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Insight into the roles of selection in speciation from genomic patterns of divergence and introgression in secondary contact in venomous rattlesnakes.

ABSTRACT: Investigating secondary contact of historically isolated lineages can provide insight into how selection and drift influence genomic divergence and admixture. Here, we studied the genomic landscape of divergence and introgression following secondary contact between lineages of the Western Diamondback Rattlesnake (Crotalus atrox) to determine whether genomic regions under selection in allopatry also contribute to reproductive isolation during introgression. We used thousands of nuclear loci to study genomic differentiation between two lineages that have experienced recent secondary contact following isolation, and incorporated sampling from a zone of secondary contact to identify loci that are resistant to gene flow in hybrids. Comparisons of patterns of divergence and introgression revealed a positive relationship between allelic differentiation and resistance to introgression across the genome, and greater-than-expected overlap between genes linked to lineage-specific divergence and loci that resist introgression. Genes linked to putatively selected markers were related to prominent aspects of rattlesnake biology that differ between populations of Western Diamondback rattlesnakes (i.e., venom and reproductive phenotypes). We also found evidence for selection against introgression of genes that may contribute to cytonuclear incompatibility, consistent with previously observed biased patterns of nuclear and mitochondrial alleles suggestive of partial reproductive isolation due to cytonuclear incompatibilities. Our results provide a genome-scale perspective on the relationships between divergence and introgression in secondary contact that is relevant for understanding the roles of selection in maintaining partial isolation of lineages, causing admixing lineages to not completely homogenize.

SUBMITTER: Schield DR

PROVIDER: S-EPMC5468163 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Insight into the roles of selection in speciation from genomic patterns of divergence and introgression in secondary contact in venomous rattlesnakes.

Schield Drew R DR Adams Richard H RH Card Daren C DC Perry Blair W BW Pasquesi Giulia M GM Jezkova Tereza T Portik Daniel M DM Andrew Audra L AL Spencer Carol L CL Sanchez Elda E EE Fujita Matthew K MK Mackessy Stephen P SP Castoe Todd A TA

Ecology and evolution 20170423 11

Investigating secondary contact of historically isolated lineages can provide insight into how selection and drift influence genomic divergence and admixture. Here, we studied the genomic landscape of divergence and introgression following secondary contact between lineages of the Western Diamondback Rattlesnake (<i>Crotalus atrox</i>) to determine whether genomic regions under selection in allopatry also contribute to reproductive isolation during introgression. We used thousands of nuclear loc ...[more]

PMID: 28616190

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Project description:BackgroundHaldane's Rule, the tendency for the heterogametic sex to show reduced fertility in hybrid crosses, can obscure the signal of gene flow in mtDNA between species where females are heterogametic. Therefore, it is important when studying speciation and species limits in female-heterogametic species like birds to assess the signature of gene flow in the nuclear genome as well. We studied introgression of microsatellites and mtDNA across a secondary contact zone between coastal and interior lineages of Western Scrub-Jays (Aphelocoma californica) to test for a signature of Haldane's Rule: a narrower cline of introgression in mtDNA compared to nuclear markers.ResultsOur initial phylogeographic analysis revealed that there is only one major area of contact between coastal and interior lineages and identified five genetic clusters with strong spatial structuring: Pacific Slope, Interior US, Edwards Plateau (Texas), Northern Mexico, and Southern Mexico. Consistent with predictions from Haldane's Rule, mtDNA showed a narrower cline than nuclear markers across a transect through the hybrid zone. This result is not being driven by female-biased dispersal because neutral diffusion analysis, which included estimates of sex-specific dispersal rates, also showed less diffusion of mtDNA. Lineage-specific plumage traits were associated with nuclear genetic profiles for individuals in the hybrid zone, indicating that these differences are under genetic control.ConclusionsThis study adds to a growing list of studies that support predictions of Haldane's Rule using cline analysis of multiple loci of differing inheritance modes, although alternate hypotheses like selection on different mtDNA types cannot be ruled out. That Haldane's Rule appears to be operating in this system suggests a measure of reproductive isolation between the Pacific Slope and interior lineages. Based on a variety of evidence from the phenotype, ecology, and genetics, we recommend elevating three lineages to species level: A. californica (Pacific Slope); A. woodhouseii (Interior US plus Edwards Plateau plus Northern Mexico); A. sumichrasti (Southern Mexico). The distinctive Edwards Plateau population in Texas, which was monophyletic in mtDNA except for one individual, should be studied in greater detail given habitat threat.

Dataset Information

Insight into the roles of selection in speciation from genomic patterns of divergence and introgression in secondary contact in venomous rattlesnakes.

Publications

Insight into the roles of selection in speciation from genomic patterns of divergence and introgression in secondary contact in venomous rattlesnakes.

Similar Datasets

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