Independent divergences of the aquaporins across different genera highlight the distinct adaptation mechanisms within Mytilida

Mussels are naturally distributed throughout ocean and freshwater ecosystems, with each species exhibiting distinct adaptive characteristics to dynamic environments. Aquaporins (AQPs) are essential selective transmembrane transport proteins that facilitate the permeation of water and other small solutes. These proteins play a significant role in maintaining metabolic homeostasis and supporting environmental adaptation via independent duplication and subsequent diversification. This study employs a comprehensive phylogenomic approach to uncover the original evolution and subsequent divergence of AQPs within the order Mytilida, a group that encompasses numerous mussel species. Utilizing genome-wide data from multiple organisms across different genera, our analysis revealed ancient foundational duplications that occurred in the last common ancestor of mussels and abundant subsequent lineage-specific expansions and diversifications following the divergence of different genera. Intriguingly, independent duplications of c-AQP orthologs primarily occurred in genera other than Mytilus. As a form of compensation, diversifications of the AQGP and AQP8 orthologs mainly occurred within the genus Mytilus. By integrating structural modeling, we provide insights into how the diversified amino acid compositions in the selective filters influence the inner-surface properties of the channel among duplicated paralogs. Moreover, comparative genomic analyses highlighted the role of presence/absence variations (PAVs) in promoting the further diversification of the AQP8 subfamily, presenting as adaptive genetic signatures among geographical distinct populations. These findings underscore the importance of ancestral gene duplication, subsequent functional diversification, and large-scale genomic variation in shaping the evolutionary success and ecological adaptability of mussel AQPs, particularly within the Mytilus genus.