Pleistocene glacial cycles drove lineage diversification and fusion in the Yosemite toad (Anaxyrus canorus)

Abstract

Species endemic to alpine environments can evolve via steep ecological selection gradients between lowland and upland environments. Additionally, many alpine environments have faced repeated glacial episodes over the past two million years, fracturing these endemics into isolated populations. In this “glacial pulse” model of alpine diversification, cycles of allopatry and ecologically divergent glacial refugia play a role in generating biodiversity, including novel admixed (“fused”) lineages. We tested for patterns of glacial pulse lineage diversification in the Yosemite toad (Anaxyrus [Bufo] canorus), an alpine endemic tied to glacially influenced meadow environments. Using double‐digest RADseq on populations densely sampled from a portion of the species range, we identified nine distinct lineages with divergence times ranging from 18 to 724 thousand years ago (ka), coinciding with multiple Sierra Nevada glacial events. Three lineages have admixed origins, and demographic models suggest these fused lineages have persisted throughout past glacial cycles. Directionality indices supported the hypothesis that some lineages recolonized Yosemite from east of the ice sheet, whereas other lineages remained in western refugia. Finally, refugial niche reconstructions suggest that low‐ and high‐elevation lineages have convergently adapted to similar climatic niches. Our results suggest glacial cycles and refugia may be important crucibles of adaptive diversity across deep evolutionary time.

Phylogeographic analysis of shrubby beardtongues reveals range expansions during the Last Glacial Maximum and implicates the Klamath Mountains as a hotspot for hybridization

“…Advancements in sequencing technology have given rise to an increased availability of high-throughput sequence data for use in phylogeographic studies (Garrick et al, 2015), which has in turn allowed researchers to compare more complex models of demographic history (e.g., Smith et al, 2017). Although it has long been suggested that the expansion and contraction of species ranges in response to glacial cycles led to the formation of many hybrid zones (Hewitt, 2011;Stebbins, 1985), the use of high-throughput sequence data in phylogeographic studies has increased awareness of the prevalence and complexity of gene flow and hybridization in species' responses to climatic change (Maier et al, 2019;Ruffley et al, 2018;Smith & Carstens, 2020). There are numerous potential outcomes of secondary contact, but some well-known examples include lineage fusion (Petit et al, 2003), adaptive introgression (Anderson & Stebbins, 1954), and speciation via reinforcement (Butlin, 1987).…”

Evidence for Glacial Refugia of the Forest Understorey Species Helleborus niger (Ranunculaceae) in the Southern as Well as in the Northern Limestone Alps

“…To do so, all RADseq tags were exported from the Stacks catalogue using populations.pl and the --fasta-samples flag ( Catchen et al, 2013 ). The fasta file was converted to phylip format using the python script fasta2genotype.py ( Maier et al, 2019 ), and by doing so, also loci with excess heterozygosity (>65%) were removed to filter for paralogs. For further analysis, the individuals with the lowest amount of missing data were selected from each of the three clusters, resulting in an alignment with 29 individuals (Western Group 10, South-Eastern Subgroup 9, and North-Eastern Subgroup 10).…”

Reticulate Evolutionary History in a Recent Radiation of Montane Grasshoppers Revealed by Genomic Data

“…Isolation periods contributed to genetic and phenotypic differentiation, fueling allopatric adaptive (i.e., divergent natural selection) and nonadaptive (i.e., genetic-drift) lineage divergence and/or reinforcing existing species boundaries (Hewitt 1996(Hewitt , 1999Czekanski-Moir and Rundell 2019). If reproductive isolation did not evolve while in refugia, secondary contact during range shifts resulted in the collapse of formerly distinct lineages (i.e., speciation reversal; Kearns et al 2018;Maier et al 2019), introgressive hybridization (e.g., Salzburger et al 2002;Schweizer et al 2019), or even contributed to complete the speciation process via reinforcement of reproductive isolation (Butlin and Hewitt 1985;Hewitt 1996;Nevado et al 2018). For these reasons, Pleistocene glacial cycles have been considered to both promote range fragmentation and allopatric speciation (Knowles 2000) and inhibit speciation through genetic homogenization (Zink and Slowinski 1995;Klicka and Zink 1997).…”