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  • 1.
    Backström, Niclas
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Brandström, Mikael
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Cheng, Hans
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): Conserved synteny but gene order rearrangements on the avian Z chromosome2006In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 174, no 1, 377-386 p.Article in journal (Refereed)
    Abstract [en]

    Data from completely sequenced genomes are likely to open the way for novel studies of the genetics of nonmodel organisms, in particular when it comes to the identification and analysis of genes responsible for traits that are under selection in natural populations. Here we use the draft sequence of the chicken genome as a starting point for linkage mapping in a wild bird species, the collared flycatcher-one of the most well-studied avian species in ecological and evolutionary research. A pedigree of 365 flycatchers was established and genotyped for single nucleotide polymorphisms in 23 genes selected from (and spread over most of) the chicken Z chromosome. All genes were also found to be located on the Z chromosome in the collared flycatcher, confirming conserved synteny at the level of gene content across distantly related avian lineages. This high degree of conservation mimics the situation seen for the mammalian X chromosome and may thus be a general feature in sex chromosome evolution, irrespective of whether there is male or female heterogamety. Alternatively, such unprecedented chromosomal conservation may be characteristic of most chromosomes in avian genome evolution. However, several internal rearrangements were observed, meaning that the transfer of map information from chicken to nonmodel bird species cannot always assume conserved gene orders. Interestingly, the rate of recombination on the Z chromosome of collared flycatchers was only similar to 50% that of chicken, challenging the widely held view that birds generally have high recombination rates.

  • 2.
    Backström, Niclas
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Karaiskou, Nikoletta
    Leder, Erica H.
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Primmer, Craig R.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    A Gene-Based Genetic Linkage Map of the Collared Flycatcher (Ficedula albicollis) Reveals Extensive Synteny and Gene-Order Conservation During 100 Million Years of Avian Evolution2008In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 179, 1479-1495 p.Article in journal (Refereed)
    Abstract [en]

    By taking advantage of a recently developed reference markerset for avian genome analysis we have constructed a gene-basedgenetic map of the collared flycatcher, an important "ecologicalmodel" for studies of life-history evolution, sexual selection,speciation, and quantitative genetics. A pedigree of 322 birdsfrom a natural population was genotyped for 384 single nucleotidepolymorphisms (SNPs) from 170 protein-coding genes and 71 microsatellites.Altogether, 147 gene markers and 64 microsatellites form 33linkage groups with a total genetic distance of 1787 cM. Malerecombination rates are, on average, 22% higher than femalerates (total distance 1982 vs. 1627 cM). The ability to anchorthe collared flycatcher map with the chicken genome via thegene-based SNPs revealed an extraordinary degree of both syntenyand gene-order conservation during avian evolution. The greatmajority of chicken chromosomes correspond to a single linkagegroup in collared flycatchers, with only a few cases of inter-and intrachromosomal rearrangements. The rate of chromosomaldiversification, fissions/fusions, and inversions combined isthus considerably lower in birds (0.05/MY) than in mammals (0.6–2.0/MY).A dearth of repeat elements, known to promote chromosomal breakage,in avian genomes may contribute to their stability. The degreeof genome stability is likely to have important consequencesfor general evolutionary patterns and may explain, for example,the comparatively slow rate by which genetic incompatibilityamong lineages of birds evolves.

  • 3.
    Backström, Niclas
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Lindell, Johan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Zhang, Yu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Palkopoulou, Eleftheria
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Sætre, Glenn-Peter
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    A high-density scan of the Z chromosome in ficedula flycatchers reveals candidate loci for diversifying selection2010In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 64, no 12, 3461-3475 p.Article in journal (Refereed)
    Abstract [en]

    Theoretical and empirical data suggest that genes located on sex chromosomes may play an important role both for sexually selected traits and for traits involved in the build-up of hybrid incompatibilities. We investigated patterns of genetic variation in 73 genes located on the Z chromosomes of two species of the flycatcher genus Ficedula, the pied flycatcher and the collared flycatcher. Sequence data were evaluated for signs of selection potentially related to genomic differentiation in these young sister species, which hybridize despite reduced fitness of hybrids. Seven loci were significantly more divergent between the two species than expected under neutrality and they also displayed reduced nucleotide diversity, consistent with having been influenced by directional selection. Two of the detected candidate regions contain genes that are associated with plumage coloration in birds. Plumage characteristics play an important role in species recognition in these flycatchers suggesting that the detected genes may have been involved in the evolution of sexual isolation between the species.

  • 4.
    Backström, Niclas
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Palkopoulou, Eleftheria
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    No evidence for Z-chromosome rearrangements between the pied flycatcher and the collared flycatcher as judged by gene-based comparative genetic maps2010In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 19, no 16, 3394-3405 p.Article in journal (Refereed)
    Abstract [en]

    Revealing the genetic basis of reproductive isolation is fundamental for understanding the speciation process. Chromosome speciation models propose a role for chromosomal rearrangements in promoting the build up of reproductive isolation between diverging populations and empirical data from several animal and plant taxa support these models. The pied flycatcher and the collared flycatcher are two closely related species that probably evolved reproductive isolation during geographical separation in Pleistocene glaciation refugia. Despite the short divergence time and current hybridization, these two species demonstrate a high degree of intrinsic post-zygotic isolation and previous studies have shown that traits involved in mate choice and hybrid viability map to the Z-chromosome. Could rearrangements of the Z-chromosome between the species explain their reproductive isolation? We developed high coverage Z-chromosome linkage maps for both species, using gene-based markers and large-scale SNP genotyping. Best order maps contained 57-62 gene markers with an estimated average density of one every 1-1.5 Mb. We estimated the recombination rates in flycatcher Z-chromosomes to 1.1-1.3 cM/Mb. A comparison of the maps of the two species revealed extensive co-linearity with no strong evidence for chromosomal rearrangements. This study does therefore not provide support the idea that sex chromosome rearrangements have caused the relatively strong post-zygotic reproductive isolation between these two Ficedula species.

  • 5.
    Backström, Niclas
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Levels of linkage disequilibrium in a wild bird population2006In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 2, no 3, 435-438 p.Article in journal (Refereed)
    Abstract [en]

    Population-based mapping approaches are attractive for tracing the genetic background to phenotypic traits in wild species, given that it is often difficult to gather extensive and well-defined pedigrees needed for quantitative trait locus analysis. However, the feasibility of association or hitch-hiking mapping is dependent on the degree of linkage disequilibrium. (LD) in the population, on which there is yet limited information for wild species. Here we use single nucleotide polymorphism (SNP) markers from 23 genes in a recently established linkage map of the Z chromosome of the collared flycatcher, to study the extent of LD in a natural bird population. In most but not all cases we find SNPs within the same intron (less than 500 bp) to be in perfect LD. However, LD then decays to background level at a distance 1 cM or 400-500 kb. Although LD seems more extensive than in other species, if the observed pattern is representative for other regions of the genome and turns out to be a general feature of natural bird populations, dense marker maps might be needed for genome scans aimed at identifying association between marker and trait loci.

  • 6.
    Bailey, Richard I.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Innocenti, Paolo
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Morrow, Edward H.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Female Drosophila melanogaster Gene Expression and Mate Choice: The X Chromosome Harbours Candidate Genes Underlying Sexual Isolation2011In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 6, no 2, e17358- p.Article in journal (Refereed)
    Abstract [en]

    Background: The evolution of female choice mechanisms favouring males of their own kind is considered a crucial step during the early stages of speciation. However, although the genomics of mate choice may influence both the likelihood and speed of speciation, the identity and location of genes underlying assortative mating remain largely unknown. Methods and Findings: We used mate choice experiments and gene expression analysis of female Drosophila melanogaster to examine three key components influencing speciation. We show that the 1,498 genes in Zimbabwean female D. melanogaster whose expression levels differ when mating with more (Zimbabwean) versus less (Cosmopolitan strain) preferred males include many with high expression in the central nervous system and ovaries, are disproportionately X-linked and form a number of clusters with low recombination distance. Significant involvement of the brain and ovaries is consistent with the action of a combination of pre- and postcopulatory female choice mechanisms, while sex linkage and clustering of genes lead to high potential evolutionary rate and sheltering against the homogenizing effects of gene exchange between populations. Conclusion: Taken together our results imply favourable genomic conditions for the evolution of reproductive isolation through mate choice in Zimbabwean D. melanogaster and suggest that mate choice may, in general, act as an even more important engine of speciation than previously realized.

