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1.
  • Antoniazza, Sylvain, et al. (author)
  • Local adaptation maintains clinal variation in melanin-based coloration of European barn owls (Tyto alba).
  • 2010
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 64:7, s. 1944-1954
  • Journal article (peer-reviewed)abstract
    • Ecological parameters vary in space, and the resulting heterogeneity of selective forces can drive adaptive population divergence. Clinal variation represents a classical model to study the interplay of gene flow and selection in the dynamics of this local adaptation process. Although geographic variation in phenotypic traits in discrete populations could be remainders of past adaptation, maintenance of adaptive clinal variation requires recurrent selection. Clinal variation in genetically determined traits is generally attributed to adaptation of different genotypes to local conditions along an environmental gradient, although it can as well arise from neutral processes. Here, we investigated whether selection accounts for the strong clinal variation observed in a highly heritable pheomelanin-based color trait in the European barn owl by comparing spatial differentiation of color and of neutral genes among populations. Barn owl's coloration varies continuously from white in southwestern Europe to reddish-brown in northeastern Europe. A very low differentiation at neutral genetic markers suggests that substantial gene flow occurs among populations. The persistence of pronounced color differentiation despite this strong gene flow is consistent with the hypothesis that selection is the primary force maintaining color variation among European populations. Therefore, the color cline is most likely the result of local adaptation.
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2.
  • Antoniazza, Sylvain, et al. (author)
  • Natural selection in a postglacial range expansion : the case of the colour cline in the European barn owl
  • 2014
  • In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 23:22, s. 5508-5523
  • Research review (peer-reviewed)abstract
    • Gradients of variationor clineshave always intrigued biologists. Classically, they have been interpreted as the outcomes of antagonistic interactions between selection and gene flow. Alternatively, clines may also establish neutrally with isolation by distance (IBD) or secondary contact between previously isolated populations. The relative importance of natural selection and these two neutral processes in the establishment of clinal variation can be tested by comparing genetic differentiation at neutral genetic markers and at the studied trait. A third neutral process, surfing of a newly arisen mutation during the colonization of a new habitat, is more difficult to test. Here, we designed a spatially explicit approximate Bayesian computation (ABC) simulation framework to evaluate whether the strong cline in the genetically based reddish coloration observed in the European barn owl (Tyto alba) arose as a by-product of a range expansion or whether selection has to be invoked to explain this colour cline, for which we have previously ruled out the actions of IBD or secondary contact. Using ABC simulations and genetic data on 390 individuals from 20 locations genotyped at 22 microsatellites loci, we first determined how barn owls colonized Europe after the last glaciation. Using these results in new simulations on the evolution of the colour phenotype, and assuming various genetic architectures for the colour trait, we demonstrate that the observed colour cline cannot be due to the surfing of a neutral mutation. Taking advantage of spatially explicit ABC, which proved to be a powerful method to disentangle the respective roles of selection and drift in range expansions, we conclude that the formation of the colour cline observed in the barn owl must be due to natural selection.
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3.
  • Burri, Reto, et al. (author)
  • Adaptive divergence of ancient gene duplicates in the avian MHC class II beta
  • 2010
  • In: Molecular biology and evolution. - : Oxford University Press (OUP). - 0737-4038 .- 1537-1719. ; 27:10, s. 2360-2374
  • Journal article (peer-reviewed)abstract
    • Gene duplication and neofunctionalization are known to be important processes in the evolution of phenotypic complexity. They account for important evolutionary novelties that confer ecological adaptation, such as the major histocompatibility complex (MHC), a multigene family crucial to the vertebrate immune system. In birds, two MHC class II β (MHCIIβ) exon 3 lineages have been recently characterized, and two hypotheses for the evolutionary history of MHCIIβ lineages were proposed. These lineages could have arisen either by 1) an ancient duplication and subsequent divergence of one paralog or by 2) recent parallel duplications followed by functional convergence. Here, we compiled a data set consisting of 63 MHCIIβ exon 3 sequences from six avian orders to distinguish between these hypotheses and to understand the role of selection in the divergent evolution of the two avian MHCIIβ lineages. Based on phylogenetic reconstructions and simulations, we show that a unique duplication event preceding the major avian radiations gave rise to two ancestral MHCIIβ lineages that were each likely lost once later during avian evolution. Maximum likelihood estimation shows that following the ancestral duplication, positive selection drove a radical shift from basic to acidic amino acid composition of a protein domain facing the α-chain in the MHCII α β-heterodimer. Structural analyses of the MHCII α β-heterodimer highlight that three of these residues are potentially involved in direct interactions with the α-chain, suggesting that the shift following duplication may have been accompanied by coevolution of the interacting α- and β-chains. These results provide new insights into the long-term evolutionary relationships among avian MHC genes and open interesting perspectives for comparative and population genomic studies of avian MHC evolution.
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4.
  • Burri, Reto, et al. (author)
  • Evolutionary patterns of MHC class II B in owls and their implications for the understanding of avian MHC evolution
  • 2008
  • In: Molecular biology and evolution. - : Oxford University Press (OUP). - 0737-4038 .- 1537-1719. ; 25:6, s. 1180-1191
  • Journal article (peer-reviewed)abstract
    • Owing to its special mode of evolution and central role in the adaptive immune system, the major histocompatibility complex (MHC) has become the focus of diverse disciplines such as immunology, evolutionary ecology, and molecular evolution. MHC evolution has been studied extensively in diverse vertebrate lineages over the last few decades, and it has been suggested that birds differ from the established mammalian norm. Mammalian MHC genes evolve independently, and duplication history (i.e., orthology) can usually be traced back within lineages. In birds, this has been observed in only 3 pairs of closely related species. Here we report strong evidence for the persistence of orthology of MHC genes throughout an entire avian order. Phylogenetic reconstructions of MHC class II B genes in 14 species of owls trace back orthology over tens of thousands of years in exon 3. Moreover, exon 2 sequences from several species show closer relationships than sequences within species, resembling transspecies evolution typically observed in mammals. Thus, although previous studies suggested that long-term evolutionary dynamics of the avian MHC was characterized by high rates of concerted evolution, resulting in rapid masking of orthology, our results question the generality of this conclusion. The owl MHC thus opens new perspectives for a more comprehensive understanding of avian MHC evolution.
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5.
  • Burri, Reto, et al. (author)
  • Isolation and characterization of 21 microsatellite markers in the barn owl (Tyto alba)
  • 2008
  • In: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 8:5, s. 977-979
  • Journal article (peer-reviewed)abstract
    • We report 21 new polymorphic microsatellite markers in the European barn owl (Tyto alba). The polymorphism of the reported markers was evaluated in a population situated in western Switzerland and in another from Tenerife, Canary Islands. The number of alleles per locus varies between two and 31, and expected heterozygosity per population ranges from 0.16 to 0.95. All loci are in Hardy-Weinberg equilibrium and no linkage disequilibrium was detected. Two loci exhibit a null allele in the Tenerife population.
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6.
