Genome-wide differentiation in closely related populations: the roles of selection and geographic isolation.

Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as 'Isolation by Adaptation' (IBA). IBA can be complementary to the well-known pattern of 'Isolation by Distance' (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome-wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole genome sequence for H. rustica, to which we aligned a set of 9,493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behavior and sexual signaling, as well as geographic distance together, explain over 70% of genome-wide divergence among populations. Controlling for IBD, we find 42% of genome-wide divergence is attributable to IBA through pairwise differences in traits related to migratory behavior and sexual signaling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population-level differentiation in this group of closely related populations. This article is protected by copyright. All rights reserved

Data from: Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography

1. Patterns of diversity and turnover in macroorganism communities can often be predicted from differences in habitat, phylogenetic relationships among species, and the geographic scale of comparisons. In this study, we asked if these factors also predict diversity and turnover in parasite communities. 2. We studied communities of avian malaria in two sympatric, ecologically similar, congeneric host species at three different sites. We asked if parasite prevalence and community structure varied with host population, host phylogeography, or geographic distance. 3. We used PCR to screen birds for infections, and then used Bayesian methods to determine phylogenetic relationships among malaria strains. Metrics of both community and phylogenetic beta diversity were used to examine patterns of malaria strain turnover between host populations, and partial Mantel tests were used determine the correlation between malaria beta diversity and geographic distance. Finally, we developed microsatellite markers to describe the genetic structure of host populations and assess the relationship between host phylogeography and parasite beta diversity. 4. We found that although some malaria lineages occur in both host species, different genera of malaria parasites infect the two hosts at different rates. Additionally, host species was a better predictor of parasite community similarity than study site. Within hosts, parasite communities in one population were phylogenetically clustered, but there was otherwise no correlation between metrics of parasite beta diversity and geographic or genetic distance between host populations. Patterns of parasite turnover among host populations are consistent with malaria transmission occurring in the winter rather than on the breeding grounds 5. Our results indicate greater turnover in parasite communities between different hosts than between different sites. Differences in host species, as well as transmission location and vector ecology, seem to be more important in structuring malaria communities than the distance-decay relationships frequently found in macroorganisms. Determining the factors affecting parasite community diversity and turnover has wide-ranging implications for understanding the selective pressures shaping host ecology and ecosystem structure. This study shows that metrics of community and phylogenetic beta diversity can be useful tools for disentangling the ecological and evolutionary processes that underlie geographical variation in parasite communities

Data from: Genomic variation across two barn swallow hybrid zones reveals traits associated with divergence in sympatry and allopatry

Hybrid zones are geographic regions where isolating barriers between divergent populations are challenged by admixture. Identifying factors that facilitate or inhibit hybridization in sympatry can illuminate the processes that maintain those reproductive barriers. We analyzed patterns of hybridization and phenotypic variation across two newly-discovered hybrid zones between three subspecies of barn swallow (Hirundo rustica). These subspecies differ in ventral coloration and wing length, traits that are targets of sexual and natural selection, respectively, and are associated with genome-wide differentiation in allopatry. We tested the hypothesis that the degree of divergence in these traits is associated with the extent of hybridization in secondary contact. We applied measures of population structure based on > 23,000 SNPs to confirm that named subspecies correspond to distinct genomic clusters, and assessed coincidence between geographic clines for ancestry and phenotype. Although gene flow was ongoing across both hybrid zones and pairwise FST between subspecies was extremely low, we found striking differences in the extent of hybridization. In the more phenotypically differentiated subspecies pair, clines for ancestry, wing length, and ventral coloration were steep and coincident, suggestive of strong isolation and, potentially, selection associated with phenotype. In the less phenotypically differentiated pair, gene flow and phenotypic variation occured over a wide geographic span, indicative of weaker isolation. Traits associated with genome-wide differentiation in allopatry may thus also contribute to isolation in sympatry. We discuss potentially important additional roles for evolutionary history and ecology in shaping variation in the extent hybridization between closely related pairs of subspecies

Data from: Effects of assortative mate choice on the genomic and morphological structure of a hybrid zone between two bird subspecies

Phenotypic differentiation plays an important role in the formation and maintenance of reproductive barriers. In some cases, variation in a few key aspects of phenotype can promote and maintain divergence; hence the identification of these traits and their associations with patterns of genomic divergence are crucial for understanding the patterns and processes of population differentiation. We studied hybridization between the alba and personata subspecies of the white wagtail (Motacilla alba), and quantified divergence and introgression of multiple morphological traits and 19,437 SNP loci on a 3000 km transect. Our goal was to identify traits that may contribute to reproductive barriers and to assess how variation in these traits corresponds to patterns of genome-wide divergence. Variation in only one trait – head plumage patterning – was consistent with reproductive isolation. Transitions in head plumage were steep and occurred over otherwise morphologically and genetically homogeneous populations, whereas cline centers for other traits and genomic ancestry were displaced over one hundred kilometers from the head cline. Field observational data show that social pairs mated assortatively by head plumage, suggesting that these phenotypes are maintained by divergent mating preferences. In contrast, variation in all other traits and genetic markers could be explained by neutral diffusion, although weak ecological selection cannot be ruled out. Our results emphasize that assortative mating may maintain phenotypic differences independent of other processes shaping genome-wide variation, consistent with other recent findings that raise questions about the relative importance of mate choice, ecological selection and selectively neutral processes for divergent evolution