  • 7.
    Boström, Jannika E.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Dimitrova, Marina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Stockholm Univ, Dept Zool, S-10691 Stockholm, Sweden..
    Canton, Cindy
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Hastad, Olle
    Swedish Univ Agr Sci, Dept Anat Physiol & Biochem, Box 7011, S-75007 Uppsala, Sweden..
    Qvarnstrom, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ödeen, Anders
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Swedish Univ Agr Sci, Dept Anat Physiol & Biochem, Box 7011, S-75007 Uppsala, Sweden..
    Ultra-Rapid Vision in Birds2016In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, no 3, e0151099Article in journal (Refereed)
    Abstract [en]

    Flying animals need to accurately detect, identify and track fast-moving objects and these behavioral requirements are likely to strongly select for abilities to resolve visual detail in time. However, evidence of highly elevated temporal acuity relative to non-flying animals has so far been confined to insects while it has been missing in birds. With behavioral experiments on three wild passerine species, blue tits, collared and pied flycatchers, we demonstrate temporal acuities of vision far exceeding predictions based on the sizes and metabolic rates of these birds. This implies a history of strong natural selection on temporal resolution. These birds can resolve alternating light-dark cycles at up to 145 Hz (average: 129, 127 and 137, respectively), which is ca. 50 Hz over the highest frequency shown in any other vertebrate. We argue that rapid vision should confer a selective advantage in many bird species that are ecologically similar to the three species examined in our study. Thus, rapid vision may be a more typical avian trait than the famously sharp vision found in birds of prey.

  • 8. Brommer, Jon E.
    et al.
    Kirkpatrick, M.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    The intersexual genetic correlation for lifetime fitness in the wild and its implications for sexual selection2007In: PLoS ONE, ISSN 1932-6203, Vol. 2, no 8, e744- p.Article in journal (Refereed)
    Abstract [en]

    Background

    The genetic benefits of mate choice are limited by the degree to which male and female fitness are genetically correlated. If the intersexual correlation for fitness is small or negative, choosing a highly fit mate does not necessarily result in high fitness offspring.

    Methodology/Principal Finding

    Using an animal-model approach on data from a pedigreed population of over 7,000 collared flycatchers (Ficedula albicollis), we estimate the intersexual genetic correlation in Lifetime Reproductive Success (LRS) in a natural population to be negative in sign (−0.85±0.6). Simulations show this estimate to be robust in sign to the effects of extra-pair parentage. The genetic benefits in this population are further limited by a low level of genetic variation for fitness in males.

    Conclusions/Significance

    The potential for indirect sexual selection is nullified by sexual antagonistic fitness effects in this natural population. Our findings and the scarce evidence from other studies suggest that the intersexual genetic correlation for lifetime fitness may be very low in nature. We argue that this form of conflict can, in general, both constrain and maintain sexual selection, depending on the sex-specific additive genetic variances in lifetime fitness.

  • 9. Burger, Claudia
    et al.
    Belskii, Eugen
    Eeva, Tapio
    Laaksonen, Toni
    Maegi, Marko
    Maend, Raivo
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Slagsvold, Tore
    Veen, Thor
    Visser, Marcel E.
    Wiebe, Karen L.
    Wiley, Chris
    Wright, Jonathan
    Both, Christiaan
    Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation2012In: Journal of Animal Ecology, ISSN 0021-8790, E-ISSN 1365-2656, Vol. 81, no 4, 926-936 p.Article in journal (Refereed)
    Abstract [en]

    1. Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2. We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3. Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4. We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.

  • 10.
    Burri, Reto
    et al.
    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.
    Kawakami, Takeshi
    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.
    Ólason, Páll I.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
    Smeds, Linnea
    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.
    Dutoit, Ludovic
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Bures, Stanislav
    Palacky Univ, Dept Zool, Lab Ornithol, Olomouc 77146, Czech Republic..
    Garamszegi, Laszlo Z.
    CSIC, Dept Evolutionary Ecol, Estn Biol Donana, Seville 41092, Spain..
    Hogner, Silje
    Univ Oslo, Ctr Ecol & Evolutionary Synth, Dept Biosci, N-0316 Oslo, Norway.;Univ Oslo, Nat Hist Museum, N-0318 Oslo, Norway..
    Moreno, Juan
    CSIC, Museo Nacl Ciencias Nat, E-28006 Madrid, Spain..
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ruzic, Milan
    Bird Protect & Study Soc Serbia, Novi Sad 21000, Serbia..
    Saether, Stein-Are
    Univ Oslo, Ctr Ecol & Evolutionary Synth, Dept Biosci, N-0316 Oslo, Norway.;Norwegian Inst Nat Res NINA, N-7034 Trondheim, Norway..
    Saetre, Glenn-Peter
    Univ Oslo, Ctr Ecol & Evolutionary Synth, Dept Biosci, N-0316 Oslo, Norway..
    Toeroek, Janos
    Eotvos Lorand Univ, Dept Systemat Zool & Ecol, Behav Ecol Grp, H-1117 Budapest, Hungary..
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers2015In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 25, no 11, 1656-1665 p.Article in journal (Refereed)
    Abstract [en]

    Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d(XY) relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.

  • 11. Eeva, Tapio
    et al.
    Ruuskanen, Suvi
    Salminen, Juha-Pekka
    Belskii, Eugen
    Järvinen, Antero
    Kerimov, Anvar
    Korpimäki, Erkki
    Krams, Indrikis
    Moreno, Juan
    Morosinotto, Chiara
    Maend, Raivo
    Orell, Markku
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Siitari, Heli
    Slater, Fred M.
    Tilgar, Vallo
    Visser, Marcel E.
    Winkel, Wolfgang
    Zang, Herwig
    Laaksonen, Toni
    Geographical trends in the yolk carotenoid composition of the pied flycatcher (Ficedula hypoleuca)2011In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 165, no 2, 277-287 p.Article in journal (Refereed)
    Abstract [en]

    Carotenoids in the egg yolks of birds are considered to be important antioxidants and immune stimulants during the rapid growth of embryos. Yolk carotenoid composition is strongly affected by the carotenoid composition of the female's diet at the time of egg formation. Spatial and temporal differences in carotenoid availability may thus be reflected in yolk concentrations. To assess whether yolk carotenoid concentrations or carotenoid profiles show any large-scale geographical trends or differences among habitats, we collected yolk samples from 16 European populations of the pied flycatcher, Ficedula hypoleuca. We found that the concentrations and proportions of lutein and some other xanthophylls in the egg yolks decreased from Central Europe northwards. The most southern population (which is also the one found at the highest altitude) also showed relatively low carotenoid levels. Concentrations of beta-carotene and zeaxanthin did not show any obvious geographical gradients. Egg yolks also contained proportionally more lutein and other xanthophylls in deciduous than in mixed or coniferous habitats. We suggest that latitudinal gradients in lutein and xanthophylls reflect the lower availability of lutein-rich food items in the northern F. hypoleuca populations and in montane southern populations, which start egg-laying earlier relative to tree phenology than the Central European populations. Similarly, among-habitat variation is likely to reflect the better availability of lutein-rich food in deciduous forests. Our study is the first to indicate that the concentration and profile of yolk carotenoids may show large-scale spatial variation among populations in different parts of the species' geographical range. Further studies are needed to test the fitness effects of this geographical variation.