  • Burri, Reto, et al. (author)
  • Isolation and characterization of major histocompatibility complex (MHC) class II B genes in the Barn owl (Aves: Tyto alba)
  • 2008
  • In: Immunogenetics. - : Springer Science and Business Media LLC. - 0093-7711 .- 1432-1211. ; 60:9, s. 543-550
  • Journal article (peer-reviewed)abstract
    • We isolated major histocompatibility complex class II B (MHCIIB) genes in the Barn owl (Tyto alba). A PCR-based approach combined with primer walking on genomic and complementary DNA as well as Southern blot analyses revealed the presence of two MHCIIB genes, both being expressed in spleen, liver, and blood. Characteristic structural features of MHCIIB genes as well as their expression and high non-synonymous substitution rates in the region involved in antigen binding suggest that both genes are functional. MHC organization in the Barn owl is simple compared to passerine species that show multiple duplications, and resembles the minimal essential MHC of chicken.
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7.
  • Burri, Reto, et al. (author)
  • Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers
  • 2015
  • In: Genome Research. - : Cold Spring Harbor Laboratory. - 1088-9051 .- 1549-5469. ; 25:11, s. 1656-1665
  • Journal article (peer-reviewed)abstract
    • 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.
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8.
  • Burri, Reto, et al. (author)
  • PCR-based isolation of multigene families : Lessons from the avian MHC class IIB.
  • 2014
  • In: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 14:4, s. 778-788
  • Journal article (peer-reviewed)abstract
    • The amount of sequence data available today highly facilitates the access to genes from many gene families. Primers amplifying the desired genes over a range of species are readily obtained by aligning conserved gene regions, and laborious gene isolation procedures can often be replaced by quicker PCR-based approaches. However, in the case of multigene families, PCR-based approaches bear the often ignored risk of incomplete isolation of family members. This problem is most prominent in gene families with highly variable and thus unpredictable number of gene copies among species, such as in the major histocompatibility complex (MHC). In the present study we (i) report new primers for the isolation of the MHC class IIB (MHCIIB) gene family in birds, and (ii) share our experience with isolating MHCIIB genes from an unprecedented number of avian species from all over the avian phylogeny. We report important and usually underappreciated problems encountered during PCR-based multigene family isolation, and provide a collection of measures to help significantly improving the chance of successfully isolating complete multigene families using PCR-based approaches.
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9.
  • Burri, Reto, et al. (author)
  • The genetic basis of color-related local adaptation in a ring-like colonization around the Mediterranean
  • 2016
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 70:1, s. 140-153
  • Journal article (peer-reviewed)abstract
    • Uncovering the genetic basis of phenotypic variation and the population history under which it established is key to understand the trajectories along which local adaptation evolves. Here, we investigated the genetic basis and evolutionary history of a clinal plumage color polymorphism in European barn owls (Tyto alba). Our results suggest that barn owls colonized the Western Palearctic in a ring-like manner around the Mediterranean and meet in secondary contact in Greece. Rufous coloration appears to be linked to a recently evolved nonsynonymous-derived variant of the melanocortin 1 receptor (MC1R) gene, which according to quantitative genetic analyses evolved under local adaptation during or following the colonization of Central Europe. Admixture patterns and linkage disequilibrium between the neutral genetic background and color found exclusively within the secondary contact zone suggest limited introgression at secondary contact. These results from a system reminiscent of ring species provide a striking example of how local adaptation can evolve from derived genetic variation.
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10.
  • Collin, Helene, et al. (author)
  • Combining molecular evolution and environmental genomics to unravel adaptive processes of MHC class IIB diversity in European minnows (Phoxinus phoxinus)
  • 2013
  • In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 3:8, s. 2568-2585
  • Journal article (peer-reviewed)abstract
    • Host-pathogen interactions are a major evolutionary force promoting local adaptation. Genes of the major histocompatibility complex (MHC) represent unique candidates to investigate evolutionary processes driving local adaptation to parasite communities. The present study aimed at identifying the relative roles of neutral and adaptive processes driving the evolution of MHC class IIB (MHCIIB) genes in natural populations of European minnows (Phoxinus phoxinus). To this end, we isolated and genotyped exon 2 of two MHCIIB gene duplicates (DAB1 and DAB3) and 1665 amplified fragment length polymorphism (AFLP) markers in nine populations, and characterized local bacterial communities by 16S rDNA barcoding using 454 amplicon sequencing. Both MHCIIB loci exhibited signs of historical balancing selection. Whereas genetic differentiation exceeded that of neutral markers at both loci, the populations' genetic diversities were positively correlated with local pathogen diversities only at DAB3. Overall, our results suggest pathogen-mediated local adaptation in European minnows at both MHCIIB loci. While at DAB1 selection appears to favor different alleles among populations, this is only partially the case in DAB3, which appears to be locally adapted to pathogen communities in terms of genetic diversity. These results provide new insights into the importance of host-pathogen interactions in driving local adaptation in the European minnow, and highlight that the importance of adaptive processes driving MHCIIB gene evolution may differ among duplicates within species, presumably as a consequence of alternative selective regimes or different genomic context.
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11.
  • Dreiss, A N, et al. (author)
  • Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration.
  • 2012
  • In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 25:1, s. 103-114
  • Journal article (peer-reviewed)abstract
    • Local adaptation is a major mechanism underlying the maintenance of phenotypic variation in spatially heterogeneous environments. In the barn owl (Tyto alba), dark and pale reddish-pheomelanic individuals are adapted to conditions prevailing in northern and southern Europe, respectively. Using a long-term dataset from Central Europe, we report results consistent with the hypothesis that the different pheomelanic phenotypes are adapted to specific local conditions in females, but not in males. Compared to whitish females, reddish females bred in sites surrounded by more arable fields and less forests. Colour-dependent habitat choice was apparently beneficial. First, whitish females produced more fledglings when breeding in wooded areas, whereas reddish females when breeding in sites with more arable fields. Second, cross-fostering experiments showed that female nestlings grew wings more rapidly when both their foster and biological mothers were of similar colour. The latter result suggests that mothers should particularly produce daughters in environments that best match their own coloration. Accordingly, whiter females produced fewer daughters in territories with more arable fields. In conclusion, females displaying alternative melanic phenotypes bred in habitats providing them with the highest fitness benefits. Although small in magnitude, matching habitat selection and local adaptation may help maintain variation in pheomelanin coloration in the barn owl.
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12.
  • Dutoit, Ludovic, et al. (author)
  • Covariation in levels of nucleotide diversity in homologous regions of the avian genome long after completion of lineage sorting
  • 2017
  • In: Proceedings of the Royal Society of London. Biological Sciences. - : ROYAL SOC. - 0962-8452 .- 1471-2954. ; 284:1849
  • Journal article (peer-reviewed)abstract
    • Closely related species may show similar levels of genetic diversity in homologous regions of the genome owing to shared ancestral variation still segregating in the extant species. However, after completion of lineage sorting, such covariation is not necessarily expected. On the other hand, if the processes that govern genetic diversity are conserved, diversity may potentially covary even among distantly related species. We mapped regions of conserved synteny between the genomes of two divergent bird speciescollared flycatcher and hooded crow-and identified more than 600 Mb of homologous regions (66% of the genome). From analyses of whole-genome resequencing data in large population samples of both species we found nucleotide diversity in 200 kb windows to be well correlated (Spearman's rho = 0.407). The correlation remained highly similar after excluding coding sequences. To explain this covariation, we suggest that a stable avian karyotype and a conserved landscape of recombination rate variation render the diversity-reducing effects of linked selection similar in divergent bird lineages. Principal component regression analysis of several potential explanatory variables driving heterogeneity in flycatcher diversity levels revealed the strongest effects from recombination rate variation and density of coding sequence targets for selection, consistent with linked selection. It is also possible that a stable karyotype is associated with a conserved genomic mutation environment contributing to covariation in diversity levels between lineages. Our observations imply that genetic diversity is to some extent predictable.
