract [en]

    Background: The nearly neutral theory of molecular evolution predicts that the efficacy of natural selection increases with the effective population size. This prediction has been verified by independent observations in diverse taxa, which show that life-history traits are strongly correlated with measures of the efficacy of selection, such as the d(N)/d(S) ratio. Surprisingly, avian taxa are an exception to this theory because correlations between life-history traits and d(N)/d(S) are apparently absent. Here we explore the role of GC-biased gene conversion on estimates of substitution rates as a potential driver of these unexpected observations.

    Results: We analyze the relationship between d(N)/d(S) estimated from alignments of 47 avian genomes and several proxies for effective population size. To distinguish the impact of GC-biased gene conversion from selection, we use an approach that accounts for non-stationary base composition and estimate d(N)/d(S) separately for changes affected or unaffected by GC-biased gene conversion. This analysis shows that the impact of GC-biased gene conversion on substitution rates can explain the lack of correlations between life-history traits and d(N)/d(S). Strong correlations between life-history traits and d(N)/d(S) are recovered after accounting for GC-biased gene conversion. The correlations are robust to variation in base composition and genomic location.

    Conclusions: Our study shows that gene sequence evolution across a wide range of avian lineages meets the prediction of the nearly neutral theory,the efficacy of selection increases with effective population size. Moreover, our study illustrates that accounting for GC-biased gene conversion is important to correctly estimate the strength of selection.

  • 194.
    Bolivar, Paulina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Mugal, Carina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Sebastiano, Matteo Rossi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Ludwig Maximilians Univ Munchen, Fac Biol, Dept Biol 2, Planegg Martinsried, Germany.
    Nater, Alexander
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ Konstanz, Dept Biol, Chair Zool & Evolutionary Biol, Constance, Germany.
    Wang, Mi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Dutoit, Ludovic
    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.
    Biased Inference of Selection Due to GC-Biased Gene Conversion and the Rate of Protein Evolution in Flycatchers When Accounting for It2018In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 10, p. 2475-2486Article in journal (Refereed)
    Abstract [en]

    The rate of recombination impacts on rates of protein evolution for at least two reasons: it affects the efficacy of selection due to linkage and influences sequence evolution through the process of GC-biased gene conversion (gBGC). We studied how recombination, via gBGC, affects inferences of selection in gene sequences using comparative genomic and population genomic data from the collared flycatcher (Ficedula albicollis). We separately analyzed different mutation categories ("strong"-to-"weak" "weak-to-strong," and GC-conservative changes) and found that gBGC impacts on the distribution of fitness effects of new mutations, and leads to that the rate of adaptive evolution and the proportion of adaptive mutations among nonsynonymous substitutions are underestimated by 22-33%. It also biases inferences of demographic history based on the site frequency spectrum. In light of this impact, we suggest that inferences of selection (and demography) in lineages with pronounced gBGC should be based on GC-conservative changes only. Doing so, we estimate that 10% of nonsynonymous mutations are effectively neutral and that 27% of nonsynonymous substitutions have been fixed by positive selection in the flycatcher lineage. We also find that gene expression level, sex-bias in expression, and the number of protein-protein interactions, but not Hill-Robertson interference (HRI), are strong determinants of selective constraint and rate of adaptation of collared flycatcher genes. This study therefore illustrates the importance of disentangling the effects of different evolutionary forces and genetic factors in interpretation of sequence data, and from that infer the role of natural selection in DNA sequence evolution.

  • 195.
    Bolund, Elisabeth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Hayward, Adam
    Pettay, Jenni E.
    Lummaa, Virpi
    Effects of the demographic transition on the genetic variances and covariances of human life-history traits2015In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 69, no 3, p. 747-755Article in journal (Refereed)
    Abstract [en]

    The recent demographic transitions to lower mortality and fertility rates in most human societies have led to changes and even quick reversals in phenotypic selection pressures. This can only result in evolutionary change if the affected traits are heritable, but changes in environmental conditions may also lead to subsequent changes in the genetic variance and covariance (the G matrix) of traits. It currently remains unclear if there have been concomitant changes in the G matrix of life-history traits following the demographic transition. Using 300 years of genealogical data from Finland, we found that four key life-history traits were heritable both before and after the demographic transition. The estimated heritabilities allow a quantifiable genetic response to selection during both time periods, thus facilitating continued evolutionary change. Further, the G matrices remained largely stable but revealed a trend for an increased additive genetic variance and thus evolutionary potential of the population after the transition. Our results demonstrate the validity of predictions of evolutionary change in human populations even after the recent dramatic environmental change, and facilitate predictions of how our biology interacts with changing environments, with implications for global public health and demography.