  • 12.
    Ellegren, Hans
    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.
    Burri, Reto
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ólason, Páll I.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Backström, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Kawakami, Takeshi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Künstner, Axel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Mäkinen, Hannu
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Nadachowska-Brzyska, Krystyna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Uebbing, Severin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Wolf, Jochen B. W.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    The genomic landscape of species divergence in Ficedula flycatchers2012In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 491, no 7426, 756-760 p.Article in journal (Refereed)
    Abstract [en]

    Unravelling the genomic landscape of divergence between lineages is key to understanding speciation. The naturally hybridizing collared flycatcher and pied flycatcher are important avian speciation models that show pre-as well as postzygotic isolation. We sequenced and assembled the 1.1-Gb flycatcher genome, physically mapped the assembly to chromosomes using a low-density linkage map and re-sequenced population samples of each species. Here we show that the genomic landscape of species differentiation is highly heterogeneous with approximately 50 'divergence islands' showing up to 50-fold higher sequence divergence than the genomic background. These non-randomly distributed islands, with between one and three regions of elevated divergence per chromosome irrespective of chromosome size, are characterized by reduced levels of nucleotide diversity, skewed allele-frequency spectra, elevated levels of linkage disequilibrium and reduced proportions of shared polymorphisms in both species, indicative of parallel episodes of selection. Proximity of divergence peaks to genomic regions resistant to sequence assembly, potentially including centromeres and telomeres, indicate that complex repeat structures may drive species divergence. A much higher background level of species divergence of the Z chromosome, and a lower proportion of shared polymorphisms, indicate that sex chromosomes and autosomes are at different stages of speciation. This study provides a roadmap to the emerging field of speciation genomics.

  • 13.
    Gustafsson, L
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Qvarnström, A
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    A test of the "sexy son" hypothesis: sons of polygynous collared flycatchers do not inherit their fathers' mating status2006In: American Naturalist, Vol. 167, 297-302 p.Article in journal (Refereed)
  • 14.
    Haavie, J
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology.
    Borge, T
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Evolutionary Biology.
    Bures, S
    Garamszegi, L
    Lampe, HM
    Moreno, J
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Animal Ecology.
    Török, J
    Saetre, GP
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolutionary Biology, Evolutionary Biology.
    Flycatcher song in allopatry and sympatry: convergence, divergence and reinforcement2004In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 17, no 2, 227-237 p.Article in journal (Refereed)
    Abstract [en]

    The theory of reinforcement predicts that natural selection against the production of unfit hybrids favours traits that increase assortative mating. Whether culturally inherited traits, such as bird song, can increase assortative mating by reinforcement is largely unknown. We compared songs of pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) from two hybrid zones of different ages with songs from allopatric populations. Previously, a character divergence in male plumage traits has been shown to reinforce premating isolation in sympatric flycatchers. In contrast, we find that the song of the pied flycatcher has converged towards that of the collared flycatcher (mixed singing). However, a corresponding divergence in the collared flycatcher shows that the species differences in song characters are maintained in sympatry. Genetic analyses suggest that mixed song is not caused by introgression from the collared flycatcher, but rather due to heterospecific copying. Circumstantial evidence suggests that mixed song may increase the rate of maladaptive hybridization. In the oldest hybrid zone where reinforcement on plumage traits is most pronounced, the frequency of mixed singing and hybridization is also lowest. Thus, we suggest that reinforcement has reduced the frequency of mixed singing in the pied flycatcher and caused a divergence in the song of the collared flycatcher. Whether a culturally inherited trait promotes or opposes speciation in sympatry may depend on its plasticity. The degree of plasticity may be genetically determined and accordingly under selection by reinforcement.

  • 15. Haavie, J
    et al.
    Borge, T
    Bures, S
    Garamszegi, LZ
    Lampe, HM
    Moreno, J
    Qvarnström, Anna
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Torok, J
    Saetre, GP
    Flyctacher song in allopatry and sympatry - convergence, divergence and reinforcement2004In: Journal of Evolutionary Biology, Vol. 17, 227-237 p.Article in journal (Refereed)
  • 16.
    Husby, Arild
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ekblom, Robert
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Let's talk turkey: immune competence in domestic and wild fowl2011In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 107, no 2, 103-104 p.Article in journal (Other academic)
  • 17.
    Husby, Arild
    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.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Low Genetic Variance in the Duration of the Incubation Period in a Collared Flycatcher (Ficedula albicollis) Population2012In: American Naturalist, ISSN 0003-0147, E-ISSN 1537-5323, Vol. 179, no 1, 132-136 p.Article in journal (Refereed)
    Abstract [en]

    The avian incubation period is associated with high energetic costs and mortality risks suggesting that there should be strong selection to reduce the duration to the minimum required for normal offspring development. Although there is much variation in the duration of the incubation period across species, there is also variation within species. It is necessary to estimate to what extent this variation is genetically determined if we want to predict the evolutionary potential of this trait. Here we use a long-term study of collared flycatchers to examine the genetic basis of variation in incubation duration. We demonstrate limited genetic variance as reflected in the low and nonsignificant additive genetic variance, with a corresponding heritability of 0.04 and coefficient of additive genetic variance of 2.16. Any selection acting on incubation duration will therefore be inefficient. To our knowledge, this is the first time heritability of incubation duration has been estimated in a natural bird population.

  • 18.
    Husby, Arild
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kawakami, Takeshi
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ronnegard, Lars
    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.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Genome-wide association mapping in a wild avian population identifies a link between genetic and phenotypic variation in a life-history trait2015In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, no 1806Article in journal (Refereed)
    Abstract [en]

    Understanding the genetic basis of traits involved in adaptation is a major challenge in evolutionary biology but remains poorly understood. Here, we use genome-wide association mapping using a custom 50 k single nucleotide polymorphism (SNP) array in a natural population of collared flycatchers to examine the genetic basis of clutch size, an important life-history trait in many animal species. We found evidence for an association on chromosome 18 where one SNP significant at the genome-wide level explained 3.9% of the phenotypic variance. We also detected two suggestive quantitative trait loci (QTLs) on chromosomes 9 and 26. Fitness differences among genotypes were generally weak and not significant, although there was some indication of a sex-by-genotype interaction for lifetime reproductive success at the suggestive QTL on chromosome 26. This implies that sexual antagonism may play a role in maintaining genetic variation at this QTL. Our findings provide candidate regions for a classic avian life-history trait that will be useful for future studies examining the molecular and cellular function of, as well as evolutionary mechanisms operating at, these loci.

  • 19.
    Husby, Arild
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Schielzeth, Holger
    Forstmeier, Wolfgang
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sex chromosome linked genetic variance and the evolution of sexual dimorphism of quantitative traits2013In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 67, no 3, 609-619 p.Article in journal (Refereed)
    Abstract [en]

    Theory predicts that sex chromsome linkage should reduce intersexual genetic correlations thereby allowing the evolution of sexual dimorphism. Empirical evidence for sex linkage has come largely from crosses and few studies have examined how sexual dimorphism and sex linkage are related within outbred populations. Here, we use data on an array of different traits measured on over 10,000 individuals from two pedigreed populations of birds (collared flycatcher and zebra finch) to estimate the amount of sex-linked genetic variance (h2z). Of 17 traits examined, eight showed a nonzero h2Z estimate but only four were significantly different from zero (wing patch size and tarsus length in collared flycatchers, wing length and beak color in zebra finches). We further tested how sexual dimorphism and the mode of selection operating on the trait relate to the proportion of sex-linked genetic variance. Sexually selected traits did not show higher h2Z than morphological traits and there was only a weak positive relationship between h2Z and sexual dimorphism. However, given the relative scarcity of empirical studies, it is premature to make conclusions about the role of sex chromosome linkage in the evolution of sexual dimorphism.

