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

Drew R Schield,Stephen P Mackessy,Richard H Adams,Audra L Andrew,Todd A Castoe,Carol L Spencer,Matthew K Fujita,Daniel M Portik,Elda E Sanchez,Blair W Perry,Tereza Jezkova,Giulia M Pasquesi,Daren C Card

doi:10.1002/ece3.2996

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.

Highlights

Understanding the process of speciation requires insight into both the processes that underlie lineage divergence in isolation and the processes that maintain lineage integrity in the face of gene flow during secondary contact
Locally adapted genes subject to geographically variable selection may contribute to reduced gene flow and genetic isolation in structured populations that come into secondary contact (Boughman, 2001; Nosil, Egan, & Funk, 2008; Orr & Smith, 1998; Rosenblum, 2006), as alleles from one parental population may offer a greater fitness advantage to hybrids
While links between adaptive evolution and speciation have been established (Faria et al, 2014; Schluter & Conte, 2009), a largely unanswered question is whether the same genomic regions are important in both the process of divergence in isolation and in preventing gene flow in secondary contact

Summary

| INTRODUCTION

Understanding the process of speciation requires insight into both the processes that underlie lineage divergence in isolation and the processes that maintain lineage integrity (i.e., limit gene flow) in the face of gene flow during secondary contact. We did not observe individuals with largely “western” nuclear genomes with “eastern” mitochondrial haplotypes (Schield et al, 2015) We proposed that this asymmetry could have arisen from cytonuclear incompatibilities that evolved during divergence in isolation and that reduce the fitness of hybrids in secondary contact, which we explore further in this paper with expanded data and analyses. We first use our large nuclear locus dataset to test competing models of speciation in Western Diamondbacks to test the hypothesis of population divergence followed by secondary contact, which is strongly supported by previous studies (Castoe et al, 2007; Schield et al, 2015) We leverage this system to address the following questions central to the role of adaptive evolution in lineage divergence and.

| MATERIALS AND METHODS

| DISCUSSION

| CONCLUSIONS

Findings

DATA ACCESSIBILITY