Not Just a Matter of Space: Integrating Ecological Niche Modeling With Genotype-Environment Associations Suggests High Maladaptation Risks Under Climate Change for a Microendemic Malagasy Frog

Climate change is impacting biodiversity worldwide at an accelerating pace. Traditionally, Ecological Niche Models (ENMs) have been widely used to infer the likely impacts of climate change on species, while accounting for their potential dispersal towards climatically suitable habitats. More recently, Genotype-environment association (GEA) approaches applied to genomic data have opened the possibility to investigate local adaptation underlying species' genetic adaptive capacity, allowing quantification of maladaptation risk under future climatic conditions. In this study, we integrate ENMs with GEAs to assess climate change impacts on Mantidactylus bourgati, a frog microendemic to the Andringitra Massif in southeastern Madagascar. ENMs forecasted a progressive decline in climatically suitable habitat that, depending on the climate change scenario, could lead to either complete extinction or a strong reduction and disjunct future distribution. GEA analyses suggested spatially structured genotype-environment associations consistent with local adaptation, with three distinct adaptive units associated with the wide environmental gradients characterizing the Andringitra Massif region. Genetic offset calculations suggested that even if M. bourgati may succeed in tracking suitable habitats through dispersal, the future genetic change required to maintain the same adaptation to current climatic conditions will be significant, implying a high risk of maladaptation. Moreover, most future refugial habitats are projected to fall outside Madagascar's network of protected areas. These findings emphasize the importance of integrating species' genetic adaptive capacity into conservation strategies and spatial planning to help mitigate future climate change impacts on biodiversity.