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In marine habitats, Atlantic salmon (Salmo salar) imbibe seawater (SW) to replace body water that is passively lost to the ambient environment. By desalinating consumed SW, the esophagus enables solute‐linked water absorption across the intestinal epithelium. The processes underlying esophageal desalination in salmon and their hormonal regulation during smoltification and following SW exposure are unresolved. To address this, we considered whether two Na⁺/H⁺exchangers (Nhe2 and −3) expressed in the esophagus contribute to the uptake of Na⁺from lumenal SW. There were no seasonal changes in esophagealnhe2or−3expression during smoltification; however,nhe3increased following 48 h of SW exposure in May. Esophagealnhe2, −3, andgrowth hormone receptor b1were elevated in smolts acclimated to SW for 2.5 weeks. Treatment with cortisol stimulated branchial Na⁺/K⁺‐ATPase (Nka) activity, andNa⁺/K⁺/2Cl⁻cotransporter 1(nkcc1),cystic fibrosis transmembrane regulator 1 (cftr1), andnka‐α1bexpression. Esophagealnhe2, but notnhe3expression, was stimulated by cortisol. In anterior intestine, cortisol stimulatednkcc2, cftr2, andnka‐α1b. Our findings indicate that salinity stimulates esophagealnhe2and−3, and that cortisol coordinates the expression of esophageal, intestinal, and branchial solute transporters to support the SW adaptability of Atlantic salmon.

Ecological transitions across salinity boundaries have led to some of the most important diversification events in the animal kingdom, especially among fishes. Adaptations accompanying such transitions include changes in morphology, diet, whole-organism performance, and osmoregulatory function, which may be particularly prominent since divergent salinity regimes make opposing demands on systems that maintain ion and water balance. Research in the last decade has focused on the genetic targets underlying such adaptations, most notably by comparing populations of species that are distributed across salinity boundaries. Here, we synthesize research on the targets of natural selection using whole-genome approaches, with a particular emphasis on the osmoregulatory system. Given the complex, integrated and polygenic nature of this system, we expected that signatures of natural selection would span numerous genes across functional levels of osmoregulation, especially salinity sensing, hormonal control, and cellular ion exchange mechanisms. We find support for this prediction: genes coding for V-type, Ca2+, and Na+/K+-ATPases, which are key cellular ion exchange enzymes, are especially common targets of selection in species from six orders of fishes. This indicates that while polygenic selection contributes to adaptation across salinity boundaries, changes in ATPase enzymes may be of particular importance in supporting such transitions.

It is unknown whether and how osmoregulation is controlled by corticosteroid signaling in the phylogenetically basal vertebrate group Agnatha, including lampreys and hagfishes. It is known that a truncated steroid biosynthetic pathway in lampreys produces two predominant circulating corticosteroids, 11-deoxycortisol (S) and 11-deoxycorticosterone (DOC). Furthermore, lampreys express only a single, ancestral corticosteroid receptor (CR). Whether S and/or DOC interact with the CR to control osmoregulation in lampreys is still unknown. We examined the role of the endogenous corticosteroids in vivo and ex vivo in sea lamprey (Petromyzon marinus) during the critical metamorphic period during which sea lamprey increase osmoregulatory capacity and acquire seawater (SW) tolerance. We demonstrate in vivo that increases in circulating [S] and gill CR abundance are associated with increases in osmoregulatory capacity during metamorphosis. We further show that in vivo and ex vivo treatment with S increases activity and expression of gill active ion transporters and improves SW tolerance, and that only S (and not DOC) has regulatory control over active ion transport in the gills. Lastly, we show that the lamprey CR expresses an ancestral, spironolactone-as-agonist structural motif and that spironolactone treatment in vivo increases osmoregulatory capacity. Together, these results demonstrate that S is an osmoregulatory hormone in lamprey and that receptor-mediated discriminative corticosteroid regulation of hydromineral balance is an evolutionarily basal trait among vertebrates.

Growth hormone receptor (GHR) and prolactin receptor (PRLR) in jawed vertebrates were thought to arise after the divergence of gnathostomes from a basal vertebrate. In this study we have identified two genes encoding putative GHR and PRLR in sea lamprey (Petromyzon marinus) and Arctic lamprey (Lethenteron camtschaticum), extant members of one of the oldest vertebrate groups, agnathans. Phylogenetic analysis revealed that lamprey GHR and PRLR cluster at the base of gnathostome GHR and PRLR clades, respectively. This indicates that distinct GHR and PRLR arose prior to the emergence of the lamprey branch of agnathans. In the sea lamprey, GHR and PRLR displayed a differential but overlapping pattern of expression; GHR had high expression in liver and heart tissues, whereas PRLR was expressed highly in the brain and moderately in osmoregulatory tissues. Branchial PRLR mRNA levels were significantly elevated by stage 5 of metamorphosis and remained elevated through stage 7, whereas levels of GHR mRNA were only elevated in the final stage (7). Branchial expression of GHR increased following seawater (SW) exposure of juveniles, but expression of PRLR was not significantly altered. The results indicate that GHR and PRLR may both participate in metamorphosis and that GHR may mediate SW acclimation.