Genome-wide signatures of selection and introgression during rattlesnake speciation

Farleigh, Keaka 1 

Keaka.farleigh@virginia.edu

Dylan K. Highland 1, Megan G. Alderman 1, Yannick Francioli 2, Samuel R. Hirst 3, Blair W. Perry 4, Matthew L. Holding 5, Mark J. Margres 3, Stephen P. Mackessy 6, Jesse M. Meik 7, Todd A. Castoe 2 

Schield, Drew 1 *

drew.schield@virginia.edu

1 University of Virginia, 2 University of Texas at Arlington, 3 University of South Florida, 4 University of California Santa Cruz, 5 University of Michigan, 6 University of Northern Colorado, 7 Tarleton State University

* presenter

Speciation occurs as reproductive isolation evolves and prevents gene flow between species, yet gene flow can occur between lineages even at later stages of speciation. This influences heterogeneous genomic landscapes of genetic diversity and differentiation, and dissecting the interplay between selection and introgression is key to linking genomic patterns to reproductive isolation. Theoretically, genomic landscapes are tightly correlated between populations at the early stages of speciation and become less correlated with greater divergence. However, our knowledge is incomplete regarding how these expectations hold across the genome in regions affected by introgression and natural selection and how patterns are influenced by recombination rate. Species complexes that exchange gene flow across a continuum of divergence are ideally suited for investigating these factors. We generated whole genome sequencing data for 182 individuals from two rattlesnake species complexes with a history of gene flow in secondary contact following allopatric divergence – the western rattlesnakes and speckled rattlesnakes (Crotalus spp.) – to examine genomic landscapes of diversity and differentiation and to map genome-wide signatures of selection and introgression. We generated a new chromosome-level reference genome assembly for the southwestern speckled rattlesnake (C. pyrrhus) and used it to interpret genomic patterns of variation within and between species. We find strong correlations among genomic landscapes within low recombination regions of the genome but idiosyncratic patterns in regions with high recombination rates. We also find positive genome-wide relationships between recombination rate and introgression, consistent with the effects of selection against gene flow in low recombination regions. Conversely, numerous genomic regions show evidence of introgression, even between distantly related species. A subset of these regions shows signatures of adaptive introgression, wherein beneficial alleles are exchanged between snake populations. Our findings reveal complex genomic landscapes of selection and introgression and provide new context for understanding strong but incomplete reproductive isolation between rattlesnake species.