  • 196.
    Bolund, Elisabeth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lummaa, V.
    Univ Turku, Dept Biol, Turku, Finland..
    The effects of resource availability and the demographic transition on the genetic correlation between number of children and grandchildren in humans2017In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 118, no 2, p. 186-192Article in journal (Refereed)
    Abstract [en]

    Studies of evolutionary change require an estimate of fitness, and lifetime reproductive success is widely used for this purpose. However, many species face a trade-off between the number and quality of offspring and in such cases number of grandoffspring may better represent the genetic contribution to future generations. Here, we apply quantitative genetic methods to a genealogical data set on humans from Finland to address how the genetic correlation between number of children and grandchildren is influenced by the severity of the trade-off between offspring quality and quantity, as estimated by different levels of resource access among individuals in the population. Further, we compare the genetic correlation before and after the demographic transition to low mortality and fertility rates. The genetic correlation was consistently high (0.79-0.92) with the strongest correlations occurring in individuals with higher access to resources and before the demographic transition, and a tendency for lower correlations in resource poor individuals and after the transition. These results indicate that number of grandoffspring is a slightly better predictor of long-term genetic fitness than number of offspring in a human population across a range of environmental conditions, and more generally, that patterns of resource availability need to be taken into account when estimating genetic covariances with fitness.

  • 197.
    Bolívar, Paulina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Rates and patterns of molecular evolution in avian genomes2019Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Evolution is the change in inherited characteristics of a population through subsequent generations. The interplay of several evolutionary mechanisms determines the rate at which this change occurs. In short, genetic variation is generated though mutation, and the fate of these mutations in a population is determined mainly by the combined effect of genetic drift, natural selection and recombination. Elucidating the relative impact of these mechanisms is complex; making it a long-standing question in evolutionary biology. In this thesis, I focus on disentangling the relative roles of these evolutionary mechanisms and genetic factors in determining rates and patterns of evolution at the molecular level, by studying variation in the DNA sequence of multiple avian species, and in particular the collared flycatcher (Ficedula albicollis). Specifically, I aim to further our understanding regarding the impact of recombination rate on genome evolution, through its interaction with the efficacy of selection and through the process of GC-biased gene conversion (gBGC), which has been poorly characterized in birds. I demonstrate that gBGC has a pervasive effect on the genome of the collared flycatcher and other avian species, as it increases the substitution rate and affects interpretations of the impact of natural selection and adaptation. Interestingly, its effect is even stronger in neutrally evolving sites compared to sites evolving under selection. After accounting for gBGC, I disentangle the true impact of natural selection versus non-adaptive processes in determining rates of molecular evolution in the collared flycatcher genome, shedding light on the process of adaptation. Finally, I demonstrate the significant role of recombination through its impact on linked selection, along with mutation rate differences, in determining relative levels of genetic diversity and their relationship to the fast-Z effect across the avian phylogeny. This thesis urges future studies to account for the effect of recombination before interpreting patterns of selection in sequence evolution.

    List of papers
    1. Recombination Rate Variation Modulates Gene Sequence Evolution Mainly via GC-Biased Gene Conversion, Not Hill-Robertson Interference, in an Avian System
    Open this publication in new window or tab >>Recombination Rate Variation Modulates Gene Sequence Evolution Mainly via GC-Biased Gene Conversion, Not Hill-Robertson Interference, in an Avian System
    2016 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 33, no 1, p. 216-227Article in journal (Refereed) Published
    Abstract [en]