Data from: Genomic divergence in a ring species complex

Ring species provide particularly clear demonstrations of how one species can gradually evolve into two, but are rare in nature. In the greenish warbler (Phylloscopus trochiloides) species complex, a ring of populations wraps around Tibet. Two reproductively isolated forms co-exist in central Siberia, with a gradient of genetic and phenotypic characteristics through the southern chain of populations connecting them. Previous genetic evidence has proven inconclusive, however, regarding whether species divergence took place in the face of continuous gene flow and whether hybridization between the terminal forms of the ring ever occurred. Here we use genome-wide analyses to show that, although spatial patterns of genetic variation are currently mostly as expected of a ring species, historical breaks in gene flow have existed at more than one location around the ring, and the two Siberian forms have occasionally interbred. Substantial periods of geographical isolation occurred not only in the north but also in the western Himalayas, where there is now an extensive hybrid zone between genetically divergent forms. Limited asymmetric introgression has occurred directly between the Siberian forms, although it has not caused a blending of those forms, suggesting selection against introgressed genes in the novel genetic background. Levels of reproductive isolation and genetic introgression are consistent with levels of phenotypic divergence around the ring, with phenotypic similarity and extensive interbreeding across the southwestern contact zone and strong phenotypic divergence and nearly complete reproductive isolation across the northern contact zone. These results cast doubt on the hypothesis that the greenish warbler should be viewed as a rare example of speciation by distance, but demonstrate that the greenish warbler displays a continuum from slightly divergent neighbouring populations to almost fully reproductively isolated species

Greenish Warbler De Novo Assembly Draft

De Novo Assembly of a whole-genome sequencing library from one Phylloscopus trochiloides viridanus bird (SRA accession number: SRX473141). De Novo Assembly was carried out in the CLC genomic workbench and following the default parameters set by the developer

Greenish warbler sequences and SNPs mapped on zebra finch genome

Greenish warbler sequences mapped on zebra finch genome assembly (pink annotations). The physical location of SNP markers is also indicated. Grey annotations refer to the set of 81,034 SNPs with data in at least 80% of individuals (N=95 birds). Yellow annotations refer to the subset of 2,334 SNPs with no missing data and minimum coverage = 3 reads. Blue annotations refer to the 1,827 SNP markers used during the chromosome-by-chromosome introgression analysis. These assemblies can be inspected in the free version of the Geneious genomic workbench, which can be downloaded from http://www.geneious.com/download

The impact of urbanization on body size of Barn Swallows Hirundo rustica gutturalis

Abstract Urbanization implies a dramatic impact on ecosystems, which may lead to drastic phenotypic differences between urban and nonurban individuals. For instance, urbanization is associated with increased metabolic costs, which may constrain body size, but urbanization also leads to habitat fragmentation, which may favor increases in body mass when for instance it correlates with dispersal capacity. However, this apparent contradiction has rarely been studied. This is particularly evident in China where the urbanization process is currently occurring at an unprecedented scale. Moreover, no study has addressed this issue across large geographical areas encompassing locations in different climates. In this regard, Barn Swallows (Hirundo rustica) are a suitable model to study the impact of urbanization on wild animals because they are a widely distributed species tightly associated with humans. Here, we collected body mass and wing length data for 359 breeding individuals of Barn Swallow (H. r. gutturalis) from 128 sites showing different levels of urbanization around the whole China. Using a set of linear mixed‐effects models, we assessed how urbanization and geography influenced body size measured using body mass, wing length, and their regression residuals. Interestingly, we found that the impact of urbanization was sex‐dependent, negatively affecting males’ body mass, its regression residuals, and females’ wing length. We also found that northern and western individuals were larger, regarding both body mass and wing length, than southern and eastern individuals. Females were heavier than males, yet males had slightly longer wings than females. Overall, our results showed that body mass of males was particularly sensitive trait to urbanization, latitude, and longitude, while it only showed a weak response to latitude in females. Conversely, while wing length showed a similar geographical pattern, it was only affected by urbanization in the case of females. Further research is needed to determine whether these phenotypic differences are associated with negative effects of urbanization or potential selective advantages

On the Role of Male Competition in Speciation: A Review and Research Agenda

Support for the role of sexual selection in speciation has grown over the last 30 years. Work in this area, however, has largely focused on a single dominant question: when and how do divergent male sexual signals and corresponding female preferences lead to reproductive isolation? The field has not given adequate attention to the role that male competition, Darwin’s second mechanism of sexual selection, might also play in speciation. In this review, we summarize recent work that shows precopulatory male competition can initiate speciation in sympatry, drive divergence of competitive phenotypes in allopatry, and strengthen reproductive barriers between competitive types during secondary contact. The manner by which male competition contributes to divergence in allopatry is a poorly understood yet compelling area of research; similar to female choice, male competition may be more likely to lead to speciation when working in concert with divergent ecology, and allopatry sets the stage for divergence among environments with reduced gene flow. To encourage future research in this area, we place potential mechanisms for speciation by male competition into existing speciation frameworks and propose a theoretical and empirical research agenda to reveal how male competition contributes to the accumulation of reproductive isolation. Our current understanding of when and how divergence in competitive phenotypes leads to reproductive isolation is limited, and theoretical work may be particularly well-suited to reveal when divergence by male competition is fastest and most likely