Osmoregulatory evolution of gills promoted salinity adaptation following the sea-land transition of crustaceans.

Abstract

The sea-land transition is one of the most dramatic evolutionary changes and requires an adaptive genetic response to salinity changes and osmotic stress. Here, we used multi-species genomes and multi-tissue transcriptomes of the talitrid crustaceans, a living sea-land transition model, to investigate the adaptive genetic changes and osmoregulatory organs that facilitated their salinity adaptation. Genomic analyses detected numerous osmoregulatory genes in terrestrial talitrids undergoing gene family expansions and positive selection. Gene expression comparisons among species and tissues confirmed the gill being the primary organ responsible for ion transport and identified the genetic expression variation that enable talitrids to adapt to marine and land habitats. V-type H⁺-ATPases related to H⁺ transport play a crucial role in land adaptations, while genes related to the transport of inorganic ions (Na⁺, K⁺, Cl^-) are upregulated in marine habitats. Our results demonstrate that talitrids have divergent genetic responses to salinity change that led to the uptake or excretion of ions in the gills and promoted habitat adaptation. These findings suggest that detecting gene expression changes in talitrids presents promising potential as a biomarker for salinity monitoring.

Supplementary information: The online version contains supplementary material available at 10.1007/s42995-025-00298-6.