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13.
  • Dutoit, Ludovic, et al. (author)
  • Genomic distribution and estimation of nucleotide diversity in natural populations : perspectives from the collared flycatcher (Ficedula albicollis) genome
  • 2017
  • In: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 17:4, s. 586-597
  • Journal article (peer-reviewed)abstract
    • Properly estimating genetic diversity in populations of nonmodel species requires a basic understanding of how diversity is distributed across the genome and among individuals. To this end, we analysed whole-genome resequencing data from 20 collared flycatchers (genome size approximate to 1.1 Gb; 10.13 million single nucleotide polymorphisms detected). Genomewide nucleotide diversity was almost identical among individuals (mean = 0.00394, range = 0.00384-0.00401), but diversity levels varied extensively across the genome (95% confidence interval for 200-kb windows = 0.0013-0.0053). Diversity was related to selective constraint such that in comparison with intergenic DNA, diversity at fourfold degenerate sites was reduced to 85%, 3' UTRs to 82%, 5' UTRs to 70% and nondegenerate sites to 12%. There was a strong positive correlation between diversity and chromosome size, probably driven by a higher density of targets for selection on smaller chromosomes increasing the diversity-reducing effect of linked selection. Simulations exploring the ability of sequence data from a small number of genetic markers to capture the observed diversity clearly demonstrated that diversity estimation from finite sampling of such data is bound to be associated with large confidence intervals. Nevertheless, we show that precision in diversity estimation in large out-bred population benefits from increasing the number of loci rather than the number of individuals. Simulations mimicking RAD sequencing showed that this approach gives accurate estimates of genomewide diversity. Based on the patterns of observed diversity and the performed simulations, we provide broad recommendations for how genetic diversity should be estimated in natural populations.
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14.
  • Ellegren, Hans, et al. (author)
  • The genomic landscape of species divergence in Ficedula flycatchers
  • 2012
  • In: Nature. - : Springer Science and Business Media LLC. - 0028-0836 .- 1476-4687. ; 491:7426, s. 756-760
  • Journal article (peer-reviewed)abstract
    • 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.
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15.
  • Gaigher, A., et al. (author)
  • Family-assisted inference of the genetic architecture of major histocompatibility complex variation
  • 2016
  • In: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 16:6, s. 1353-1364
  • Journal article (peer-reviewed)abstract
    • With their direct link to individual fitness, genes of the major histocompatibility complex (MHC) are a popular system to study the evolution of adaptive genetic diversity. However, owing to the highly dynamic evolution of the MHC region, the isolation, characterization and genotyping of MHC genes remain a major challenge. While high-throughput sequencing technologies now provide unprecedented resolution of the high allelic diversity observed at the MHC, in many species, it remains unclear (i) how alleles are distributed among MHC loci, (ii) whether MHC loci are linked or segregate independently and (iii) how much copy number variation (CNV) can be observed for MHC genes in natural populations. Here, we show that the study of allele segregation patterns within families can provide significant insights in this context. We sequenced two MHC class I (MHC-I) loci in 1267 European barn owls (Tyto alba), including 590 offspring from 130 families using Illumina MiSeq technology. Coupled with a high per-individual sequencing coverage (similar to 3000x), the study of allele segregation patterns within families provided information on three aspects of the architecture of MHC-I variation in barn owls: (i) extensive sharing of alleles among loci, (ii) strong linkage of MHC-I loci indicating tandem architecture and (iii) the presence of CNV in the barn owl MHC-I. We conclude that the additional information that can be gained from high-coverage amplicon sequencing by investigating allele segregation patterns in families not only helps improving the accuracy of MHC genotyping, but also contributes towards enhanced analyses in the context of MHC evolutionary ecology.
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16.
  • Heckel, G, et al. (author)
  • Genetic structure and colonization processes in European populations of the common vole, Microtus arvalis
  • 2005
  • In: Evolution. - 0014-3820 .- 1558-5646. ; 59:10, s. 2231-2242
  • Journal article (peer-reviewed)abstract
    • The level of genetic differentiation within and between evolutionary lineages of the common vole (Microtusarvalis) in Europe was examined by analyzing mitochondrial sequences from the control region (mtDNA) and 12nuclear microsatellite loci (nucDNA) for 338 voles from 18 populations. The distribution of evolutionary lineagesand the affinity of populations to lineages were determined with additional sequence data from the mitochondrialcytochrome b gene. Our analyses demonstrated very high levels of differentiation between populations (overall FST:mtDNA 70%; nucDNA 17%). The affinity of populations to evolutionary lineages was strongly reflected in mtDNAbut not in nucDNA variation. Patterns of genetic structure for both markers visualized in synthetic genetic mapssuggest a postglacial range expansion of the species into the Alps, as well as a potentially more ancient colonizationfrom the northeast to the southwest of Europe. This expansion is supported by estimates for the divergence timesbetween evolutionary lineages and within the western European lineage, which predate the last glacial maximum(LGM). Furthermore, all measures of genetic diversity within populations increased significantly with longitude andshowed a trend toward increase with latitude. We conclude that the detected patterns are difficult to explain only byrange expansions from separate LGM refugia close to the Mediterranean. This suggests that someM. arvalis populationspersisted during the LGM in suitable habitat further north and that the gradients in genetic diversity may representtraces of a more ancient colonization of Europe by the species.
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17.
  • Heg, Dik, et al. (author)
  • Cichlids do not adjust reproductive skew to the availability of independent breeding options
  • 2006
  • In: Behavioral Ecology. - : Oxford University Press (OUP). - 1045-2249 .- 1465-7279. ; 17:3, s. 419-429
  • Journal article (peer-reviewed)abstract
    • Helpers in cooperatively breeding species forego all or part of their reproduction when remaining at home and assisting breeders to raise offspring. Different models of reproductive skew generate alternative predictions about the share of reproduction unrelated subordinates will get depending on the degree of ecological constraints. Concession models predict a larger share when independent breeding options are good, whereas restraint and tug-of-war models predict no effects on reproductive skew. We tested these predictions by determining the share of reproduction by unrelated male and female helpers in the Lake Tanganyika cichlid Neolamprologus pulcher depending on experimentally manipulated possibilities for helper dispersal and independent breeding and depending on helper size and sex. We created 32 breeding groups in the laboratory, consisting of two breeders and two helpers each, where only the helpers had access to a nearby dispersal compartment with (treatment) or without (control) breeding substrate, using a repeated measures design. We determined the paternity and maternity of 1185 offspring from 47 broods using five to nine DNA microsatellite loci and found that: (1) helpers participated in reproduction equally across the treatments, (2) large male helpers were significantly more likely to reproduce than small helpers, and (3) male helpers engaged in significantly more reproduction than female helpers. Interestingly, in four broods, extragroup helper males had fertilized part of the brood. No helper evictions from the group after helper reproduction were observed. Our results suggest that tug-of-war models based on competition over reproduction within groups describe best the reproductive skew observed in our study system. Female breeders produced larger clutches in the treatment compared to the control situation when the large helpers were males. This suggests that male breeder-male helper reproductive conflicts may be alleviated by females producing larger clutches with helpers around.
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18.
