Fine‐scale population structure within an Eastern Nearctic snake complex (Pituophis melanoleucus)

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.

Phylogenetics, subspecies, and conservation of the eastern pinesnake

“…As in Nikolakis et al (2022), the currently recognized subspecies do not correspond to monophyletic groups; however, in contrast to Nikolakis et al (2022), we disagree that this means the subspecies should not be recognized. We do not believe that monophyly or independent lineages (Nikolakis et al 2022) should be expected for subspecific units, as other researchers have reported (Mikles et al 2020, Marshall et al 2021) and as theory predicts (Wilson and Brown 1953, Hillis et al 2021, Dufresnes et al 2023). If subspecific lineages were truly independent, they might be better referred to as species, not subspecies (Wiley 1978; de Queiroz 1998, 2020; Hillis 2020; Dufresnes et al 2023).…”

“…We used 2 genomic methods to understand eastern pinesnake relationships: ultra‐conserved element (UCE) sequencing and restriction‐associated digest sequencing (RADseq, specifically 3RAD; Figure 1). The UCE dataset helped resolve deeper phylogenetic nodes (Faircloth et al 2012), and allowed us to compare our new data to existing eastern pinesnake genomics (Nikolakis et al 2022). The 3RAD dataset allowed us to sequence more individuals, and derive population‐level analyses.…”

“…We used the PHYLUCE package (Faircloth 2016) to clean the UCE data, assemble the raw data into known UCE loci, and align those loci among the individuals in our library. First, we added 39 additional Pituophis species and 3 outgroup samples from the short read archive (PRJNA635996; Nikolakis et al 2022), totaling 89 samples in our combined dataset. Next, we trimmed the combined samples according to the default settings in PHYLUCE.…”

“…The samples used in this study are colored by whether they were used in the restriction‐associated digest sequencing (RADseq) or ultra‐conserved element (UCE) analyses. The map does not include samples from Nikolakis et al (2022), which were added to the UCE analysis. The map shows higher elevation areas in dark colors, and rivers referenced in the text.…”

Complex cycles of divergence and migration shape lineage structure in the common kingsnake species complex

“…However, higher sNMF support for all eastern samples as a single cluster and a linear relationship between genetic and geographical distance for the eastern samples indicates that the structure in the eastern lineage of the L. getula complex ( holbrooki, nigra and getula sensu stricto) is primarily continuous spatial structure, consistent with isolation by distance, rather than discrete lineage structure. A similar pattern was identified in the Eastern Pinesnake ( Pituophis melanoleucus ) complex, which also shows clinal structure across the eastern Nearctic dominated by isolation by distance (Nikolakis et al, 2022). This does not imply that the eastern lineage was not fragmented at some point during glacial cycles or subject to other processes, only that our data do not indicate the presence of multiple discrete lineages at present.…”