Using landscape genomics to delineate future adaptive potential for climate change in the Yosemite toad (Anaxyrus canorus)

Abstract

An essential goal in conservation biology is delineating population units that maximize the probability of species persisting into the future and adapting to future environmental change. However, future‐facing conservation concerns are often addressed using retrospective patterns that could be irrelevant. We recommend a novel landscape genomics framework for delineating future “Geminate Evolutionary Units” (GEUs) in a focal species: (1) identify loci under environmental selection, (2) model and map adaptive conservation units that may spawn future lineages, (3) forecast relative selection pressures on each future lineage, and (4) estimate their fitness and likelihood of persistence using geo‐genomic simulations. Using this process, we delineated conservation units for the Yosemite toad ( Anaxyrus canorus ), a U.S. federally threatened species that is highly vulnerable to climate change. We used a genome‐wide dataset, redundancy analysis, and Bayesian association methods to identify 24 candidate loci responding to climatic selection ( R 2 ranging from 0.09 to 0.52), after controlling for demographic structure. Candidate loci included genes such as MAP3K5, involved in cellular response to environmental change. We then forecasted future genomic response to climate change using the multivariate machine learning algorithm Gradient Forests. Based on all available evidence, we found three GEUs in Yosemite National Park, reflecting contrasting adaptive optima: YF‐North (high winter snowpack with moderate summer rainfall), YF‐East (low to moderate snowpack with high summer rainfall), and YF‐Low‐Elevation (low snowpack and rainfall). Simulations under the RCP 8.5 climate change scenario suggest that the species will decline by 29% over 90 years, but the highly diverse YF‐East lineage will be least impacted for two reasons: (1) geographically it will be sheltered from the largest climatic selection pressures, and (2) its standing genetic diversity will promote a faster adaptive response. Our approach provides a comprehensive strategy for protecting imperiled non‐model species with genomic data alone and has wide applicability to other declining species.

Yosemite toad (Anaxyrus canorus) transcriptome reveals interplay between speciation genes and adaptive introgression

“…Yosemite toad tadpoles in the Y‐East lineage have been shown to possess faster development times than any other lineage (P. Maier, unpublished data), and so this trait may be spreading adaptively into the lower elevation Y‐West. Lower elevation toads face more intense selective death due to climate change, where other climate‐related loci such as MAP3K5 show patterns of adaptation (Maier et al., 2023).…”

“…Fish & Wildlife Service, 2014). These toads appear to have lineage‐specific genomic variation adapted to varying levels of winter snowpack and summer rainfall (Maier et al., 2023). Tadpole growth and development are generally seen as a life history trade‐off, where faster development comes at the expense of smaller size at metamorphosis (for a comparative analysis, see Richter‐Boix et al., 2011).…”

“…Our analytical workflow used several divergence estimators to ensure that putative islands were not artifacts of any particular method (Cruickshank & Hahn, 2014), and used Bayesian genomic cline analysis (Gompert & Buerkle, 2011) to identify likely rivers. Understanding how adaptation and speciation proceed for this federally threatened species is essential, because long‐term population declines and susceptibility to climate change make its future uncertain (Brown et al., 2015; Maier et al., 2022b, 2023; U.S. Fish & Wildlife Service, 2014).…”

Importance of Genetic–Fitness Correlations for the Conservation of Amphibians

“…Once those genes have been identified, beneficial variants should be introduced into the affected threatened populations. For example, in the Yosemite toad, Anaxyrus canorus, 24 candidate genes have been identified that seem to be under climate-related selection [85]. Identifying more critical genes under selection by environmental change and how they might contribute to species conservation, together with the maintenance of a substantial level of local genetic variation, is the next challenge in genetic amphibian conservation science.…”

“…A matter of current and future interest should be the correlation between neutral genetic variation and adaptive variation as well as the presence of adaptive loci that help to counteract particular adverse environmental conditions. For example, only a few studies to date have found adaptive loci associated with climatic conditions [82,[84][85][86] despite the evident risk climate change poses on amphibians.…”