Parallel duplication and loss of aquaporin-coding genes during the ‘out of the sea’ transition as potential key drivers of animal terrestrialization

Abstract

One of the most important physiological challenges animals had to overcome during terrestrialization (i.e., the transition from sea to land) is water loss, which alters their osmotic and hydric homeostasis. Aquaporins are a superfamily of membrane water transporters heavily involved in osmoregulatory processes. Their diversity and evolutionary dynamics in most animal lineages remain unknown, hampering our understanding of their role in marine-terrestrial transitions. Here, we interrogated aquaporin gene repertoire evolution across the main terrestrial animal lineages. We annotated aquaporin-coding genes in genomic data from 458 species from 7 animal phyla where terrestrialization episodes occurred. We then explored aquaporin gene evolutionary dynamics to assess differences between terrestrial and aquatic species through phylogenomics and phylogenetic comparative methods. Our results revealed parallel aquaporin-coding gene duplications in aquaporins transporting water, glycerol and ammonia in the transition from marine to non-marine environments (e.g., brackish, freshwater and terrestrial), rather than from aquatic to terrestrial ones, with some notable duplications in ancient lineages. Contrarily, we also recovered a significantly lower number of oxygen peroxide-transporting aquaporin-coding genes in terrestrial arthropods, suggesting that more efficient oxygen homeostasis in land arthropods might be linked to a reduction in this type of aquaporins. Our results thus indicate that aquaporin-coding gene duplication and loss might have been one of the key steps towards the evolution of osmoregulation across animals, facilitating the "out of the sea" transition and ultimately the colonisation of land.

Genomic innovation, convergence and parallelism facilitated the ecological transition to life out of the sea in molluscs

“…In this sense, among these orthogroups expanded in parallel we detected aquaporins (orthogroup OG0000253; Supplementary Table 2), a superfamily of membrane water and solute transporters such as glycerol or urea strongly involved in osmoregulation 26 . Moreover, this family was recently shown in a targeted analysis to have undergone parallel expansions across several non-marine animal phyla 27 , confirming the robustness of our methodological approach to detect such events. Moreover, a previous study based on a limited phylogenetic sampling suggested that a family of Zinc metalloproteinases with a potential role in reducing oxidative damage had expanded in the Stylommatophora gastropods ( 7).…”