Abstract
BackgroundMarine mammals are well adapted to their hyperosmotic environment. Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance. However, most previous studies have focused on the unique renal physiology of marine mammals, but the molecular bases of these mechanisms remain poorly explored. Many genes have been identified to be involved in osmotic regulation, including the aquaporins. Considering that aquaporin genes were potentially subject to strong selective pressure, the aim of this study was to analyze the molecular evolution of seven aquaporin genes (AQP1, AQP2, AQP3, AQP4, AQP6, AQP7, and AQP9) comparing the lineages of cetaceans and terrestrial mammals.ResultsOur results demonstrated strong positive selection in cetacean-specific lineages acting only in the gene for AQP2 (amino acids 23, 83, 107,179, 180, 181, 182), whereas no selection was observed in terrestrial mammalian lineages. We also analyzed the changes in the 3D structure of the aquaporin 2 protein. Signs of strong positive selection in AQP2 sites 179, 180, 181, and 182 were unexpectedly identified only in the baiji lineage, which was the only river dolphin examined in this study. Positive selection in aquaporins AQP1 (45), AQP4 (74), AQP7 (342, 343, 356) was detected in cetaceans and artiodactyls, suggesting that these events are not related to maintaining water and electrolyte homeostasis in seawater.ConclusionsOur results suggest that the AQP2 gene might reflect different selective pressures in maintaining water balance in cetaceans, contributing to the passage from the terrestrial environment to the aquatic. Further studies are necessary, especially those including other freshwater dolphins, who exhibit osmoregulatory mechanisms different from those of marine cetaceans for the same essential task of maintaining serum electrolyte balance.
Highlights
The transition from the terrestrial to the aquatic environment occurred in the evolutionary process of cetaceans, resulting in notable and distinct morphological and physiological changes, fundamental to survival in an exclusively aquatic environment [1,2,3,4,5]
Our results demonstrated strong positive selection in cetacean-specific lineages acting only in the gene for AQP2, whereas no selection was observed in terrestrial mammalian lineages
Positive selection in aquaporins AQP1 (45), AQP4 (74), AQP7 (342, 343, 356) was detected in cetaceans and artiodactyls, suggesting that these events are not related to maintaining water and electrolyte homeostasis in seawater
Summary
The transition from the terrestrial to the aquatic environment occurred in the evolutionary process of cetaceans, resulting in notable and distinct morphological and physiological changes, fundamental to survival in an exclusively aquatic environment [1,2,3,4,5]. Morphological characteristics of the kidneys, such as a relatively large size when compared with those of other mammals, and hundreds of individual lobes, or reniculi [7,8,9], are associated with the ability to retain water. They exhibit increased medullary thickness, necessary to produce a highly concentrated urine, resulting in excretion of the excess salt from food and ingested seawater, reducing water loss [4,10,11,12]. Considering that aquaporin genes were potentially subject to strong selective pressure, the aim of this study was to analyze the molecular evolution of seven aquaporin genes (AQP1, AQP2, AQP3, AQP4, AQP6, AQP7, and AQP9) comparing the lineages of cetaceans and terrestrial mammals
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