Genomic architecture of parallel ecological divergence: beyond a single environmental contrast

Abstract

The genetic basis of parallel ecological divergence provides important clues to the operation of natural selection and the predictability of evolution. Many examples exist where binary environmental contrasts seem to drive parallel divergence. However, this simplified view can conceal important components of parallel divergence because environmental variation is often more complex. Here, we disentangle the genetic basis of parallel divergence across two axes of environmental differentiation (crab-predation vs. wave-action and low-shore vs. high-shore habitat contrasts) in the marine snail Littorina saxatilis, a well established natural system of parallel ecological divergence. We used whole-genome resequencing across multiple instances of these two environmental axes, at local and regional scales from Spain to Sweden. Overall, sharing of genetic differentiation is generally low but it is highly heterogeneous across the genome and increases at smaller spatial scales. We identified genomic regions, both overlapping and non-overlapping with recently described candidate chromosomal inversions, that are differentially involved in adaptation to each of the environmental axis. Thus, the evolution of parallel divergence in L. saxatilis is largely determined by the joint action of geography, history, genomic architecture and congruence between environmental axes. We argue that the maintenance of standing variation, perhaps as balanced polymorphism, and/or the re-distribution of adaptive variants via gene flow can facilitate parallel divergence in multiple directions as an adaptive response to heterogeneous environments.