  • Henry, Isabelle, et al. (author)
  • Multiple Paternity in Polyandrous Barn Owls (Tyto alba)
  • 2013
  • In: PLOS ONE. - : Public Library of Science (PLoS). - 1932-6203. ; 8:11, s. e80112-
  • Journal article (peer-reviewed)abstract
    • In polyandrous species females produce successive clutches with several males. Female barn owls (Tyto alba) often desert their offspring and mate to produce a 2nd annual brood with a second male. We tested whether copulating during chick rearing at the 1st annual brood increases the male's likelihood to obtain paternity at the 2nd annual breeding attempt of his female mate in case she deserts their brood to produce a second brood with a different male. Using molecular paternity analyses we found that 2 out of 26 (8%) second annual broods of deserting females contained in total 6 extra-pair young out of 15 nestlings. These young were all sired by the male with whom the female had produced the 1st annual brood. In contrast, none of the 49 1st annual breeding attempts (219 offspring) and of the 20 2nd annual breeding attempts (93 offspring) of non-deserting females contained extra-pair young. We suggest that female desertion can select male counter-strategies to increase paternity and hence individual fitness. Alternatively, females may copulate with the 1st male to derive genetic benefits, since he is usually of higher quality than the 2nd male which is commonly a yearling individual.
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19.
  • Kakhki, Niloofar Alaei, et al. (author)
  • A Phylogenomic Assessment of Processes Underpinning Convergent Evolution in Open-Habitat Chats
  • 2023
  • In: Molecular biology and evolution. - : Oxford University Press. - 0737-4038 .- 1537-1719. ; 40:1
  • Journal article (peer-reviewed)abstract
    • Insights into the processes underpinning convergent evolution advance our understanding of the contributions of ancestral, introgressed, and novel genetic variation to phenotypic evolution. Phylogenomic analyses characterizing genome-wide gene tree heterogeneity can provide first clues about the extent of ILS and of introgression and thereby into the potential of these processes or (in their absence) the need to invoke novel mutations to underpin convergent evolution. Here, we were interested in understanding the processes involved in convergent evolution in open-habitat chats (wheatears of the genus Oenanthe and their relatives). To this end, based on whole-genome resequencing data from 50 taxa of 44 species, we established the species tree, characterized gene tree heterogeneity, and investigated the footprints of ILS and introgression within the latter. The species tree corroborates the pattern of abundant convergent evolution, especially in wheatears. The high levels of gene tree heterogeneity in wheatears are explained by ILS alone only for 30% of internal branches. For multiple branches with high gene tree heterogeneity, D-statistics and phylogenetic networks identified footprints of introgression. Finally, long branches without extensive ILS between clades sporting similar phenotypes provide suggestive evidence for the role of novel mutations in the evolution of these phenotypes. Together, our results suggest that convergent evolution in open-habitat chats involved diverse processes and highlight that phenotypic diversification is often complex and best depicted as a network of interacting lineages.
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20.
  • Kawakami, Takeshi, et al. (author)
  • Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array
  • 2014
  • In: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 14:6, s. 1248-1260
  • Journal article (peer-reviewed)abstract
    • 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.
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21.
  • Kawakami, Takeshi, et al. (author)
  • Whole-genome patterns of linkage disequilibrium across flycatcher populations clarify the causes and consequences of fine-scale recombination rate variation in birds
  • 2017
  • In: Molecular Ecology. - : WILEY. - 0962-1083 .- 1365-294X. ; 26:16, s. 4158-4172
  • Journal article (peer-reviewed)abstract
    • Recombination rate is heterogeneous across the genome of various species and so are genetic diversity and differentiation as a consequence of linked selection. However, we still lack a clear picture of the underlying mechanisms for regulating recombination. Here we estimated fine-scale population recombination rate based on the patterns of linkage disequilibrium across the genomes of multiple populations of two closely related flycatcher species (Ficedula albicollis and F. hypoleuca). This revealed an overall conservation of the recombination landscape between these species at the scale of 200 kb, but we also identified differences in the local rate of recombination despite their recent divergence (<1 million years). Genetic diversity and differentiation were associated with recombination rate in a lineage-specific manner, indicating differences in the extent of linked selection between species. We detected 400-3,085 recombination hotspots per population. Location of hotspots was conserved between species, but the intensity of hotspot activity varied between species. Recombination hotspots were primarily associated with CpG islands (CGIs), regardless of whether CGIs were at promoter regions or away from genes. Recombination hotspots were also associated with specific transposable elements (TEs), but this association appears indirect due to shared preferences of the transposition machinery and the recombination machinery for accessible open chromatin regions. Our results suggest that CGIs are a major determinant of the localization of recombination hotspots, and we propose that both the distribution of TEs and fine-scale variation in recombination rate may be associated with the evolution of the epigenetic landscape.
  •  
22.
  • Lutgen, Dave, et al. (author)
  • Linked-read sequencing enables haplotype-resolved resequencing at population scale
  • 2020
  • In: Molecular Ecology Resources. - : WILEY. - 1755-098X .- 1755-0998. ; 20:5, s. 1311-1322
  • Journal article (peer-reviewed)abstract
    • The feasibility to sequence entire genomes of virtually any organism provides unprecedented insights into the evolutionary history of populations and species. Nevertheless, many population genomic inferences - including the quantification and dating of admixture, introgression and demographic events, and inference of selective sweeps - are still limited by the lack of high-quality haplotype information. The newest generation of sequencing technology now promises significant progress. To establish the feasibility of haplotype-resolved genome resequencing at population scale, we investigated properties of linked-read sequencing data of songbirds of the genusOenantheacross a range of sequencing depths. Our results based on the comparison of downsampled (25x, 20x, 15x, 10x, 7x, and 5x) with high-coverage data (46-68x) of seven bird genomes mapped to a reference suggest that phasing contiguities and accuracies adequate for most population genomic analyses can be reached already with moderate sequencing effort. At 15x coverage, phased haplotypes span about 90% of the genome assembly, with 50% and 90% of phased sequences located in phase blocks longer than 1.25-4.6 Mb (N50) and 0.27-0.72 Mb (N90). Phasing accuracy reaches beyond 99% starting from 15x coverage. Higher coverages yielded higher contiguities (up to about 7 Mb/1 Mb [N50/N90] at 25x coverage), but only marginally improved phasing accuracy. Phase block contiguity improved with input DNA molecule length; thus, higher-quality DNA may help keeping sequencing costs at bay. In conclusion, even for organisms with gigabase-sized genomes like birds, linked-read sequencing at moderate depth opens an affordable avenue towards haplotype-resolved genome resequencing at population scale.
  •  
23.
  • Meunier, Joël, et al. (author)
  • Eumelanin-based coloration and fitness parameters in birds : a meta-analysis
  • 2011
  • In: Behavioral Ecology and Sociobiology. - : Springer Science and Business Media LLC. - 0340-5443 .- 1432-0762. ; 65:4, s. 559-567
  • Journal article (peer-reviewed)abstract
    • Although melanin is the most common pigment in animal integuments, the adaptive function of variation in melanin-based coloration remains poorly understood. The individual fitness returns associated with melanin pigments can be variable across species as these pigments can have physical and biological protective properties and genes involved in melanogenesis may vary in the intensity of pleiotropic effects. Moreover, dark and pale coloration can also enhance camouflage in alternative habitats and melanin-based coloration can be involved in social interactions. We investigated whether darker or paler individuals achieve a higher fitness in birds, a taxon wherein associations between melanin-based coloration and fitness parameters have been studied in a large number of species. A meta-analysis showed that the degree of melanin-based coloration was not significantly associated with laying date, clutch size, brood size, and survival across 26 species. Similar results were found when restricting the analyses to non-sexually dimorphic birds, colour polymorphic and monomorphic species, in passerines and non-passerines and in species for which inter-individual variation in melanism is due to colour intensity. However, eumelanic coloration was positively associated with clutch and brood size in sexually dimorphic species and those that vary in the size of black patches, respectively. Given that greater extent of melanin-based coloration was positively associated with reproductive parameters and survival in some species but negatively in other species, we conclude that in birds the sign and magnitude of selection exerted on melanin-based coloration is species- or trait-specific.
