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.

Multiple forms of selection shape reproductive isolation in a primate hybrid zone

“…Similarly, we observed neutral and increased introgression for markers with very high, moderate and no differentiation (i.e., from F ST = 0 to F ST = 1) (Figure b). These observations are similar to those in other hybrid zones (e.g., Janoušek et al, , Schield et al, ) and are likely a reflection of the complexity of the interaction between selection, drift and recombination and suggest that these forces vary across the genome. Despite the mechanism of divergence, this also demonstrates that high differentiation in allopatry is not a perfect predictor for reproductive isolation.…”

“…Similarly, we observed neutral and increased introgression for markers with very high, moderate and no differentiation (i.e., from F ST = 0 to F ST = 1) ( Figure 5b). These observations are similar to those in other hybrid zones (e.g., Janoušek et al, 2015, Schield et al, 2017 and…”

The combined use of raw and phylogenetically independent methods of outlier detection uncovers genome‐wide dynamics of local adaptation in a lizard

“…Bar colors represent posterior probabilities of cluster membership unmistakably eastern genetic background, but is consistent with their western-like habitat. This link between habitat and phenotype was in harmony with the pattern of genetic structuring of the outliers identified in the genome, an observation which substantiates the adaptive value of these genetic variants (Rhode et al, 2017;Rosenblum, Rompler, Schoneberg, & Hoekstra, 2010;Schield et al, 2017). Highly divergent populations (Aranjuez and western) have genetic variants subject to selection that seem to have been fixed along their evolutionary history.…”

“…Thus, the way in which populations locally adapt will depend on their phylogeographic history as realized in terms of past genetic change (either adaptive or stochastic, or influenced by gene flow; Barrett & Schluter, 2008;Han et al, 2017). This may often complicate the detection and interpretation of loci subject to selection (Rhode, Bester-Van Der Merwe, & Roodt-Wilding, 2017;Schield et al, 2017;Tigano, Shultz, Edwards, Robertson, & Friesen, 2017).…”

Genomic divergence in allopatric Northern Cardinals of the North American warm deserts is linked to behavioral differentiation

“…The genetic turnover of taxa between the Sonoran and Chihuahuan deserts generally occurs between the Baboquivari Mountains of Arizona and the Trans-Pecos of Texas (108-112°W longitude; reviewed by Hafner & Riddle, 2011), but there is no narrow concordant transition zone across taxa (Pyron & Burbrink, 2010). Some species are genetically isolated across the Cochise Filter Barrier while others are unstructured or appear to maintain gene flow in birds (Riddle & Hafner, 2006;Zink, 2002;Zink, Kessen, Line, & Blackwell-Rago, 2001) and other vertebrates (Castoe, Spencer, & Parkinson, 2007;Jaeger, Riddle, & Bradford, 2005;Mantooth, Hafner, Bryson, & Riddle, 2013;Myers, Hickerson, & Burbrink, 2017;Orange, Riddle, & Nickle, 1999;Pyron & Burbrink, 2009;Riddle & Hafner, 2006;Riddle, Hafner, & Alexander, 2000;Schield et al, 2017Schield et al, , 2015Serb, Phillips, & Iverson, 2001); as such, the barrier is semipermeable to gene flow. For populations distributed across the Cochise Filter Barrier, it is unclear which mechanisms have facilitated or inhibited gene flow.…”