  • 20.
    Kardos, Marty
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Husby, Arild
    Univ Helsinki, Dept Biosci, POB 65, FIN-00014 Helsinki, Finland.;Norwegian Univ Sci & Technol, Ctr Biodivers Dynam, Dept Biol, N-7491 Trondheim, Norway..
    McFarlane, S. Eryn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ellegren, Hans
    Whole-genome resequencing of extreme phenotypes in collared flycatchers highlights the difficulty of detecting quantitative trait loci in natural populations2016In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 16, no 3, 727-741 p.Article in journal (Refereed)
    Abstract [en]

    Dissecting the genetic basis of phenotypic variation in natural populations is a long-standing goal in evolutionary biology. One open question is whether quantitative traits are determined only by large numbers of genes with small effects, or whether variation also exists in large-effect loci. We conducted genomewide association analyses of forehead patch size (a sexually selected trait) on 81 whole-genome-resequenced male collared flycatchers with extreme phenotypes, and on 415 males sampled independent of patch size and genotyped with a 50K SNP chip. No SNPs were genomewide statistically significantly associated with patch size. Simulation-based power analyses suggest that the power to detect large-effect loci responsible for 10% of phenotypic variance was <0.5 in the genome resequencing analysis, and <0.1 in the SNP chip analysis. Reducing the recombination by two-thirds relative to collared flycatchers modestly increased power. Tripling sample size increased power to >0.8 for resequencing of extreme phenotypes (N=243), but power remained <0.2 for the 50K SNP chip analysis (N=1245). At least 1 million SNPs were necessary to achieve power >0.8 when analysing 415 randomly sampled phenotypes. However, power of the 50K SNP chip to detect large-effect loci was nearly 0.8 in simulations with a small effective population size of 1500. These results suggest that reliably detecting large-effect trait loci in large natural populations will often require thousands of individuals and near complete sampling of the genome. Encouragingly, far fewer individuals and loci will often be sufficient to reliably detect large-effect loci in small populations with widespread strong linkage disequilibrium.

  • 21.
    Kardos, Marty
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ Montana, Div Biol Sci, Flathead Lake Biol Stn, Polson, MT 59860 USA..
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Inferring Individual Inbreeding and Demographic History from Segments of Identity by Descent in Ficedula Flycatcher Genome Sequences2017In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 205, no 3, 1319-1334 p.Article in journal (Refereed)
    Abstract [en]

    Individual inbreeding and historical demography can be estimated by analyzing runs of homozygosity (ROH), which are indicative of chromosomal segments of identity by descent (IBD). Such analyses have so far been rare in natural populations due to limited genomic resources. We analyzed ROH in whole genome sequences from 287 Ficedula flycatchers representing four species, with the objectives of evaluating the causes of genome-wide variation in the abundance of ROH and inferring historical demography. ROH were clearly more abundant in genomic regions with low recombination rate. However, this pattern was substantially weaker when ROH were mapped using genetic rather than physical single nucleotide polymorphism (SNP) coordinates in the genome. Empirical results and simulations suggest that high ROH abundance in regions of low recombination was partly caused by increased power to detect the very long IBD segments typical of regions with a low recombination rate. Simulations also showed that hard selective sweeps (but not soft sweeps or background selection) likely contributed to variation in the abundance of ROH across the genome. Comparisons of the abundance of ROH among several study populations indicated that the Spanish pied flycatcher population had the smallest historical effective population size (Ne) for this species, and that a putatively recently founded island (Baltic) population had the smallest historical Ne among the collared flycatchers. Analysis of pairwise IBD in Baltic collared flycatchers indicated that this population was founded,60 generations ago. This study provides a rare genomic glimpse into demographic history and the mechanisms underlying the genome-wide distribution of ROH.

  • 22.
    Kawakami, Takeshi
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Backström, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Burri, Reto
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Husby, Arild
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ólason, Páll
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Rice, Amber M.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array2014In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 14, no 6, 1248-1260 p.Article in journal (Refereed)
    Abstract [en]

    With the access to draft genome sequence assemblies and whole-genome resequencing data from population samples, molecular ecology studies will be able to take truly genome-wide approaches. This now applies to an avian model system in ecological and evolutionary research: Old World flycatchers of the genus Ficedula, for which we recently obtained a 1.1Gb collared flycatcher genome assembly and identified 13 million single-nucleotide polymorphism (SNP)s in population resequencing of this species and its sister species, pied flycatcher. Here, we developed a custom 50K Illumina iSelect flycatcher SNP array with markers covering 30 autosomes and the Z chromosome. Using a number of selection criteria for inclusion in the array, both genotyping success rate and polymorphism information content (mean marker heterozygosity=0.41) were high. We used the array to assess linkage disequilibrium (LD) and hybridization in flycatchers. Linkage disequilibrium declined quickly to the background level at an average distance of 17kb, but the extent of LD varied markedly within the genome and was more than 10-fold higher in genomic islands' of differentiation than in the rest of the genome. Genetic ancestry analysis identified 33 F-1 hybrids but no later-generation hybrids from sympatric populations of collared flycatchers and pied flycatchers, contradicting earlier reports of backcrosses identified from much fewer number of markers. With an estimated divergence time as recently as <1Ma, this suggests strong selection against F-1 hybrids and unusually rapid evolution of reproductive incompatibility in an avian system.

  • 23.
    Kawakami, Takeshi
    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.
    Backstrom, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Husby, Arild
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Mugal, Carina F.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Ólason, Páll
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution2014In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 23, no 16, 4035-4058 p.Article, review/survey (Refereed)
    Abstract [en]

    Detailed linkage and recombination rate maps are necessary to use the full potential of genome sequencing and population genomic analyses. We used a custom collared flycatcher 50K SNP array to develop a high-density linkage map with 37262 markers assigned to 34 linkage groups in 33 autosomes and the Z chromosome. The best-order map contained 4215 markers, with a total distance of 3132cM and a mean genetic distance between markers of 0.12cM. Facilitated by the array being designed to include markers from most scaffolds, we obtained a second-generation assembly of the flycatcher genome that approaches full chromosome sequences (N50 super-scaffold size 20.2Mb and with 1.042Gb (of 1.116Gb) anchored to and mostly ordered and oriented along chromosomes). We found that flycatcher and zebra finch chromosomes are entirely syntenic but that inversions at mean rates of 1.5-2.0 event (6.6-7.5Mb) per My have changed the organization within chromosomes, rates high enough for inversions to potentially have been involved with many speciation events during avian evolution. The mean recombination rate was 3.1cM/Mb and correlated closely with chromosome size, from 2cM/Mb for chromosomes >100Mb to >10cM/Mb for chromosomes <10Mb. This size dependence seemed entirely due to an obligate recombination event per chromosome; if 50cM was subtracted from the genetic lengths of chromosomes, the rate per physical unit DNA was constant across chromosomes. Flycatcher recombination rate showed similar variation along chromosomes as chicken but lacked the large interior recombination deserts characteristic of zebra finch chromosomes.

  • 24.
    Kulma, Katarzyna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Butterfield, Eileen
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Strand, Tanja
    Swedish Institute for Communicable Disease Control, Stockholm, Sweden.
    Lundkvist, Åke
    Swedish Institute for Communicable Disease Control, Stockholm, Sweden.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Immunoglobulin level and infection intensity influence how malaria-infected collared flycatchers respond to brood size manipulationArticle in journal (Refereed)
    Abstract [en]

    1.The existence of a trade-off between investment in reproduction and immune function is well-established in many species. However, variation in the underlying physiological allocation strategies, which is what selection operates on, remains largely unexplored.

    2.We investigated how haemosporidian infection influenced stress hormone level and ability to increase parental effort in female collared flycatchers (Ficedula albicollis). We especially focused on how estimates of investment in humoral immune response and level of parasitemia influenced subsequent parental investment (i.e. offspring provisioning and offspring mass).

    3.To achieve these goals, we combined a brood size manipulation experiment with nested- and quantitative PCR methods to establish infection status and intensity. In addition, we quantified immunoglobulin Y (IgY) and stress protein levels.

    4. Malaria-infected females reared enlarged broods with lower mass but there was large variation in their response to the experiment. Only infected females with low IgY levels decreased their relative provisioning rate and there was a positive relationship between the intensity of infection and total brood mass.