  •  
24.
  • Nadachowska-Brzyska, Krystyna, et al. (author)
  • Demographic Divergence History of Pied Flycatcher and Collared Flycatcher Inferred from Whole-Genome Re-sequencing Data
  • 2013
  • In: PLOS Genetics. - : Public Library of Science (PLoS). - 1553-7390 .- 1553-7404. ; 9:11, s. e1003942-
  • Journal article (peer-reviewed)abstract
    • Profound knowledge of demographic history is a prerequisite for the understanding and inference of processes involved in the evolution of population differentiation and speciation. Together with new coalescent-based methods, the recent availability of genome-wide data enables investigation of differentiation and divergence processes at unprecedented depth. We combined two powerful approaches, full Approximate Bayesian Computation analysis (ABC) and pairwise sequentially Markovian coalescent modeling (PSMC), to reconstruct the demographic history of the split between two avian speciation model species, the pied flycatcher and collared flycatcher. Using whole-genome re-sequencing data from 20 individuals, we investigated 15 demographic models including different levels and patterns of gene flow, and changes in effective population size over time. ABC provided high support for recent (mode 0.3 my, range <0.7 my) species divergence, declines in effective population size of both species since their initial divergence, and unidirectional recent gene flow from pied flycatcher into collared flycatcher. The estimated divergence time and population size changes, supported by PSMC results, suggest that the ancestral species persisted through one of the glacial periods of middle Pleistocene and then split into two large populations that first increased in size before going through severe bottlenecks and expanding into their current ranges. Secondary contact appears to have been established after the last glacial maximum. The severity of the bottlenecks at the last glacial maximum is indicated by the discrepancy between current effective population sizes (20,000–80,000) and census sizes (5–50 million birds) of the two species. The recent divergence time challenges the supposition that avian speciation is a relatively slow process with extended times for intrinsic postzygotic reproductive barriers to evolve. Our study emphasizes the importance of using genome-wide data to unravel tangled demographic histories. Moreover, it constitutes one of the first examples of the inference of divergence history from genome-wide data in non-model species.
  •  
25.
  • Nadachowska-Brzyska, Krystyna, et al. (author)
  • Footprints of adaptive evolution revealed by whole Z chromosomes haplotypes in flycatchers
  • 2019
  • In: Molecular Ecology. - : John Wiley & Sons. - 0962-1083 .- 1365-294X. ; 28:9, s. 2290-2304
  • Journal article (peer-reviewed)abstract
    • Detecting positive selection using genomic data is critical to understanding the role of adaptive evolution. Of particular interest in this context is sex chromosomes since they are thought to play a special role in local adaptation and speciation. We sought to circumvent the challenges associated with statistical phasing when using haplotype-based statistics in sweep scans by benefitting from that whole chromosome haplotypes of the sex chromosomes can be obtained by resequencing of individuals of the hemizygous sex. We analyzed whole Z chromosome haplotypes from 100 females from several populations of four black and white flycatcher species (in birds, females are ZW and males ZZ). Based on integrated haplotype score (iHS) and number of segregating sites by length (nSL) statistics, we found strong and frequent haplotype structure in several regions of the Z chromosome in each species. Most of these sweep signals were population-specific, with essentially no evidence for regions under selection shared among species. Some completed sweeps were revealed by the cross-population extended haplotype homozygosity (XP-EHH) statistic. Importantly, by using statistically phased Z chromosome data from resequencing of males, we failed to recover the signals of selection detected in analyses based on whole chromosome haplotypes from females; instead, what likely represent false signals of selection were frequently seen. This highlights the power issues in statistical phasing and cautions against conclusions from selection scans using such data. The detection of frequent selective sweeps on the avian Z chromosome supports a large role of sex chromosomes in adaptive evolution.
  •  
26.
  • Nadachowska-Brzyska, Krystyna, et al. (author)
  • PSMC analysis of effective population sizes in molecular ecology and its application to black-and-white Ficedula flycatchers
  • 2016
  • In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 25:5, s. 1058-1072
  • Research review (peer-reviewed)abstract
    • Climatic fluctuations during the Quaternary period governed the demography of species and contributed to population differentiation and ultimately speciation. Studies of these past processes have previously been hindered by a lack of means and genetic data to model changes in effective population size (N-e) through time. However, based on diploid genome sequences of high quality, the recently developed pairwise sequentially Markovian coalescent (PSMC) can estimate trajectories of changes in N-e over considerable time periods. We applied this approach to resequencing data from nearly 200 genomes of four species and several populations of the Ficedula species complex of black-and-white flycatchers. N-e curves of Atlas, collared, pied and semicollared flycatcher converged 1-2million years ago (Ma) at an N-e of approximate to 200000, likely reflecting the time when all four species last shared a common ancestor. Subsequent separate N-e trajectories are consistent with lineage splitting and speciation. All species showed evidence of population growth up until 100-200thousand years ago (kya), followed by decline and then start of a new phase of population expansion. However, timing and amplitude of changes in N-e differed among species, and for pied flycatcher, the temporal dynamics of N-e differed between Spanish birds and central/northern European populations. This cautions against extrapolation of demographic inference between lineages and calls for adequate sampling to provide representative pictures of the coalescence process in different species or populations. We also empirically evaluate criteria for proper inference of demographic histories using PSMC and arrive at recommendations of using sequencing data with a mean genome coverage of 18X, a per-site filter of 10 reads and no more than 25% of missing data.
  •  
27.
  • Nater, Alexander, et al. (author)
  • Resolving Evolutionary Relationships in Closely Related Species with Whole-Genome Sequencing Data
  • 2015
  • In: Systematic Biology. - : Oxford University Press (OUP). - 1063-5157 .- 1076-836X. ; 64:6, s. 1000-1017
  • Journal article (peer-reviewed)abstract
    • Using genetic data to resolve the evolutionary relationships of species is of major interest in evolutionary and systematic biology. However, reconstructing the sequence of speciation events, the so-called species tree, in closely related and potentially hybridizing species is very challenging. Processes such as incomplete lineage sorting and interspecific gene flow result in local gene genealogies that differ in their topology from the species tree, and analyses of few loci with a single sequence per species are likely to produce conflicting or even misleading results. To study these phenomena on a full phylogenomic scale, we use whole-genome sequence data from 200 individuals of four black-and-white flycatcher species with so far unresolved phylogenetic relationships to infer gene tree topologies and visualize genome-wide patterns of gene tree incongruence. Using phylogenetic analysis in nonoverlapping 10-kb windows, we show that gene tree topologies are extremely diverse and change on a very small physical scale. Moreover, we find strong evidence for gene flow among flycatcher species, with distinct patterns of reduced introgression on the Z chromosome. To resolve species relationships on the background of widespread gene tree incongruence, we used four complementary coalescent-based methods for species tree reconstruction, including complex modeling approaches that incorporate post-divergence gene flow among species. This allowed us to infer the most likely species tree with high confidence. Based on this finding, we show that regions of reduced effective population size, which have been suggested as particularly useful for species tree inference, can produce positively misleading species tree topologies. Our findings disclose the pitfalls of using loci potentially under selection as phylogenetic markers and highlight the potential of modeling approaches to disentangle species relationships in systems with large effective population sizes and post-divergence gene flow.
