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    Genome-wide differentiation in closely related populations: the roles of selection and geographic isolation
    (Wiley, 2016) Safran, Rebecca J.; Scordato, Elizabeth S. C.; Wilkins, Matthew R.; Hubbard, Joanna K.; Jenkins, Brittany R.; Albrecht, Tomas; Karaardıç, Hakan; Vortman,Yoni; Arnon, Lotem; Pap, Peter L.; Shen, Sheng-Feng; Chan, Shih-Fan; Parchman, Thomas L.; Kane, Nolan C.; Nosil, Patrik
    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 9493 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 behaviour and sexual signalling, as well as geographic distance, together explain over 70% of genome-wide divergence among populations. Controlling for IBD, we find 42% of genomewide divergence is attributable to IBA through pairwise differences in traits related to migratory behaviour and sexual signalling 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.
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    Global song divergence in barn swallows (Hirundo rustica): exploring the roles of genetic, geographical and climatic distance in sympatry and allopatry
    (Oxford Univ Press, 2018) Wilkins, Matthew R.; Scordato, Elizabeth S. C.; Semenov, Georgy A.; Karaardıç, Hakan; Shizuka, Daizaburo; Rubtsov, Alexander; Safran, Rebecca J.
    Divergence in acoustic signals plays an important role in the production and maintenance of biodiversity in numerous taxa. In this study, we assess patterns of acoustic divergence in geographically isolated and sympatric subspecies of barn swallows (Hirundo rustica), including analyses of whether song differentiation varies with geographical isolation, genetic distance and climatic distance. We provide the first description of geographical variation in song among five of six currently recognized barn swallow subspecies. Temporal traits describing terminal trills were the most distinct song traits among subspecies, adding to growing evidence that trills are important in speciation among many birds, insects and fish. Across a similar to 6000 km transect of Russia, acoustic distance was predicted by genetic and geographical distance, but not climatic distance. We also found no reproductive character displacement of song traits in a contact zone between H. r. rustica and H. r. tytleri. Based on patterns discovered in this study, we infer an important role of sexual selection, genetic and/or cultural drift in the gradual build-up of acoustic divergence, which is accelerated in small populations.
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    Phenotypic differentiation is associated with divergent sexual selection among closely related barn swallow populations
    (Wiley-Blackwell, 2016) Wilkins, Matthew R.; Karaardıç, Hakan; Vortman, Yoni; Parchman, Thomas L.; Albrecht, Tomas; Petrzelkova, Adela; Safran, Rebecca J.
    Sexual selection plays a key role in the diversification of numerous animal clades and may accelerate trait divergence during speciation. However, much of our understanding of this process comes from phylogenetic comparative studies, which rely on surrogate measures such as dimorphism that may not represent selection in wild populations. In this study, we assess sexual selection pressures for multiple male visual signals across four barn swallow (Hirundo rustica) populations. Our sample encompassed 2400 linear km and two described subspecies: European H. r. rustica (in the Czech Republic and Romania) and eastern Mediterranean H. r. transitiva (in Israel), as well as a potential area of contact (in Turkey). We demonstrate significant phenotypic differentiation in four sexual signalling axes, despite very low-level genomic divergence and no comparable divergence in an ecological trait. Moreover, the direction of phenotypic divergence is consistent with differences in sexual selection pressures among subspecies. Thus, H. r. transitiva, which have the darkest ventral plumage of any population, experience directional selection for darker plumage. Similarly, H. r. rustica, which have the longest tail feathers of any population, experience directional selection for elongated tail feathers and disruptive selection for ventral plumage saturation. These results suggest that sexual selection is the primary driver of phenotypic differentiation in this species. Our findings add to growing evidence of phenotypic divergence with gene flow. However, to our knowledge, this is the first study to relate direct measures of the strength and targets of sexual selection to phenotypic divergence among closely related wild populations.