    5. Our study implies that malaria-infected flycatchers experience a trade-off between keeping their infection at bay (i.e. low level of parasitemia) and responding to increased offspring demands (i.e. high offspring mass in enlarged broods). However, relatively immunocompetent individuals (i.e. individuals with high IgY levels) did not compromise their parental care suggesting that the main cost of raising the immune response does not lay in antibody production.

  • 25.
    Kulma, Katarzyna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Low, Matthew
    Swedish University of Agricultural Sciences, Uppsala, Sweden.
    Bensch, Staffan
    Lund University, Lund, Sweden.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone2013In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 22, no 17, 4591-4601 p.Article in journal (Refereed)
    Abstract [en]

    Parasites may influence the outcome of interspecific competition between closely-related host species through lower parasite virulence in the host with which they share the longer evolutionary history. We tested this idea by comparing the prevalence of avian malaria (Haemosporidia) lineages and their association with survival in pied and collared flycatchers (Ficedula hypoleuca & F. albicollis) breeding in a recent contact zone on the Swedish island of Öland. A nested PCR protocol amplifying haemosporidian fragments of mtDNA was used to screen the presence of malaria lineages in 1048 blood samples collected during 6 years. Competitively inferior pied flycatchers had a higher prevalence of blood parasites, including the lineages that were shared between the two flycatcher species. Multistate mark-recapture models revealed a lower survival of infected versus uninfected female pied flycatchers, while no such effects were detected in male pied flycatchers or in collared flycatchers of either sex. Our results show that a comparatively new host, the collared flycatcher, appears to be less susceptible to a local northern European malarial lineage where the collared flycatchers have recently expanded their distribution. Pied flycatchers experience strong reproductive interference from collared flycatchers, and the additional impact of species-specific blood parasite effects adds to this competitive exclusion. These results support the idea that parasites can strongly influence the outcome of interspecific competition between closely-related host species, but that the invading species need not necessarily be more susceptible to local parasites.

  • 26.
    Kulma, Katarzyna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Low, Matthew
    Swedish University of Agricultural Sciences, Uppsala, Sweden.
    Bensch, Staffan
    Lund University, Lund, Sweden.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Malaria-infected female collared flycatchers (Ficedula albicollis) do not pay the cost of late breeding2014In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 1, e85822- p.Article in journal (Refereed)
    Abstract [en]

    Life-history theory predicts that the trade-off between parasite defense and other costly traits such as reproduction may be most evident when resources are scarce. The strength of selection that parasites inflict on their host may therefore vary across environmental conditions. Collared flycatchers (Ficedula albicollis) breeding on the Swedish island Oland experience a seasonal decline in their preferred food resource, which opens the possibility to test the strength of life-history trade-offs across environmental conditions. We used nested-PCR and quantitative-PCR protocols to investigate the association of Haemosporidia infection with reproductive performance of collared flycatcher females in relation to a seasonal change in the external environment. We show that despite no difference in mean onset of breeding, infected females produced relatively more of their fledglings late in the season. This pattern was also upheld when considering only the most common malaria lineage (hPHSIB1), however there was no apparent link between the reproductive output and the intensity of infection. Infected females produced heavier-than-average fledglings with higher-than-expected recruitment success late in the season. This reversal of the typical seasonal trend in reproductive output compensated them for lower fledging and recruitment rates compared to uninfected birds earlier in the season. Thus, despite different seasonal patterns of reproductive performance the overall number of recruits was the same for infected versus uninfected birds. A possible explanation for our results is that infected females breed in a different microhabitat where food availability is higher late in the season but also is the risk of infection. Thus, our results suggest that another trade-off than the one we aimed to test is more important for explaining variation in reproductive performance in this natural population: female flycatchers appear to face a trade-off between the risk of infection and reproductive success late in the season.

  • 27.
    Marzal, Julia Carolina Segami
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rudh, Andreas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rogell, Björn
    Stockholm Univ, Dept Zool Ecol, Stockholm, Sweden..
    Ödeen, Anders
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lovlie, Hanne
    Linkoping Univ, IFM Biol, Linkoping, Sweden..
    Rosher, Charlotte
    Linkoping Univ, IFM Biol, Linkoping, Sweden.;Univ Manchester, Fac Life Sci, Manchester, Lancs, England..
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Cryptic female Strawberry poison frogs experience elevated predation risk when associating with an aposematic partner2017In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 7, no 2, 744-750 p.Article in journal (Refereed)
    Abstract [en]

    Population divergence in sexual signals may lead to speciation through prezygotic isolation. Sexual signals can change solely due to variation in the level of natural selection acting against conspicuousness. However, directional mate choice (i.e., favoring conspicuousness) across different environments may lead to gene flow between populations, thereby delaying or even preventing the evolution of reproductive barriers and speciation. In this study, we test whether natural selection through predation upon mate-choosing females can favor corresponding changes in mate preferences. Our study system, Oophaga pumilio, is an extremely color polymorphic neotropical frog with two distinctive antipredator strategies: aposematism and crypsis. The conspicuous coloration and calling behavior of aposematic males may attract both cryptic and aposematic females, but predation may select against cryptic females choosing aposematic males. We used an experimental approach where domestic fowl were encouraged to find digitized images of cryptic frogs at different distances from aposematic partners. We found that the estimated survival time of a cryptic frog was reduced when associating with an aposematic partner. Hence, predation may act as a direct selective force on female choice, favoring evolution of color assortative mating that, in turn, may strengthen the divergence in coloration that natural selection has generated.

  • 28.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sirkiä, Päivi
    Univ Helsinki, Finnish Museum Nat Hist, Zool Unit, Helsinki, Finland; Univ Turku, Sect Ecol, Dept Biol, Turku, Finland.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Hybrid Dysfunction Expressed as Elevated Metabolic Rate in Male Ficedula Flycatchers2016In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, no 9, e0161547Article in journal (Refereed)
    Abstract [en]

    Studies of ecological speciation are often biased towards extrinsic sources of selection against hybrids, resulting from intermediate hybrid morphology, but the knowledge of how genetic incompatibilities accumulate over time under natural conditions is limited. Here we focus on a physiological trait, metabolic rate, which is central to life history strategies and thermoregulation but is also likely to be sensitive to mismatched mitonuclear interactions. We measured the resting metabolic rate of male collared, and pied flycatchers as well as of naturally occurring F1 hybrid males, in a recent hybrid zone. We found that hybrid males had a higher rather than intermediate metabolic rate, which is indicative of hybrid physiological dysfunction. Fitness costs associated with elevated metabolic rate are typically environmentally dependent and exaggerated under harsh conditions. By focusing on male hybrid dysfunction in an eco-physiological trait, our results contribute to the general understanding of how combined extrinsic and intrinsic sources of hybrid dysfunction build up under natural conditions.

  • 29.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Sirkiä, Päivi M.
    Finnish Museum of Natural History, Zoology Unit, University of Helsinki, Finland.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Sexual selection affects climate adaptation in collared flycatchers2017Manuscript (preprint) (Other academic)
    Abstract [en]

    The role of sexual selection in climate adaptation is debated. We tested whether sexual selection has the potential to speed up adaptation to thermal conditions in a natural population of collared flycatchers. Based on a three-year cross-fostering experiment, we found that the size of a sexually selected trait predicted offspring metabolic rate: male collared flycatchers with large forehead patches sired offspring with low metabolic rate regardless of the ambient temperature. Thus, there was a stable significant relationship between forehead patch size of genetic fathers and offspring metabolic rate. Nestlings with high metabolic rate experienced a survival advantage when growing under warm temperatures, while the opposite was true in cold environments. Our study shows that females can modulate their offspring’s physiology through mate choice, and that sexual selection can thus affect climate adaptation.