  •  
28.
  • O'Connor, Emily, et al. (author)
  • Avian MHC Evolution in the Era of Genomics : Phase 1.0
  • 2019
  • In: Cells. - : MDPI AG. - 2073-4409. ; 8:10
  • Journal article (peer-reviewed)abstract
    • Birds are a wonderfully diverse and accessible clade with an exceptional range of ecologies and behaviors, making the study of the avian major histocompatibility complex (MHC) of great interest. In the last 20 years, particularly with the advent of high-throughput sequencing, the avian MHC has been explored in great depth in several dimensions: its ability to explain ecological patterns in nature, such as mating preferences; its correlation with parasite resistance; and its structural evolution across the avian tree of life. Here, we review the latest pulse of avian MHC studies spurred by high-throughput sequencing. Despite high-throughput approaches to MHC studies, substantial areas remain in need of improvement with regard to our understanding of MHC structure, diversity, and evolution. Recent studies of the avian MHC have nonetheless revealed intriguing connections between MHC structure and life history traits, and highlight the advantages of long-term ecological studies for understanding the patterns of MHC variation in the wild. Given the exceptional diversity of birds, their accessibility, and the ease of sequencing their genomes, studies of avian MHC promise to improve our understanding of the many dimensions and consequences of MHC variation in nature. However, significant improvements in assembling complete MHC regions with long-read sequencing will be required for truly transformative studies.
  •  
29.
  • Peona, Valentina, et al. (author)
  • An annotated chromosome-scale reference genome for Eastern black-eared wheatear (Oenanthe melanoleuca)
  • 2023
  • In: G3. - : Oxford University Press. - 2160-1836. ; 13:6
  • Journal article (peer-reviewed)abstract
    • Pervasive convergent evolution and in part high incidences of hybridization distinguish wheatears (songbirds of the genus Oenanthe) as a versatile system to address questions at the forefront of research on the molecular bases of phenotypic and species diversification. To prepare the genomic resources for this venture, we here generated and annotated a chromosome-scale assembly of the Eastern black-eared wheatear (Oenanthe melanoleuca). This species is part of the Oenanthe hispanica complex that is characterized by convergent evolution of plumage coloration and high rates of hybridization. The long-read-based male nuclear genome assembly comprises 1.04 Gb in 32 autosomes, the Z chromosome, and the mitogenome. The assembly is highly contiguous (contig N50, 12.6 Mb; scaffold N50, 70 Mb), with 96% of the genome assembled at the chromosome level and 95.5% benchmarking universal single-copy orthologs (BUSCO) completeness. The nuclear genome was annotated with 18,143 protein-coding genes and 31,333 mRNAs (annotation BUSCO completeness, 98.0%), and about 10% of the genome consists of repetitive DNA. The annotated chromosome-scale reference genome of Eastern black-eared wheatear provides a crucial resource for research into the genomics of adaptation and speciation in an intriguing group of passerines.
  •  
30.
  •  
31.
  • Peona, Valentina, et al. (author)
  • Identifying the causes and consequences of assembly gaps using a multiplatform genome assembly of a bird‐of‐paradise
  • 2020
  • In: Molecular Ecology Resources. - : Wiley. - 1755-098X .- 1755-0998. ; 21:1, s. 263-286
  • Journal article (peer-reviewed)abstract
    • Genome assemblies are currently being produced at an impressive rate by consortia and individual laboratories. The low costs and increasing efficiency of sequencing technologies now enable assembling genomes at unprecedented quality and contiguity. However, the difficulty in assembling repeat-rich and GC-rich regions (genomic “dark matter”) limits insights into the evolution of genome structure and regulatory networks. Here, we compare the efficiency of currently available sequencing technologies (short/linked/long reads and proximity ligation maps) and combinations thereof in assembling genomic dark matter. By adopting different de novo assembly strategies, we compare individual draft assemblies to a curated multiplatform reference assembly and identify the genomic features that cause gaps within each assembly. We show that a multiplatform assembly implementing long-read, linked-read and proximity sequencing technologies performs best at recovering transposable elements, multicopy MHC genes, GC-rich microchromosomes and the repeat-rich W chromosome. Telomere-to-telomere assemblies are not a reality yet for most organisms, but by leveraging technology choice it is now possible to minimize genome assembly gaps for downstream analysis. We provide a roadmap to tailor sequencing projects for optimized completeness of both the coding and noncoding parts of nonmodel genomes.
  •  
32.
  • Promerová, Marta, et al. (author)
  • No evidence for MHC class II-based non-random mating at the gametic haplotype in Atlantic salmon
  • 2017
  • In: Heredity. - : Springer Science and Business Media LLC. - 0018-067X .- 1365-2540. ; 118:6, s. 563-567
  • Journal article (peer-reviewed)abstract
    • Genes of the major histocompatibility complex (MHC) are a likely target of mate choice because of their role in inbreeding avoidance and potential benefits for offspring immunocompetence. Evidence for female choice for complementary MHC alleles among competing males exists both for the pre- and the postmating stages. However, it remains unclear whether the latter may involve non-random fusion of gametes depending on gametic haplotypes resulting in transmission ratio distortion or non-random sequence divergence among fused gametes. We tested whether non-random gametic fusion of MHC-II haplotypes occurs in Atlantic salmon Salmo salar. We performed in vitro fertilizations that excluded interindividual sperm competition using a split family design with large clutch sample sizes to test for a possible role of the gametic haplotype in mate choice. We sequenced two MHC-II loci in 50 embryos per clutch to assess allelic frequencies and sequence divergence. We found no evidence for transmission ratio distortion at two linked MHC-II loci, nor for non-random gamete fusion with respect to MHC-II alleles. Our findings suggest that the gametic MHC-II haplotypes play no role in gamete association in Atlantic salmon and that earlier findings of MHC-based mate choice most likely reflect choice among diploid genotypes. We discuss possible explanations for these findings and how they differ from findings in mammals.
  •  
33.
  • Roulin, Alexandre, et al. (author)
  • Owl melanin-based plumage redness is more frequent near than away from the equator : implications on the effect of climate change on biodiversity
  • 2011
  • In: Biological Journal of the Linnean Society. - : Oxford University Press (OUP). - 0024-4066 .- 1095-8312. ; 102:3, s. 573-582
  • Journal article (peer-reviewed)abstract
    • Climate change acts as a major new selective agent on many organisms, particularly at high latitudes where climate change is more pronounced than at lower latitudes. Studies are required to predict which species are at a high risk of extinction and whether certain phenotypes may be more affected by climate change than others. The identification of susceptible phenotypes is important for evaluating the potential negative effect of climate change on biodiversity at the inter- and intraspecific levels. Melanin-based coloration is an interesting and easily accessible candidate trait because, within certain species, reddish pheomelanin-based coloration is associated with adaptations to warm climates. However, it is unclear whether the same holds among species. We tested one prediction of this hypothesis in four owl genera (wood, scops, screech, and pygmy owls), namely that darker reddish species are more prevalent near the equator than polewards. Our comparative analysis is consistent with this prediction for the northern hemisphere, suggesting that pale reddish species may be adapted to cold climates and dark reddish species to warmer climates. Thus, climate change may have a larger negative impact on pale pheomelanic owls and favour dark pheomelanic species.
