Contrasting signatures of introgression in North American box turtle (Terrapene spp.) contact zones

Abstract

Hybridization occurs differentially across the genome in a balancing act between selection and migration. With the unprecedented resolution of contemporary sequencing technologies, selection and migration can now be effectively quantified such that researchers can identify genetic elements involved in introgression. Furthermore, genomic patterns can now be associated with ecologically relevant phenotypes, given availability of annotated reference genomes. We do so in North American box turtles (Terrapene) by deciphering how selection affects hybrid zones at the interface of species boundaries and identifying genetic regions potentially under selection that may relate to thermal adaptations. Such genes may impact physiological pathways involved in temperature-dependent sex determination, immune system functioning and hypoxia tolerance. We contrasted these patterns across inter-and intraspecific hybrid zones that differ temporally and biogeographically. We demonstrate hybridization is broadly apparent in Terrapene, but with observed genomic cline patterns corresponding to species boundaries at loci potentially associated with thermal adaptation. These loci display signatures of directional introgression within intraspecific boundaries, despite a genome-wide selective trend against intergrades. In contrast, outlier loci for interspecific comparisons exhibited evidence of being under selection against hybrids. Importantly, adaptations coinciding with species boundaries in Terrapene overlap with climatic boundaries and highlight the vulnerability of these terrestrial ectotherms to anthropogenic pressures.

The Himalayan Uplift and the Evolution of Aquatic Biodiversity Across Asia: Snowtrout (Cyprininae: Schizothorax) as a Test Case

“…Speciation in the Karnali River Basin could thus be poorly resolved with respect to mitochondrial divergence, with a genetic signal likely obscured by the limited framework within which ancestral alleles could sort, allowing novel haplotypes to arise. More refined molecular approaches, such as reduced-representation genomics [32,33,34,49,50], could potentially provide the necessary resolution, although it will again be compounded by the rampant polyploidy found in Cyprininae.…”

Current and Forthcoming Approaches for Benchmarking Genetic and Genomic Diversity

“…Analyzing more than 10,000 unlinked reference-mapped loci, they found that while in the midwestern contact area hybrids are present in low numbers and restricted to F1 generations only, the southeastern contact area included many backcrosses and F2 individuals, providing evidence of higher levels of introgression between the taxa. Interestingly, they found a set of specific loci with steep genomic clines between taxa, strongly correlated with temperature variables, but not with any precipitation or wind-related variables (Martin et al, 2020). The authors interpreted this as evidence of thermal gradients having a strong effect on introgression patterns and predicted that future changes in temperature could significantly affect the integrity of species boundaries within this genus of turtles (Martin et al, 2020).…”

“…Particularly susceptible to temperature changes are ectotherms, such as North American box turtles (Terrapene sp.). Martin et al (2020) assembled a dataset of samples from more than 350 individuals across two well-studied zones of hybridization within this genus: one in South Eastern United States, between the woodland (T. carolina carolina), Gulf coast (T. c. major), three-toed (T. carolina triunguis) and Florida (T. bauri) box turtles, and the other one in Midwestern United States, between one subspecies of the ornate box turtle, T. ornata ornata, and T. c. carolina (see Martin et al, 2020 and references therein). Based on these replicated instances of contact at the intra and interspecific levels, the authors were also able to study the contrasting effects of selection and migration on hybridization.…”

ClinePlotR: Visualizing genomic clines and detecting outliers in R

“…We also provide several additional functions (see Figure 1) that have considerable use cases, although some seemingly deviate from the ‘core’ bgc workflow. The first of several can be used to map parameter values of bgc clines onto a chromosomal ideogram via the function plot_outlier_ideogram (e.g., Figure 3), Here, bgc results are depicted for a case study examining hybridization between Woodland ( Terrapene carolina carolina ) and Three-toed box turtles ( Terrapene mexicana triunguis ) (Martin et al, 2020). However, some external user-steps are required to use the function.…”

“…Patterns of multi-locus differentiation, as distributed across admixture gradients, have long provided a window into divergence and speciation (e.g., Barton, 1983; Gompert, Mandeville, & Buerkle, 2017). Accordingly, they have been used to map loci associated with adaptation or reproductive isolation (Buerkle & Lexer, 2008; Martin et al, 2020), and as indicators of biotic responses to environmental change (Chafin, Douglas, Martin, & Douglas, 2019). Rather than relating these to patterns in the landscape, contemporary approaches have instead drawn conclusions based on genome-wide ancestries (Gompert & Buerkle, 2009; Fitzpatrick, 2013).…”