  • 30.
    McFarlane, S. Eryn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. University of Helsinki.
    Sirkiä, Päivi
    University of Helsinki.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Adjustment of resting metabolic rate by pied flycatchers to the environment promotes regional coexistence with sister speciesArticle in journal (Refereed)
    Abstract [en]

    Differences in life history strategies of closely related species can result in variation in relative fitness across heterogeneous environments and promote coexistence. However, physiological mechanisms mediating such variation in relative fitness have not been identified. Resting metabolic rate (RMR) is tightly associated with life-history strategies and could therefore moderate differences in fitness responses to fluctuations in local environments, particularly when species have evolved to different climatic niches in allopatry. We explore whether differences in RMR match changes in relative fitness between collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca) across environmental conditions experienced in a recent hybrid zone. We found a negative correlation between nestling RMR and temperatures experienced during growth in pied flycatchers, which was absent in collared flycatchers. This implies that pied flycatchers are better adapted to the typical seasonal changes in temperature and food availability experienced at these northern breeding sites. There was sufficient additive genetic variance in RMR to respond to selection in both species that may either facilitate ecological character displacement or lead to a breakdown of coexistence. Generally, subtle differences in climate adaptation may play an important role to patterns of competition, coexistence or displacements between closely related species at recent secondary contact.

  • 31. Morales, Judith
    et al.
    Ruuskanen, Suvi
    Laaksonen, Toni
    Eeva, Tapio
    Mateo, Rafael
    Belskii, Eugen
    Ivankina, Elena V.
    Jarvinen, Antero
    Kerimov, Anvar
    Korpimaki, Erkki
    Krams, Indrikis
    Maend, Raivo
    Morosinotto, Chiara
    Orell, Markku
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Siitari, Heli
    Slater, Fred M.
    Tilgar, Vallo
    Visser, Marcel E.
    Winkel, Wolfgang
    Zang, Herwig
    Moreno, Juan
    Variation in eggshell traits between geographically distant populations of pied flycatchers Ficedula hypoleuca2013In: Journal of Avian Biology, ISSN 0908-8857, E-ISSN 1600-048X, Vol. 44, no 2, 111-120 p.Article in journal (Refereed)
    Abstract [en]

    The expression and impact of maternal effects may vary greatly between populations and environments. However, little is known about large-scale geographical patterns of variation in maternal deposition to eggs. In birds, as in other oviparous animals, the outermost maternal component of an egg is the shell, which protects the embryo, provides essential mineral resources and allows its interaction with the environment in the form of gas exchange. In this study, we explored variation of eggshell traits (mass, thickness, pore density and pigmentation) across 15 pied flycatcher populations at a large geographic scale. We found significant between-population variation in all eggshell traits, except in pore density, suggesting spatial variation in their adaptive benefits or in the females' physiological limitations during egg laying. Between- population variation in shell structure was not due to geographic location (latitude and longitude) or habitat type. However, eggshells were thicker in populations that experienced higher ambient temperature during egg laying. This could be a result of maternal resource allocation to the shell being constrained under low temperatures or of an adaptation to reduce egg water loss under high temperatures. We also found that eggshell colour intensity was positively associated with biliverdin pigment concentration, shell thickness and pore density. To conclude, our findings reveal large- scale between-population variation of eggshell traits, although we found little environmental dependency in their expression. Our findings call for further studies that explore other environmental factors (e.g. calcium availability and pollution levels) and social factors like sexual selection intensity that may account for differences in shell structure between populations.

  • 32. Part, Tomas
    et al.
    Arlt, Debora
    Doligez, Blandine
    Low, Matthew
    Qvarnstrom, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Prospectors combine social and environmental information to improve habitat selection and breeding success in the subsequent year2011In: Journal of Animal Ecology, ISSN 0021-8790, E-ISSN 1365-2656, Vol. 80, no 6, 1227-1235 p.Article in journal (Refereed)
    Abstract [en]

    1. Because habitats have profound effects on individual fitness, there is strong selection for improving the choice of breeding habitat. One possible mechanism is for individuals to use public information when prospecting future breeding sites; however, to our knowledge, no study has shown prospecting behaviour to be directly linked to subsequent choice of breeding site and future reproductive success.

    2. We collected long-term data on territory-specific prospecting behaviour and subsequent breeding in the short-lived northern wheatear (Oenanthe oenanthe). Non-breeders established prospecting territories (<2 ha) that overlapped the breeding territories of conspecifics. We tested whether: (i) prospectors used social and environmental cues that predicted territory-specific breeding success in the following year, and (ii) the prospecting territory was tightly linked to the subsequent breeding territory of the prospector, and whether this link would be weakened by intraspecific competition with original territory owners if they also survived.

    3. As expected, prospectors were attracted to a combination of site-specific cues that predicted future breeding success, i. e. short ground vegetation, a successfully breeding focal pair and successful close neighbours.

    4. Prospecting behaviour was directly linked to the choice of the following year's breeding territory: 79% of surviving prospectors established a breeding territory at their prospecting site in the following year, with their breeding success being higher than other individuals of the same age. As predicted, fidelity to the prospected site was strongly dependent on whether the original territory owner of the same sex had died or moved.

    5. Our findings suggest that the use of multiple cues reduces the negative impact of stochasticity on the reliability of social cues at small spatial scales (e. g. territories) and hence increases the probability of breeding success in the next year. Also, the use of conspecific attraction (i. e. the preference for breeding aggregations) is selectively advantageous because individuals are more likely to find a vacancy in an aggregation as compared to a solitary site. By extension, we hypothesize that species life-history traits may influence the spatial scale of prospecting behaviour and habitat selection strategies.

  • 33. Price, TD
    et al.
    Qvarnström, Anna
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Irwin, DE
    The role of phenotypic plasticity in driving genetic evolution2003In: Proceedings of the Royal Society Biological Sciences, Vol. 270, 1433-1440 p.Article in journal (Refereed)
  • 34.
    Qvarnström, A
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Brommer, JE
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Gustafsson, L
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Testing the genetics underlying the co-evolution of mate choice and ornament in the wild2006In: Nature, Vol. 441, 84-86 p.Article in journal (Refereed)
  • 35.
    Qvarnström, A
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Department of Evolution, Genomics and Systematics, Evolutionary Biology.
    Haavie, J
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Department of Evolution, Genomics and Systematics, Evolutionary Biology. Evolutionsbiologi.
    Saether, S A
    Eriksson, D
    Pärt, T
    Song similarity predicts hybridization in flycatchers.2006In: J Evol Biol, ISSN 1010-061X, Vol. 19, no 4, 1202-9 p.Article in journal (Refereed)
    Abstract [en]

    Given that population divergence in sexual signals is an important prerequisite for reproductive isolation, a key prediction is that cases of signal convergence should lead to hybridization. However, empirical studies that quantitatively demonstrate links between phenotypic characters of individuals and their likelihood to hybridize are rare. Here we show that song convergence between sympatric pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) influence social and sexual interactions between the two species. In sympatry, the majority of male pied flycatchers (65%) include various parts of collared flycatcher song in their song repertoire (but not vice versa). Playback experiments on male interactions demonstrate that male collared flycatchers respond similarly to this 'mixed' song as to conspecific song. Long-term data on pairing patterns show that males singing a converged song attract females of the other species: female collared flycatchers only pair with male pied flycatchers if the males sing the mixed song type. From the perspective of a male pied flycatcher, singing a mixed song type is associated with 30% likelihood of hybridization. This result, combined with our estimates of the frequency of mixed singers, accurately predicts the observed occurrence of hybridization among male pied flycatchers in our study populations (20.45% of 484 pairs; predicted 19.5%). Our results support the suggestion that song functions as the most important prezygotic isolation mechanism in many birds.

