Genomic Divergence and Variation in Developmental Plasticity Across Inselberg Populations of a Tropical Frog

ABSTRACT

Understanding how phenotypic plasticity and local specialization are shaped by gene flow and environmental heterogeneity requires natural systems that vary in both spatial isolation and environmental conditions across the landscape, yet such systems are uncommon. Naturally discontinuous inselbergs may provide this opportunity. Here, using populations of the inselberg‐specialist frog Leptodactylus lithonaetes , we evaluated whether habitat discontinuity translates into restricted gene flow and genetic structure and then tested how variation in connectivity and environmental heterogeneity shapes the balance between phenotypic plasticity and local specialization. We predicted that populations with higher environmental heterogeneity and higher gene flow would evolve plasticity in growth and development, whereas populations in more homogeneous environments and more genetically isolated would exhibit reduced plasticity and increased specialization. Using > 11,000 SNPs, we showed that the apparent habitat discontinuity among nine inselbergs spanning 300 km was reflected in a strong population structure and varying levels of gene flow among inselbergs, in an isolation‐by‐distance pattern. We then tested whether tadpoles alter their size or timing at metamorphosis to pond‐drying risk, and whether these plastic responses vary among populations with environmental heterogeneity (seasonality). Although tadpoles did not plastically accelerate metamorphosis under pond‐drying risk, the magnitude of body mass reduction under desiccation stress differed among populations, indicating developmental plasticity in body mass. Northern localities, exposed to greater environmental heterogeneity, showed greater survival and less body weight loss, resulting in higher tolerance to environmental stress than southern localities. Even in the absence of developmental acceleration, population‐level variation in responses to environmental stress is congruent with reduced plasticity, or increased specialization, in isolated populations exposed to less heterogeneous environments.