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

Authors: MAIER, PAUL - San Diego State University; VANDERGAST, AMY - Us Geological Society; Ostoja, Steven; AGUILAR, ANDRES - California State University; BOHONAK, ANDREW - San Diego State University

Submitted to: Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/14/2019
Publication Date: 10/29/2019
Citation: Maier, P.A., Vandergast, A.G., Ostoja, S.M., Aguilar, A., Bohonak, A.J. 2019. Pleistocene glacial cycles drove lineage diversification and fusion in the Yosemite toad (Anaxyrus canorus). Evolution. 73(12):2476-2496. https://doi.org/10.1111/evo.13868.
DOI: https://doi.org/10.1111/evo.13868

Interpretive Summary: Anticipating how ecosystems will respond to disturbances is a key challenge for scientists and a daily issue for managers. A great research effort has been devoted to improving our ability to quantify resilience – the capacity of an ecosystem to recover after perturbations. Resilience is impaired when an ecosystem can be found in different possible states (e.g. vegetation and desert in drylands) and can therefore shift between those alternative states following perturbations. Previous work has suggested that mapping the distribution of ecosystem states across very large spatial scales could inform us on the presence of alternative stable states in a given biome. However, these approaches have never been applied at scales that are directly relevant to conservation issues. Here, we extended these approaches to small scale, multivariate data such as those typically gathered in field vegetation surveys and applied them to study fragile subalpine ecosystems from two iconic conservation areas, Yosemite and Sequoia National Parks (USA). We combined vegetation surveys with measurements of local environmental conditions to reveal plausible alternative stable states in terms of plant community compositions in dry zones of subalpine meadows. Our results suggest that ecosystem resilience can be mapped in space so as to identify fragile areas and help prioritize management.

Technical 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.