  •  
34.
  • Roulin, Alexandre, et al. (author)
  • Spatial variation in the temporal change of male and female melanic ornamentation in the barn owl
  • 2011
  • In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 24:7, s. 1403-14099
  • Journal article (peer-reviewed)abstract
    • Because the magnitude of selection can vary between sexes and in space and time, sexually antagonistic selection is difficult to demonstrate. In a Swiss population of barn owls (Tyto alba), a heritable eumelanic colour trait (size of black spots on ventral feathers) was positively selected with respect to yearling survival only in females. It remains unclear whether the absence of negative selection in males is typical in this species. To tackle this issue indirectly, we measured the size of black spots in 1733 skin specimens collected by museums from 1816 to 2001 in seven European countries and in the Middle-East. The temporal change in spot size was sex- and country-specific. In males, spots became smaller particularly in three countries (Middle-East, Italy and Switzerland). In females, the size of spots increased significantly in two countries (UK and Spain) and decreased in two others (Germany and Switzerland). Because migration and phenotypic plasticity cannot explain these results, selection is the most likely cause. The weaker temporal change in spot size in females than males may be because of the combined effect of strong genetic correlation between the sexes and stronger negative selection in males than positive selection in females. We thus suggest that in the barn owl, spot size (or genetically correlated traits) is sexually antagonistically selected and that its pattern of selection may account for the maintenance of its variation and sexual dimorphism.
  •  
35.
  • Schweizer, Manuel, et al. (author)
  • Genome-wide evidence supports mitochondrial relationships and pervasive parallel phenotypic evolution in open-habitat chats
  • 2019
  • In: Molecular Phylogenetics and Evolution. - : Elsevier BV. - 1055-7903 .- 1095-9513. ; 139
  • Journal article (peer-reviewed)abstract
    • In wheatears and related species ('open-habitat chats'), molecular phylogenetics has led to a comprehensively revised understanding of species relationships and species diversity. Phylogenetic analyses have suggested that, in many cases, phenotypic similarities do not reflect species' relationships, revealing traditionally defined genera as non-monophyletic. This led to the suggestion of pervasive parallel evolution of open-habitat chats' plumage coloration and ecological phenotypes. However, to date, the molecular evidence for the phylogenetic relationships among open-habitat chats is mainly limited to mitochondrial DNA. Here, we assessed whether the mitochondrial relationships are supported by genome-wide data. To this end, we reconstructed the species tree among 14 open-habitat chat taxa using multi-species coalescent analyses based on similar to 1'300 SNPs. Our results confirm previous ones based chiefly on mitochondrial DNA; notably the paraphyly of the Oenanthe lugens complex and the clustering of individual species formerly placed in the genera Cercomela and Myrmecocichla within Oenanthe. Since several variable morphological and ecological characteristics occur in multiple places across the open-habitat chat phylogeny, our study consolidates the evidence for pervasive parallel evolution in the plumage coloration and ecology of open-habitat chats.
  •  
36.
  • Schweizer, Manuel, et al. (author)
  • Parallel plumage colour evolution and introgressive hybridization in wheatears
  • 2019
  • In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 32:1, s. 100-110
  • Journal article (peer-reviewed)abstract
    • Genetic and phenotypic mosaics, in which various phenotypes and different genomic regions show discordant patterns of species or population divergence, offer unique opportunities to study the role of ancestral and introgressed genetic variation in phenotypic evolution. Here, we investigated the evolution of discordant phenotypic and genetic divergence in a monophyletic clade of four songbird taxa-pied wheatear (O. pleschanka), Cyprus wheatear (Oenanthe cypriaca), and western and eastern subspecies of black-eared wheatear (O. h. hispanica and O. h. melanoleuca). Phenotypically, black back and neck sides distinguish pied and Cyprus wheatears from the white-backed/necked black-eared wheatears. Meanwhile, mitochondrial variation only distinguishes western black-eared wheatear. In the absence of nuclear genetic data, and given frequent hybridization among eastern black-eared and pied wheatear, it remains unclear whether introgression is responsible for discordance between mitochondrial divergence patterns and phenotypic similarities, or whether plumage coloration evolved in parallel. Multispecies coalescent analyses of about 20,000 SNPs obtained from RAD data mapped to a draft genome assembly resolve the species tree, provide evidence for the parallel evolution of colour phenotypes and establish western and eastern black-eared wheatears as independent taxa that should be recognized as full species. The presence of the entire admixture spectrum in the Iranian hybrid zone and the detection of footprints of introgression from pied into eastern black-eared wheatear beyond the hybrid zone despite strong geographic structure of ancestry proportions furthermore suggest a potential role for introgression in parallel plumage colour evolution. Our results support the importance of standing heterospecific and/or ancestral variation in phenotypic evolution.
  •  
37.
  • Smeds, Linnea, et al. (author)
  • Evolutionary analysis of the female-specific avian W chromosome
  • 2015
  • In: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 6
  • Journal article (peer-reviewed)abstract
    • The typically repetitive nature of the sex-limited chromosome means that it is often excluded from or poorly covered in genome assemblies, hindering studies of evolutionary and population genomic processes in non-recombining chromosomes. Here, we present a draft assembly of the non-recombining region of the collared flycatcher W chromosome, containing 46 genes without evidence of female-specific functional differentiation. Survival of genes during W chromosome degeneration has been highly non-random and expression data suggest that this can be attributed to selection for maintaining gene dose and ancestral expression levels of essential genes. Re-sequencing of large population samples revealed dramatically reduced levels of within-species diversity and elevated rates of between-species differentiation (lineage sorting), consistent with low effective population size. Concordance between W chromosome and mitochondrial DNA phylogenetic trees demonstrates evolutionary stable matrilineal inheritance of this nuclear-cytonuclear pair of chromosomes. Our results show both commonalities and differences between W chromosome and Y chromosome evolution.
  •  
38.
  • Smeds, Linnea, et al. (author)
  • Genomic identification and characterization of the pseudoautosomal region in highly differentiated avian sex chromosomes
  • 2014
  • In: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 5, s. 5448-
  • Journal article (peer-reviewed)abstract
    • The molecular characteristics of the pseudoautosomal region (PAR) of sex chromosomes remain elusive. Despite significant genome-sequencing efforts, the PAR of highly differentiated avian sex chromosomes remains to be identified. Here we use linkage analysis together with whole-genome re-sequencing to uncover the 630-kb PAR of an ecological model species, the collared flycatcher. The PAR contains 22 protein-coding genes and is GC rich. The genetic length is 64cM in female meiosis, consistent with an obligate crossing-over event. Recombination is concentrated to a hotspot region, with an extreme rate of > 700 cM/Mb in a 67-kb segment. We find no signatures of sexual antagonism and propose that sexual antagonism may have limited influence on PAR sequences when sex chromosomes are nearly fully differentiated and when a recombination hotspot region is located close to the PAR boundary. Our results demonstrate that a very small PAR suffices to ensure homologous recombination and proper segregation of sex chromosomes during meiosis.