  • 36.
    Qvarnström, A
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Haavie, J
    Saether, SA
    Eriksson, D
    Pärt, T
    Song similarity predicts hybridization in flycatchers2006In: Journal of Evolutionary Biology, Vol. 19, 1202-1209 p.Article in journal (Refereed)
  • 37.
    Qvarnström, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Bailey, Richard I.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution.
    Speciation through evolution of sex-linked genes2009In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 102, no 1, 4-15 p.Article, review/survey (Refereed)
    Abstract [en]

    Identification of genes involved in reproductive isolation opens novel ways to investigate links between stages of the speciation process. Are the genes coding for ecological adaptations and sexual isolation the same that eventually lead to hybrid sterility and inviability? We review the role of sex-linked genes at different stages of speciation based on four main differences between sex chromosomes and autosomes; ( 1) relative speed of evolution, ( 2) non-random accumulation of genes, ( 3) exposure of incompatible recessive genes in hybrids and ( 4) recombination rate. At early stages of population divergence ecological differences appear mainly determined by autosomal genes, but fast-evolving sex-linked genes are likely to play an important role for the evolution of sexual isolation by coding for traits with sex-specific fitness effects ( for example, primary and secondary sexual traits). Empirical evidence supports this expectation but mainly in female-heterogametic taxa. By contrast, there is clear evidence for both strong X- and Z-linkage of hybrid sterility and inviability at later stages of speciation. Hence genes coding for sexual isolation traits are more likely to eventually cause hybrid sterility when they are sex-linked. We conclude that the link between sexual isolation and evolution of hybrid sterility is more intuitive in male-heterogametic taxa because recessive sexually antagonistic genes are expected to quickly accumulate on the X-chromosome. However, the broader range of sexual traits that are expected to accumulate on the Z-chromosome may facilitate adaptive speciation in female-heterogametic species by allowing male signals and female preferences to remain in linkage disequilibrium despite periods of gene flow.

  • 38.
    Qvarnström, Anna
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Blomgren, V
    Wiley, Chris
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Svedin, Nina
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Female collared flycatchers learn to prefer maöes with an artificial npvel ornament2004In: Behavioral Ecology, Vol. 15, 543-548 p.Article in journal (Refereed)
  • 39.
    Qvarnström, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Rice, Amber M.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Speciation in Ficedula flycatchers2010In: Philosophical Transactions of the Royal Society of London. Biological Sciences, ISSN 0962-8436, E-ISSN 1471-2970, Vol. 365, no 1547, 1841-1852 p.Article, review/survey (Refereed)
    Abstract [en]

    Speciation in animals often requires that population divergence goes through three major evolutionary stages, i.e. ecological divergence, development of sexual isolation and the build-up of genetic incompatibility. There is theoretical consensus regarding favourable conditions required for speciation to reach its final and irreversible stage, but empirical tests remain rare. Here, we review recent research on processes of speciation, based on studies in hybrid zones between collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca). A major advantage of this study system is that questions concerning all three major sources of reproductive isolation and their interconnections can be addressed. We conclude that (i) ecological divergence is caused by divergence in life-history traits, (ii) females prefer mates of their own species based on differences in both plumage and song characteristics, (iii) male plumage characteristics have diverged but their song has converged in sympatry, (iv) there is genetic incompatibility in accordance with Haldane's rule, and (v) the Z-chromosome appears to be a hotspot for genes involved in sexual isolation and genetic incompatibility. We discuss how identification of the genes underlying the three major sources of reproductive isolation can be used to draw conclusions about links between the processes driving their evolution.

  • 40.
    Qvarnström, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rudh, Andreas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Edström, Torkel
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ödeen, Anders
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lovlie, Hanne
    Tullberg, Birgitta S.
    Coarse Dark Patterning Functionally Constrains Adaptive Shifts from Aposematism to Crypsis in Strawberry Poison Frogs2014In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 68, no 10, 2793-2803 p.Article in journal (Refereed)
    Abstract [en]

    Ecological specialization often requires tight coevolution of several traits, which may constrain future evolutionary pathways and make species more prone to extinction. Aposematism and crypsis represent two specialized adaptations to avoid predation. We tested whether the combined effects of color and pattern on prey conspicuousness functionally constrain or facilitate shifts between these two adaptations. We combined data from 17 natural populations of strawberry poison frogs, Oophaga pumilio with an experimental approach using digitalized images of frogs and chickens as predators. We show that bright coloration often co-occurs with coarse patterning among the natural populations. Dull green frogs with coarse patterning are rare in nature but in the experiment they were as easily detected as bright red frogs suggesting that this trait combination represents a transient evolutionary state toward aposematism. Hence, a gain of either bright color or coarse patterning leads to conspicuousness, but a transition back to crypsis would be functionally constrained in populations with both bright color and coarse patterning by requiring simultaneous changes in two traits. Thus, populations (or species) signaling aposematism by conspicuous color should be less likely to face an evolutionary dead end and more likely to radiate than populations with both conspicuous color and coarse patterning.

  • 41.
    Qvarnström, Anna
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Sheldon, BC
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Pärt, T
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Evolutionary Biology. Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Male ornamentation, timing of breeding, and cost of polygyny in the collared flycatcher2003In: Behavioral Ecology, Vol. 14, 68-73 p.Article in journal (Refereed)
  • 42.
    Qvarnström, Anna
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Svedin, Nina
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Wiley, Chris
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Veen, Tor
    Gustafsson, Lars
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Corss-fostering reveals seasonal changes in the relative fitness of two competring species of flycatchers2005In: Biology Letters, Vol. 1, 68-71 p.Article in journal (Refereed)
  • 43.
    Qvarnström, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Vallin, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Rudh, Andreas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    The role of male contest competition over mates in speciation2012In: Current Zoology, ISSN 1674-5507, Vol. 58, no 3, 493-509 p.Article in journal (Refereed)
    Abstract [en]

    Research on the role of sexual selection in the speciation process largely focuses on the diversifying role of mate choice. In particular, much attention has been drawn to the fact that population divergence in mate choice and in the male traits subject to choice directly can lead to assortative mating. However, male contest competition over mates also constitutes an important mechanism of sexual selection. We review recent empirical studies and argue that sexual selection through male contest competition can affect speciation in ways other than mate choice. For example, biases in aggression towards similar competitors can lead to disruptive and negative frequency-dependent selection on the traits used in contest competition in a similar way as competition for other types of limited resources. Moreover, male contest abilities often trade-off against other abilities such as parasite resistance, protection against predators and general stress tolerance. Populations experiencing different ecological conditions should therefore quickly diverge non-randomly in a number of traits including male contest abilities. In resource based breeding systems, a feedback loop between competitive ability and habitat use may lead to further population divergence. We discuss how population divergence in traits used in male contest competition can lead to the build up of reproductive isolation through a number of different pathways. Our main conclusion is that the role of male contest competition in speciation remains largely scientifically unexplored.

  • 44.
    Qvarnström, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Vogel Kehlenbeck, Jenny
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Wiley, Chris
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Svedin, Nina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Saether, Stein Are
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Population Biology.
    Species divergence in offspring begging intensity: Difference in need or manipulation of parents?2007In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 274, no 1612, 1003-1008 p.Article in journal (Refereed)
    Abstract [en]

    Conflicts over the delivery and sharing of food among family members are expected to lead to evolution of exaggerated offspring begging for food. Coevolution between offspring begging intensity and parent response depends on the genetic architecture of the traits involved. Given a genetic correlation between offspring begging intensity and parental response, there may be fast and arbitrary divergence in these behaviours between populations. However, there is limited knowledge about the genetic basis of offspring solicitation and parental response and whether these traits are genetically correlated. In this study, we performed a partial cross-fostering experiment of young between pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) and recorded the behaviour of individual offspring and their (foster)parents. We found that nestling collared flycatchers reached a higher phenotypic quality, estimated both as mass at fledging and as intensity of their T-lymphocyte-mediated immune response when raised by heterospecific foster parents. However, although collared flycatchers begged relatively more intensively, we found no evidence of corresponding higher resistance (i.e. lower feeding rate) of adult collared flycatchers than of adult pied flycatchers. Thus, the difference in offspring begging intensity between the two species seems not to be a result of a difference in escalation of the parent–offspring conflict. Instead, the species' divergence in exaggeration of offspring begging intensity ‘honestly’ matches a difference between the species in offspring need. This interpretation is strengthened by the fact that the difference in begging intensity between the two species increased as the season progressed, coinciding with the higher sensitivity of nestling collared flycatchers to the seasonal decline in food availability. Thus, the behavioural differentiation appears to be a direct consequence of a life-history differentiation (offspring growth patterns).

