Expression of Ion Transporter Genes in Gills and Intestine of Male and Female Gasterosteus aculeatus L. Three-Spined Sticklebacks during Freshwater Adaptation

Abstract

In euryhaline fish species, including the three-spined stickleback, a key physiological response to freshwater adaptation aimed at maintaining osmotic homeostasis is enhancement of ion uptake from the environment and reduction of ion loss. Hormone prolactin, a central regulator of this process, primarily targets gills and intestine. Our previous work demonstrated that in the model of freshwater adaptation in sticklebacks prolactin expression and sensitivity of osmoregulatory tissues to prolactin differ between the males and females. In the present study, we measured expression levels of the genes encoding α1a and α3a subunits of Na⁺/K⁺-ATPase, as well as ion transporters NKCC1a, NKCC2, NCC, and NHE2, in the gill and intestinal tissues of the male and female three-spined sticklebacks (Gasterosteus aculeatus L.) under conditions of acute (24 h) and chronic (72 h) freshwater adaptation, relative to the control conditions. During the freshwater adaptation, females, but not males, exhibited increased intestinal expression of nhe2 and atp1a3 genes (as well as of the ratio of atp1a1/atp1a3 expression), and the nkcc1a gene, along with the decreased expression of the nkcc2 gene. In contrast, only males showed increase in the ncc gene expression in the intestine. In both sexes, exposure to fresh water led to the significant decrease in the nkcc1a gene expression in the gills. These findings support our hypothesis of sex-dependent plasticity in osmoregulatory function in sticklebacks, with females exhibiting a more pronounced response. This pattern further aligns with the previously reported stronger activation of the prolactin axis in the females under freshwater adaptation conditions.