  •  
39.
  • Tang, Qindong, et al. (author)
  • Seasonal migration patterns and the maintenance of evolutionary diversity in a cryptic bird radiation
  • 2022
  • In: Molecular Ecology. - : John Wiley & Sons. - 0962-1083 .- 1365-294X. ; 31:2, s. 632-645
  • Journal article (peer-reviewed)abstract
    • Morphological differentiation associated with evolutionary diversification is often explained with adaptive benefits but the processes and mechanisms maintaining cryptic diversity are still poorly understood. Using genome-wide data, we show here that the pale sand martin Riparia diluta in Central and East Asia consists of three genetically deeply differentiated lineages which vary only gradually in morphology but broadly reflect traditional taxonomy. We detected no signs of gene flow along the eastern edge of the Qinghai-Tibetan plateau between lowland south-eastern Chinese R. d. fohkienensis and high-altitude R. d. tibetana. Largely different breeding and migration timing between these low and high altitude populations as indicated by phenology data suggests that allochrony might act as prezygotic isolation mechanism in the area where their ranges abut. Mongolian populations of R. d. tibetana, however, displayed signs of limited mixed ancestries with Central Asian R. d. diluta. Their ranges meet in the area of a well-known avian migratory divide, where western lineages take a western migration route around the Qinghai-Tibetan plateau to winter quarters in South Asia, and eastern lineages take an eastern route to Southeast Asia. This might also be the case between western R. d. diluta and eastern R. d. tibetana as indicated by differing wintering grounds. We hypothesize that hybrids might have nonoptimal intermediate migration routes and selection against them might restrict gene flow. Although further potential isolation mechanisms might exist in the pale sand martin, our study points towards contrasting migration behaviour as an important factor in maintaining evolutionary diversity under morphological stasis.
  •  
40.
  • Uebbing, Severin, et al. (author)
  • Divergence in gene expression within and between two closely related flycatcher species
  • Other publication (other academic/artistic)abstract
    • Compared to DNA sequence evolution, relatively little is known about the character of gene expression evolution as species diverge. For example, it is unclear if gene expression generally evolves in a clock-like manner (by stabilizing selection or from neutral evolution) or if there are frequent episodes of directional selection. To gain insights into the evolutionary divergence of gene expression patterns, we sequenced and compared the transcriptomes of multiple tissues from population samples of collared (Ficedula albicollis) and pied flycatchers (F. hypoleuca), a species pair which diverged less than one million years ago. Tissues resolved into separate clusters in non-metric multidimensional scaling ordination analysis and samples from the two species generally clustered by tissue rather than by species. Tissues differed in the degrees of expression variance within species and divergence between species. Variance was positively correlated with expression breadth and negatively correlated with protein interactivity, suggesting that pleiotropic constraints reduce gene expression variance within species. Variance was correlated with between-species divergence, consistent with a pattern expected from stabilizing selection and neutral evolution. Using an expression QST approach, we identified genes differentially expressed between species. We also identified 10 genes uniquely expressed in one of the species. For one such gene (DPP7, uniquely expressed in collared flycatcher), the absence of expression in pied flycatchers could be associated with a fixed ≈ 20 kb deletion including 11 out of 13 exons in this species. This study conducted in a young vertebrate speciation model system expands our knowledge of how gene expression evolves in natural populations.
  •  
41.
  • Uebbing, Severin, et al. (author)
  • Divergence in gene expression within and between two closely related flycatcher species
  • 2016
  • In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 25:9, s. 2015-2028
  • Journal article (peer-reviewed)abstract
    • Relatively little is known about the character of gene expression evolution as species diverge. It is for instance unclear if gene expression generally evolves in a clock-like manner (by stabilizing selection or neutral evolution) or if there are frequent episodes of directional selection. To gain insights into the evolutionary divergence of gene expression, we sequenced and compared the transcriptomes of multiple organs from population samples of collared (Ficedula albicollis) and pied flycatchers (F. hypoleuca), two species which diverged less than one million years ago. Ordination analysis separated samples by organ rather than by species. Organs differed in their degrees of expression variance within species and expression divergence between species. Variance was negatively correlated with expression breadth and protein interactivity, suggesting that pleiotropic constraints reduce gene expression variance within species. Variance was correlated with between-species divergence, consistent with a pattern expected from stabilizing selection and neutral evolution. Using an expression PST approach, we identified genes differentially expressed between species and found 16 genes uniquely expressed in one of the species. For one of these, DPP7, uniquely expressed in collared flycatcher, the absence of expression in pied flycatcher could be associated with a ≈ 20 kb deletion including 11 out of 13 exons. This study of a young vertebrate speciation model system expands our knowledge of how gene expression evolves as natural populations become reproductively isolated.
  •  
42.
  • Vijay, Nagarjun, et al. (author)
  • Genomewide patterns of variation in genetic diversity are shared among populations, species and higher-order taxa
  • 2017
  • In: Molecular Ecology. - : WILEY. - 0962-1083 .- 1365-294X. ; 26:16, s. 4284-4295
  • Journal article (peer-reviewed)abstract
    • Genomewide screens of genetic variation within and between populations can reveal signatures of selection implicated in adaptation and speciation. Genomic regions with low genetic diversity and elevated differentiation reflective of locally reduced effective population sizes (N-e) are candidates for barrier loci contributing to population divergence. Yet, such candidate genomic regions need not arise as a result of selection promoting adaptation or advancing reproductive isolation. Linked selection unrelated to lineage-specific adaptation or population divergence can generate comparable signatures. It is challenging to distinguish between these processes, particularly when diverging populations share ancestral genetic variation. In this study, we took a comparative approach using population assemblages from distant clades assessing genomic parallelism of variation in N-e. Utilizing population-level polymorphism data from 444 resequenced genomes of three avian clades spanning 50 million years of evolution, we tested whether population genetic summary statistics reflecting genomewide variation in N-e would covary among populations within clades, and importantly, also among clades where lineage sorting has been completed. All statistics including population-scaled recombination rate (rho), nucleotide diversity (pi) and measures of genetic differentiation between populations (F-ST, PBS, d(xy)) were significantly correlated across all phylogenetic distances. Moreover, genomic regions with elevated levels of genetic differentiation were associated with inferred pericentromeric and subtelomeric regions. The phylogenetic stability of diversity landscapes and stable association with genomic features support a role of linked selection not necessarily associated with adaptation and speciation in shaping patterns of genomewide heterogeneity in genetic diversity.
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43.
  • Yannic, Glenn, et al. (author)
  • Systematics of snow voles (Chionomys, Arvicolinae) revisited
  • 2012
  • In: Molecular Phylogenetics and Evolution. - : Elsevier BV. - 1055-7903 .- 1095-9513. ; 62:3, s. 806-815
  • Journal article (peer-reviewed)abstract
    • To elucidate the evolutionary history of snow voles, genus Chionomys, we studied the phylogeography of Chionomys nivalis across its range and investigated its relationships with two congeneric species, Chionomys gud and Chionomys roberti, using independent molecular markers. Analyses were based on mitochondrial (similar to 940 bp cyt b) and Y-chromosomal (similar to 2020 bp from three introns) genetic variation. Our data provide conclusive evidence for a Caucasian and Middle Eastern origin for the three species and a subsequent westward expansion of C. nivalis. In addition, we discuss the taxonomic status of the genus Chionomys in relation to the genus Microtus.
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