  • 45.
    Qvarnström, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Wiley, Chris
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Svedin, Nina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Vallin, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Life-history divergence facilitates regional coexistence of competing Ficedula flycatchers2009In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 90, no 7, 1948-1957 p.Article in journal (Refereed)
    Abstract [en]

    Regional coexistence of ecologically similar species is facilitated when fluctuations in environmental conditions favor different species at different times or places. However, why species with similar ecology should vary in their response to environmental change is unclear. In this study, we explore the role of a life-history divergence in causing changes in relative fitness across environmental conditions experienced by populations of two closely related Ficedula flycatchers on the Baltic island of Oland, Sweden. We compared patterns of nestling survival between Pied (Ficedula hypoleuca) and Collared (F. albicollis) Flycatchers in relation to two factors known to influence the environment experienced by nestlings: natural variation in their parents' onset of breeding and artificial manipulation of the brood size. Possible differences in the location of the nests (i.e., microhabitat differences) or in habitat use (i.e., feeding patterns) by the adult birds were controlled for by partial cross-fostering of young between the two species. We found that nestling mortality was relatively higher among Collared Flycatchers and that this difference increased with later breeding. Mass gain, which predicted survival probability, of nestling Collared Flycatchers did not respond to the seasonal decline in environmental conditions when they were raised in nests with reduced brood size (i.e., where sibling competition was experimentally reduced). This latter result suggests that the smaller clutch size of Collared Flycatchers reflects an adaptive adjustment to their offspring's higher sensitivity to environmental change. We discuss the possibility that the divergence in life-history traits between the two species represents adaptation to different environments experienced during their recent evolutionary history. We conclude that the survival of nestling Collared Flycatchers is more sensitive to harsh environment and that this is likely to limit where and when the more aggressive Collared Flycatchers are able to displace Pied Flycatchers. Our results provide support for models of species coexistence that emphasize the importance of spatial or temporal heterogeneity in relative fitness or life-history divergence. More precisely, our results demonstrate that variation in life-history adaptations may result in changes in relative fitness of species across environments despite their use of similar resources.

  • 46.
    Qvarnström, Anna
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ålund, Murielle
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    McFarlane, Eryn S.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sirkiä, Päivi M.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Climate adaptation and speciation: particular focus on reproductive barriers in Ficedula flycatchers2015In: Evolutionary Applications, ISSN 1752-4571, E-ISSN 1752-4571, Vol. 9, no 1, 119-134 p.Article, review/survey (Refereed)
    Abstract [en]

    Climate adaptation is surprisingly rarely reported as a cause for the build-up of reproductive isolation between diverging populations. In this review, we summarize evidence for effects of climate adaptation on pre- and postzygotic isolation between emerging species with a particular focus on pied (Ficedula hypoleuca) and collared (Ficedula albicollis) flycatchers as a model for research on speciation. Effects of climate adaptation on prezygotic isolation or extrinsic selection against hybrids have been documented in several taxa, but the combined action of climate adaptation and sexual selection is particularly well explored in Ficedula flycatchers. There is a general lack of evidence for divergent climate adaptation causing intrinsic postzygotic isolation. However, we argue that the profound effects of divergence in climate adaptation on the whole biochemical machinery of organisms and hence many underlying genes should increase the likelihood of genetic incompatibilities arising as side effects. Fast temperature-dependent co-evolution between mitochondrial and nuclear genomes may be particularly likely to lead to hybrid sterility. Thus, how climate adaptation relates to reproductive isolation is best explored in relation to fast-evolving barriers to gene flow, while more research on later stages of divergence is needed to achieve a complete understanding of climate-driven speciation.

  • 47.
    Rice, Amber M.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Rudh, Andreas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Ellegren, Hans
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    A guide to the genomics of ecological speciation in natural animal populations2011In: Ecology Letters, ISSN 1461-023X, E-ISSN 1461-0248, Vol. 14, no 1, 9-18 p.Article in journal (Refereed)
    Abstract [en]

    Interest in ecological speciation is growing, as evidence accumulates showing that natural selection can lead to rapid divergence between subpopulations. However, whether and how ecological divergence can lead to the buildup of reproductive isolation remains under debate. What is the relative importance of natural selection vs. neutral processes? How does adaptation generate reproductive isolation? Can ecological speciation occur despite homogenizing gene flow? These questions can be addressed using genomic approaches, and with the rapid development of genomic technology, will become more answerable in studies of wild populations than ever before. In this article, we identify open questions in ecological speciation theory and suggest useful genomic methods for addressing these questions in natural animal populations. We aim to provide a practical guide for ecologists interested in incorporating genomic methods into their research programs. An increased integration between ecological research and genomics has the potential to shed novel light on the origin of species.

  • 48.
    Rice, Amber M.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Vallin, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kulma, Katarzyna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Arntsen, Hanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Husby, Arild
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Tobler, Michael
    Qvarnstrom, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Optimizing the trade-off between offspring number and quality in unpredictable environments: Testing the role of differential androgen transfer to collared flycatcher eggs2013In: Hormones and Behavior, ISSN 0018-506X, E-ISSN 1095-6867, Vol. 63, no 5, 813-822 p.Article in journal (Refereed)
    Abstract [en]

    According to the brood reduction hypothesis, parents adjust their brood size in response to current environmental conditions. When resources are abundant, parents can successfully raise all hatched offspring, but when resources are scarce, brood reduction, i.e., the sacrifice of some siblings to secure the quality of a subset of offspring, may maximize fitness. Differential transfer of maternal androgens is one potential proximate mechanism through which female birds may facilitate brood reduction because it may alter the relative competitive ability of sibling nestlings. We tested the hypothesis that female collared flycatchers (Ficedula albicollis) manipulate sibling competition by transferring less androgens to eggs late in the laying sequence. We experimentally elevated androgen levels in i) whole clutches and ii) only the two last laid eggs, and compared growth and begging behavior of offspring from these treatments with a control treatment. By using three treatments and video assessment of begging, we examined the effects of within-clutch patterns of yolk androgen transfer on levels of sibling competition in situ. When androgens were elevated in only the two last laid eggs, begging was more even among siblings compared to control nests. We also found that female nestlings receiving additional yolk androgens showed higher mass gain later in the breeding season, while their male counterparts did not. Our results suggest that females may improve reproductive success in unpredictable environments by altering within-clutch patterns of yolk androgen transfer. We discuss the possibility that life-history divergence between the co-occurring collared and pied flycatcher (Ficedula hypoleuca) is amplified by patterns of yolk androgen transfer.

  • 49. Robinson, Matthew R
    et al.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Influence of the Environment on the Genetic Architecture of Traits Involved in Sexual Selection within Wild Populations2014In: Genotype-by-Environment Interactions and Sexual Selection, John Wiley & Sons, 2014Chapter in book (Refereed)
  • 50. Robinson, Matthew R.
    et al.
    van Doorn, G. Sander
    Gustafsson, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Qvarnström, Anna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Environment-dependent selection on mate choice in a natural population of birds2012In: Ecology Letters, ISSN 1461-023X, E-ISSN 1461-0248, Vol. 15, no 6, 611-618 p.Article in journal (Refereed)
    Abstract [en]

    Female mate choice acts as an important evolutionary force, yet the influence of the environment on both its expression and the selective pressures acting upon it remains unknown. We found consistent heritable differences between females in their choice of mate based on ornament size during a 25-year study of a population of collared flycatchers. However, the fitness consequences of mate choice were dependent on environmental conditions experienced whilst breeding. Females breeding with highly ornamented males experienced high relative fitness during dry summer conditions, but low relative fitness during wetter years. Our results imply that sexual selection within a population can be highly variable and dependent upon the prevailing weather conditions experienced by individuals.

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