Meiotic recombination in vertebrates is concentrated in hotspots throughout the genome. The location and stability of hotspots have been linked to the presence or absence of PRDM9, leading to two primary models for hotspot evolution derived from mammals and birds. Species with PRDM9-directed recombination have rapid turnover of hotspots concentrated in intergenic regions (i.e., mammals), whereas hotspots in species lacking PRDM9 are concentrated in functional regions and have greater stability over time (i.e., birds). Snakes possess PRDM9, yet virtually nothing is known about snake recombination. Here, we examine the recombination landscape and test hypotheses about the roles of PRDM9 in rattlesnakes. We find substantial variation in recombination rate within and among snake chromosomes, and positive correlations between recombination rate and gene density, GC content, and genetic diversity. Like mammals, snakes appear to have a functional and active PRDM9, but rather than being directed away from genes, snake hotspots are concentrated in promoters and functional regions—a pattern previously associated only with species that lack a functional PRDM9. Snakes therefore provide a unique example of recombination landscapes in which PRDM9 is functional, yet recombination hotspots are associated with functional genic regions—a combination of features that defy existing paradigms for recombination landscapes in vertebrates. Our findings also provide evidence that high recombination rates are a shared feature of vertebrate microchromosomes. Our results challenge previous assumptions about the adaptive role of PRDM9 and highlight the diversity of recombination landscape features among vertebrate lineages.

Understanding the processes and mechanisms that promote lineage divergence is a central goal in evolutionary biology. For instance, studies investigating the spatial distribution of genomic variation often highlight biogeographic barriers underpinning geographic isolation, as well as patterns of isolation by environment and isolation by distance that can also lead to lineage divergence. However, the patterns and processes that shape genomic variation and drive lineage divergence may be taxa-specific, even across closely related taxa co-occurring within the same biogeographic region. Here, we use molecular data in the form of ultra-conserved elements (UCEs) to infer the evolutionary relationships and population genomic structure of the Eastern Pinesnake complex (Pituophis melanoleucus) – a polytypic wide-ranging species that occupies much of the Eastern Nearctic. In addition to inferring evolutionary relationships, population genomic structure, and gene flow, we also test relationships between genomic diversity and putative barriers to dispersal, environmental variation, and geographic distance. We present results that reveal shallow population genomic structure and ongoing gene flow, despite an extensive geographic range that transcends geographic features found to reduce gene flow among many taxa, including other squamate reptiles within the Eastern Nearctic. Further, our results indicate that the observed genomic diversity is spatially distributed as a pattern of isolation by distance and suggest that the current subspecific taxonomy do not adhere to independent lineages, but rather, show a significant amount of admixture across the entire P. melanoleucus range.

No abstract

Understanding the processes and mechanisms that promote lineage divergence is a central goal in evolutionary biology. For instance, studies investigating the spatial distribution of genomic variation often highlight biogeographic barriers underpinning geographic isolation or patterns of isolation by environment and isolation by distance that can also lead to lineage divergence. However, the patterns and processes that shape genomic variation and drive lineage divergence may be taxon-specific, even across closely related taxa co-occurring within the same biogeographic region. Here, we use molecular data in the form of ultraconserved elements (UCEs) to infer the evolutionary relationships and population genomic structure of the Eastern Pinesnake complex (Pituophis melanoleucus)-a polytypic wide-ranging species that occupies much of the Eastern Nearctic. In addition to inferring evolutionary relationships, population genomic structure and gene flow, we also test relationships between genomic diversity and putative barriers to dispersal, environmental variation, and geographic distance. We present results that reveal shallow population genomic structure and ongoing gene flow, despite an extensive geographic range that transcends geographic features found to reduce gene flow among many taxa, including other squamate reptiles within the Eastern Nearctic. Further, our results indicate that the observed genomic diversity is spatially distributed as a pattern of isolation by distance and suggest that the current subspecific taxonomy do not adhere to independent lineages, but, rather, show a significant amount of admixture across the entire P. melanoleucus range.