Multi‐Taxa Genome‐Environment Associations With Contemporary and Historical Climate in the Brazilian Atlantic Forest
Laura D. Bertola, Mariana M. Vasconcellos, Roberta P. Damasceno, Ivan Prates, Marcelo Reginato, Gregory Thom, Andressa Nuss, Fabio Raposo do Amaral, Ana Beatriz da Silva Bueno, Cristina Yumi Miyaki, Gustavo S. Cabanne, Leonardo Campagna, Jacob S. Berv, Marcos Maldonado‐Coelho, Sidnei Sampaio dos Santos, Karina Lucas Silva‐Brandão, Luiza Moraes Magaldi, Daniel Michiute Carolino, André Victor Lucci Freitas, Miguel Trefaut Rodrigues, Fabián A. Michelangeli, Kyle McDonald, Ana C. Carnaval, Michael J. HickersonABSTRACT
Multi‐taxa genomic data offer valuable opportunities to assess the extent to which co‐distributed taxa exhibit parallel responses to shared environmental regimes and climatic history. In this study, we use genome‐environment associations (GEA) to examine how present and past climate may have shaped spatial patterns of adaptive genomic variation across 27 taxa in the Atlantic Forest biodiversity hotspot. Our sampling repurposes existing data from a wide array of taxonomic groups, including frogs, lizards, birds, butterflies, flowering plants, and a conifer, spanning multiple bioclimatic domains and representing variation in range size, niche volume, and niche marginality. Using these data, we explore two alternative hypotheses linking genomic adaptation to local environmental conditions with three species traits: range size, specialization (the inverse of niche volume), and niche marginality. The first hypothesis (H1) posits that taxa with large ranges, low specialization, and low niche marginality contain more climate‐associated SNPs, as they are expected to harbor higher levels of standing genetic variation, forming a crude basis for genetic adaptation. An alternative hypothesis (H2) predicts that large‐ranged species rely on other means of adaptation, such as phenotypic plasticity rather than on fixed genomic changes across environmental gradients and that stronger adaptive genomic responses happen in taxa with small ranges, high specialization, and high marginality. Our results show highly variable and species‐specific genomic associations with climate, measured as the percentage of sampled SNPs correlated with environmental variables. There is no strong evidence that species' range size, specialization, or niche marginality consistently predict the proportion of climate‐associated loci, rendering us unable to conclusively distinguish between H1 and H2. However, when the data are partitioned by taxonomic group, trend directionalities are more consistent with H2. Our findings highlight that the genomic basis of local adaptation varies substantially across taxa, underscoring the complexity of biodiversity patterns and dynamics, and the challenges of exploring alternative hypotheses through repurposing of existing data for multi‐taxa inference. They also emphasize that conservation strategies should be prepared to account for taxon‐specific responses rather than relying on generalized expectations across species. We hope that these results can inspire future studies of species' responses to climate in the Atlantic Forest and beyond, informing strategies for biodiversity monitoring and conservation.