Evidence for ecotone speciation across an African rainforest-savanna gradient.

ABSTRACT

Accelerating climate change and habitat loss make it imperative that plans to conserve biodiversity consider species' ability to adapt to changing environments. However, in biomes where biodiversity is highest, the evolutionary mechanisms responsible for generating adaptative variation and, ultimately, new species are frequently poorly understood. African rainforests represent one such biome, as decadal debates continue concerning the mechanisms generating African rainforest biodiversity. These debates hinge on the relative importance of geographic isolation versus divergent natural selection across environmental gradients. Hindering progress is a lack of robust tests of these competing hypotheses. Because African rainforests are severely at-risk due to climate change and other anthropogenic activities, addressing this long-standing debate is critical for making informed conservation decisions. We use demographic inference and allele frequency-environment relationships to investigate mechanisms of diversification in an African rainforest skink, Trachylepis affinis, a species inhabiting the gradient between rainforest and rainforest-savanna mosaic (ecotone). We provide compelling evidence of ecotone speciation, in which gene flow has all but ceased between rainforest and ecotone populations, at a level consistent with infrequent hybridization between sister species. Parallel patterns of genomic, morphological, and physiological divergence across this environmental gradient and pronounced allele frequency-environment correlation indicate speciation is mostly probably driven by ecological divergence, supporting a central role for divergent natural selection. Our results provide strong evidence for the importance of ecological gradients in African rainforest speciation and inform conservation strategies that preserve the processes that produce and maintain biodiversity.