    The ratio of nonsynonymous to synonymous substitution rates (ω) is often used to measure the strength of natural selection. However, ω may be influenced by linkage among different targets of selection, that is, Hill-Robertson interference (HRI), which reduces the efficacy of selection. Recombination modulates the extent of HRI but may also affect ω by means of GC-biased gene conversion (gBGC), a process leading to a preferential fixation of G:C ("strong," S) over A:T ("weak," W) alleles. As HRI and gBGC can have opposing effects on ω, it is essential to understand their relative impact to make proper inferences of ω. We used a model that separately estimated S-to-S, S-to-W, W-to-S, and W-to-W substitution rates in 8,423 avian genes in the Ficedula flycatcher lineage. We found that the W-to-S substitution rate was positively, and the S-to-W rate negatively, correlated with recombination rate, in accordance with gBGC but not predicted by HRI. The W-to-S rate further showed the strongest impact on both dN and dS. However, since the effects were stronger at 4-fold than at 0-fold degenerated sites, likely because the GC content of these sites is farther away from its equilibrium, ω slightly decreases with increasing recombination rate, which could falsely be interpreted as a consequence of HRI. We corroborated this hypothesis analytically and demonstrate that under particular conditions, ω can decrease with increasing recombination rate. Analyses of the site-frequency spectrum showed that W-to-S mutations were skewed toward high, and S-to-W mutations toward low, frequencies, consistent with a prevalent gBGC-driven fixation bias.

    Keywords
    gBGC; Hill-Robertson interference; d(N)/d(S); divergence; diversity; rate of molecular evolution
    National Category
    Evolutionary Biology Biochemistry and Molecular Biology
    Identifiers
    urn:nbn:se:uu:diva-280275 (URN)10.1093/molbev/msv214 (DOI)000369992600017 ()26446902 (PubMedID)
    Funder
    Swedish Research Council, 2010-5650Swedish Research Council, 2013-8271EU, European Research Council, AdG 249976Knut and Alice Wallenberg Foundation
    Available from: 2016-03-09 Created: 2016-03-09 Last updated: 2019-04-09Bibliographically approved
    2. Biased Inference of Selection Due to GC-Biased Gene Conversion and the Rate of Protein Evolution in Flycatchers When Accounting for It
    Open this publication in new window or tab >>Biased Inference of Selection Due to GC-Biased Gene Conversion and the Rate of Protein Evolution in Flycatchers When Accounting for It
    Show others...
    2018 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 10, p. 2475-2486Article in journal (Refereed) Published
    Abstract [en]

    The rate of recombination impacts on rates of protein evolution for at least two reasons: it affects the efficacy of selection due to linkage and influences sequence evolution through the process of GC-biased gene conversion (gBGC). We studied how recombination, via gBGC, affects inferences of selection in gene sequences using comparative genomic and population genomic data from the collared flycatcher (Ficedula albicollis). We separately analyzed different mutation categories ("strong"-to-"weak" "weak-to-strong," and GC-conservative changes) and found that gBGC impacts on the distribution of fitness effects of new mutations, and leads to that the rate of adaptive evolution and the proportion of adaptive mutations among nonsynonymous substitutions are underestimated by 22-33%. It also biases inferences of demographic history based on the site frequency spectrum. In light of this impact, we suggest that inferences of selection (and demography) in lineages with pronounced gBGC should be based on GC-conservative changes only. Doing so, we estimate that 10% of nonsynonymous mutations are effectively neutral and that 27% of nonsynonymous substitutions have been fixed by positive selection in the flycatcher lineage. We also find that gene expression level, sex-bias in expression, and the number of protein-protein interactions, but not Hill-Robertson interference (HRI), are strong determinants of selective constraint and rate of adaptation of collared flycatcher genes. This study therefore illustrates the importance of disentangling the effects of different evolutionary forces and genetic factors in interpretation of sequence data, and from that infer the role of natural selection in DNA sequence evolution.

