Mitochondrial genomics of Anomura reveal molecular clues for terrestrial strategies and parallel evolution

Anomura is the most phenotypically diverse Decapoda taxon, found in both hydrothermal vent and various aquatic habitats as well as on the land. Paguroidea is a unique superfamily of Anomura, which lives symbiotically with gastropod shells and certain species are well adapted to terrestrial habitats, but their phylogeny and genetic basis of terrestrial adaptive mechanisms are unclear. We newly sequenced two mitogenomes of Paguroidea (Clibanarius longitarsus, Coenobita lila) and reconstructed a comprehensive phylogenetic tree based on 38 Anomura mitogenomes. The phylogenetic tree indicates that Paguroidea may undergone complex parallel evolutions and Anomura multiple phylogenetic pathways in the context of carcinization. To identify critical genes in the terrestrial strategies of Paguroidea, we further evaluated selection pressure on mitochondrial OXPHOS genes. Positive selection was detected in several genes, suggesting that these genes may enhance cellular respiration and aerobic metabolism to adapt to the terrestrial environment. Notably, similar selection pressures were detected in distinct branches of Paguroidea, largely induced parallel origin of Paguroidea. Phylogenetic studies provide a theoretical basis for the conservation and use of Anomura's genetic resources. Additionally, the adaptive evolutionary signatures of the Paguroidea have significantly improved our understanding of the history of adaptive evolution and the survival of terrestrial animals on land.