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

RJ. Safran, ES. Scordato, MR. Wilkins, JK. Hubbard, BR. Jenkins, T. Albrecht, SM. Flaxman, H. Karaardıç, Y. Vortman, A. Lotem, P. Nosil, P. Pap, S. Shen, SF. Chan, TL. Parchman, NC. Kane,

. 2016 ; 25 (16) : 3865-83. [pub] 20160729

Language English Country Great Britain

Document type Journal Article

Persistent link   https://www.medvik.cz/link/bmc18017182

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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$a Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as 'isolation by adaptation' (IBA). IBA can be complementary to the well-known pattern of 'isolation by distance' (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome-wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole-genome sequence for H. rustica, to which we aligned a set of 9493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behaviour and sexual signalling, as well as geographic distance, together explain over 70% of genome-wide divergence among populations. Controlling for IBD, we find 42% of genomewide divergence is attributable to IBA through pairwise differences in traits related to migratory behaviour and sexual signalling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population-level differentiation in this group of closely related populations.
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$a Scordato, E S C $u Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.
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$a Wilkins, M R $u Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA. School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, USA.
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$a Hubbard, J K $u Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA. School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, USA.
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$a Jenkins, B R $u Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.
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$a Albrecht, T $u Department of Zoology, Charles University in Prague and Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Prague, Czech Republic.
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$a Flaxman, S M $u Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.
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$a Karaardıç, H $u Elementary Science Education Department, Education Faculty, Alanya Alaaddin Keykubat University, Alanya, Turkey.
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$a Vortman, Y $u Department of Zoology, Tel-Aviv University, Tel-Aviv, Israel. Hula Research Center, Department of Animal Sciences, Tel-Hai College, Israel.
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$a Lotem, A $u Department of Zoology, Tel-Aviv University, Tel-Aviv, Israel.
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$a Nosil, P $u Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK.
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$a Pap, P $u Department of Taxonomy and Ecology, Babeş-Bolyai University, Cluj-Napoca, Romania.
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$a Shen, S $u Biodiversity Research Center, Academia Sinica, Taipei, Taiwan.
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$a Chan, S-F $u Biodiversity Research Center, Academia Sinica, Taipei, Taiwan.
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$a Parchman, T L $u Department of Biology, University of Nevada, Reno, NV, USA.
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$a Kane, N C $u Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.
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