Mitogenome selection shaped the terrestrial adaptation of Grapsidae (Decapoda: Brachyura)

Abstract

The colonization of aquatic to terrestrial habitats by brachyuran crabs requires genetic innovations as well as morphological adaptations to adapt to terrestrial environments. The genetic basis of such adaptive evolution, however, is largely unknown. This study focuses on terrestrialization in Geograpsus (Grapsidae) the only highly terrestrial genus in this family, which represents a notable example of terrestrial adaptive radiation. Here, we sequenced the mitogenomes of two Geograpsus species and used the mitogenomes of 215 representative crabs to construct phylogenetic and time frameworks that we used to infer terrestrial origins and evolution. Using mitochondrial genomic data, we demonstrated that marine crab ancestors began to settle on land during the early Eocene. Ocean acidification, the Paleocene-Eocene Thermal Maximum (PETM), and mangrove expansion at that time may have driven the diversification and ecological expansion of these terrestrial crabs. Evolutionary analyses reveal strong positive selection signals on monophyletic lineages of Grapsidae, especially the terrestrial species of Geograpsus. Positively selected sites in functionally important regions of ND5 and ND4 may imply enhanced energy metabolism in Grapsidae compared to other crabs, and may have played an important role in their terrestrial adaptation. Overall, our work provides valuable resources and opportunities to reveal the adaptation of crabs to complex terrestrial environments.