    Place, publisher, year, edition, pages
    OXFORD UNIV PRESS, 2018
    Keywords
    d(N)/d(S), distribution of fitness effects, GC-biased gene conversion, gene expression, Hill-Robertson interference
    National Category
    Evolutionary Biology Genetics
    Identifiers
    urn:nbn:se:uu:diva-372675 (URN)10.1093/molbev/msy149 (DOI)000452566800011 ()30085180 (PubMedID)
    Available from: 2019-01-09 Created: 2019-01-09 Last updated: 2019-04-09Bibliographically approved
    3. GC-biased gene conversion conceals the prediction of the nearly neutral theory in avian genomes
    Open this publication in new window or tab >>GC-biased gene conversion conceals the prediction of the nearly neutral theory in avian genomes
    Show others...
    2019 (English)In: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 20, article id 5Article in journal (Refereed) Published
    Abstract [en]

    Background: The nearly neutral theory of molecular evolution predicts that the efficacy of natural selection increases with the effective population size. This prediction has been verified by independent observations in diverse taxa, which show that life-history traits are strongly correlated with measures of the efficacy of selection, such as the d(N)/d(S) ratio. Surprisingly, avian taxa are an exception to this theory because correlations between life-history traits and d(N)/d(S) are apparently absent. Here we explore the role of GC-biased gene conversion on estimates of substitution rates as a potential driver of these unexpected observations.

    Results: We analyze the relationship between d(N)/d(S) estimated from alignments of 47 avian genomes and several proxies for effective population size. To distinguish the impact of GC-biased gene conversion from selection, we use an approach that accounts for non-stationary base composition and estimate d(N)/d(S) separately for changes affected or unaffected by GC-biased gene conversion. This analysis shows that the impact of GC-biased gene conversion on substitution rates can explain the lack of correlations between life-history traits and d(N)/d(S). Strong correlations between life-history traits and d(N)/d(S) are recovered after accounting for GC-biased gene conversion. The correlations are robust to variation in base composition and genomic location.

    Conclusions: Our study shows that gene sequence evolution across a wide range of avian lineages meets the prediction of the nearly neutral theory,the efficacy of selection increases with effective population size. Moreover, our study illustrates that accounting for GC-biased gene conversion is important to correctly estimate the strength of selection.

    Place, publisher, year, edition, pages
    BMC, 2019
    Keywords
    Nearly neutral theory, Life-history traits, d(N), d(S), GC-biased gene conversion, Base composition, Avian genomes
    National Category
    Evolutionary Biology
    Identifiers
    urn:nbn:se:uu:diva-375222 (URN)10.1186/s13059-018-1613-z (DOI)000455139400002 ()30616647 (PubMedID)
    Funder
    Swedish Research Council, 2013-8271Knut and Alice Wallenberg Foundation, 2014/0044
    Available from: 2019-01-30 Created: 2019-01-30 Last updated: 2019-04-09Bibliographically approved
    4. Variation in the Z Chromosome to Autosomes Ratio of Genetic Diversity across Birds and its Relationship to the Fast-Z effect
    Open this publication in new window or tab >>Variation in the Z Chromosome to Autosomes Ratio of Genetic Diversity across Birds and its Relationship to the Fast-Z effect
    (English)Manuscript (preprint) (Other academic)
    Keywords
    sex chromosomes, genetic diversity, Fast-Z evolution, genetic drift, selection
    National Category
    Evolutionary Biology
    Research subject
    Biology with specialization in Evolutionary Genetics
    Identifiers
    urn:nbn:se:uu:diva-380263 (URN)
    Available from: 2019-03-25 Created: 2019-03-25 Last updated: 2019-04-09
  • 198.
    Bolívar, Paulina
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Mugal, Carina F
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Nater, Alexander
    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.
    Recombination Rate Variation Modulates Gene Sequence Evolution Mainly via GC-Biased Gene Conversion, Not Hill-Robertson Interference, in an Avian System2016In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 33, no 1, p. 216-227Article in journal (Refereed)
    Abstract [en]

