Evolution and phylogenetic diversity of the aquaporin gene family in arachnids

Abstract

Water flux across cells predominantly occurs through the pore formed by the aquaporin channels. Since water balance is one of the most important challenges to terrestrial animals, aquaporin evolution and diversity is known to play roles in animal terrestrialisation. Arachnids (Arthropoda: Chelicerata: Arachnida) are the second most diverse group and represent the pioneer land colonists in animals; however, there remains no thorough investigation on aquaporin evolution and diversity in this evolutionarily important lineage. Here we reported a phylogenetic study of aquaporin evolution and diversity using genomic data from 116 arachnid species covering almost all (15/16) extant orders. A previously unrecognised subfamily related to aquaporin-4 (i.e. Aqp4-like subfamily) via phylogenetic analysis was identified, suggesting certain underestimate of the arachnid aquaporin diversity in earlier studies probably due to limited taxonomic sampling. Further analysis indicates that this subfamily emerged deep within the life tree of arthropods. Gene tree of another Aqp4-like subfamily (PripL) shows an unexpected basal split between acariform mites (Acariformes) and other arachnids. A closer inspection demonstrated that the PripL evolved quickly and has been under differential selection pressure in acariform mites. Evidence is provided that the evolutionarily ancient Glp subfamily (i.e. aquaglyceroporin) is significantly expanded in terrestrial arachnids compared with their marine relatives. Finally, in spite of the phylogenetic diversity, there exists conservation of some exons in size, functional domain, and intron-insertion phase: an 81-bp and a 218-bp exon, respectively, in apq4-like and glp genes across Eumetazoa lineages including arachnids and human beings. Both exons encode the carboxyl-terminal NPA motif, implying the coding and splicing pressure during hundreds of million years of animal evolution. Hypotheses were tested to explore the possible link between these findings and arachnid terrestrialisation.

Keywords: Accelerated evolution; Adaptation; Exon conservation; Gene structure; Habitat transition; Major intrinsic protein.