    The ratio of nonsynonymous to synonymous substitution rates (ω) is often used to measure the strength of natural selection. However, ω may be influenced by linkage among different targets of selection, that is, Hill-Robertson interference (HRI), which reduces the efficacy of selection. Recombination modulates the extent of HRI but may also affect ω by means of GC-biased gene conversion (gBGC), a process leading to a preferential fixation of G:C ("strong," S) over A:T ("weak," W) alleles. As HRI and gBGC can have opposing effects on ω, it is essential to understand their relative impact to make proper inferences of ω. We used a model that separately estimated S-to-S, S-to-W, W-to-S, and W-to-W substitution rates in 8,423 avian genes in the Ficedula flycatcher lineage. We found that the W-to-S substitution rate was positively, and the S-to-W rate negatively, correlated with recombination rate, in accordance with gBGC but not predicted by HRI. The W-to-S rate further showed the strongest impact on both dN and dS. However, since the effects were stronger at 4-fold than at 0-fold degenerated sites, likely because the GC content of these sites is farther away from its equilibrium, ω slightly decreases with increasing recombination rate, which could falsely be interpreted as a consequence of HRI. We corroborated this hypothesis analytically and demonstrate that under particular conditions, ω can decrease with increasing recombination rate. Analyses of the site-frequency spectrum showed that W-to-S mutations were skewed toward high, and S-to-W mutations toward low, frequencies, consistent with a prevalent gBGC-driven fixation bias.

  • 199.
    Borinder, Niclas H.
    et al.
    Uppsala University, Music and Museums, Museum of Evolution.
    Poropat, Stephen F.
    Australian Age Dinosaurs Nat Hist Museum, Winton, Qld 4735, Australia.;Monash Univ, Wellington Rd, Clayton, Vic 3800, Australia..
    Kear, Benjamin P.
    Uppsala University, Music and Museums, Museum of Evolution.
    Reassessment of the earliest documented stegosaurian fossils from Asia2016In: Cretaceous research (Print), ISSN 0195-6671, E-ISSN 1095-998X, Vol. 68, p. 61-69Article in journal (Refereed)
    Abstract [en]

    In 1929, the famous Swedish palaeontologist Carl Wiman documented the first unequivocal stegosaurian dinosaur fossils from Asia. His material comprised an isolated dermal spine, together with a dorsal vertebra that was briefly described but never figured. Since then these remains have languished in obscurity, being noted in some stegosaur review articles but often ignored altogether. However, recent auditing of the Museum of Evolution palaeontological collection at Uppsala University in Sweden has led to the rediscovery of Wiman's original specimens, as well as two additional previously unrecognised stegosaurian dorsal vertebrae. All of these bones derive from the Lower Cretaceous (Berriasian-Valanginian) Mengyin Formation of Shandong Province in eastern China, and are morphologically compatible with the stratigraphically proximal stegosaurian taxon Wuerhosaurus from the Valanginian-Albian Tugulu Group in the Xinjiang Uyghur Autonomous Region of Western China. Wirnan's seminal stegosaurian fossils thus expand current palaeobiogeographical distributions, and contribute to the otherwise enigmatic record of Early Cretaceous stegosaurian occurrences.

  • 200.
    Boughman, Janette W.
    et al.
    Michigan State Univ, Dept Integrat Biol, E Lansing, MI 48824 USA..
    Svanbäck, Richard
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Synergistic selection between ecological niche and mate preference primes diversification2017In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 1, p. 6-22Article in journal (Refereed)
    Abstract [en]

    The ecological niche and mate preferences have independently been shown to be important for the process of speciation. Here, we articulate a novel mechanism by which ecological niche use and mate preference can be linked to promote speciation. The degree to which individual niches are narrow and clustered affects the strength of divergent natural selection and population splitting. Similarly, the degree to which individual mate preferences are narrow and clustered affects the strength of divergent sexual selection and assortative mating between diverging forms. This novel perspective is inspired by the literature on ecological niches; it also explores mate preferences and how they may contribute to speciation. Unlike much comparative work, we do not search for evolutionary patterns using proxies for adaptation and sexual selection, but rather we elucidate how ideas from niche theory relate to mate preference, and how this relationship can foster speciation. Recognizing that individual and population niches are conceptually and ecologically linked to individual and population mate preference functions will significantly increase our understanding of rapid evolutionary diversification in nature. It has potential to help solve the difficult challenge of testing the role of sexual selection in the speciation process. We also identify ecological factors that are likely to affect individual niche and individual mate preference in synergistic ways and as a consequence to promote speciation. The ecological niche an individual occupies can directly affect its mate preference. Clusters of individuals with narrow, differentiated niches are likely to have narrow, differentiated mate preference functions. Our approach integrates ecological and sexual selection research to further our understanding of diversification processes. Such integration may be necessary for progress because these processes seem inextricably linked in the natural world.

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