Decay of TRPV3 as the genomic trace of epidermal structure changes in the land‐to‐sea transition of mammals

Abstract

The epidermis plays an indispensable barrier function in animals. Some species have evolved unique epidermal structures to adapt to different environments. Aquatic and semi‐aquatic mammals (cetaceans, manatees, and hippopotamus) are good models to study the evolution of epidermal structures because of their exceptionally thickened stratum spinosum, the lack of stratum granulosum, and the parakeratotic stratum corneum. This study aimed to analyze an upstream regulatory gene transient receptor potential cation channel, subfamily V, member 3 (TRPV3) of epidermal differentiation so as to explore the association between TRPV3 evolution and epidermal changes in mammals. Inactivating mutations were detected in almost all the aquatic cetaceans and several terrestrial mammals. Relaxed selective pressure was examined in the cetacean lineages with inactivated TRPV3, which might contribute to its exceptionally thickened stratum spinosum as the significant thickening of stratum spinosum in TRPV3 knock‐out mouse. However, functional TRPV3 may exist in several terrestrial mammals due to their strong purifying selection, although they have “inactivating mutations.” Further, for intact sequences, relaxed selective constraints on the TRPV3 gene were also detected in aquatic cetaceans, manatees, and semi‐aquatic hippopotamus. However, they had intact TRPV3, suggesting that the accumulation of inactivating mutations might have lagged behind the relaxed selective pressure. The results of this study revealed the decay of TRPV3 being the genomic trace of epidermal development in aquatic and semi‐aquatic mammals. They provided insights into convergently evolutionary changes of epidermal structures during the transition from the terrestrial to the aquatic environment.

Decay of Skin-Specific Gene Modules in Pangolins

“…The evolution of mammals entailed some tantalizing lifestyle variations. Ecological transitions such as subterranean burrowing, powered flight, or obligate aquatic regimes, elaborated from prominent eco-physiological adaptations, notably in the skin (Themudo et al 2020 ; Wu et al 2022 ; Christmas et al 2023 ). Some of these skin-phenotypic shifts were quite radical, as illustrated by the complete absence of glands and pelage in Cetacea skin (Fig.…”

The genome of African manatee Trichechus senegalensis reveals secondary adaptation to the aquatic environment

“…The epidermis acts as a stable environmental barrier and performs multiple protective functions for mammals, such as preventing water loss, resisting mechanical stresses, participating in immune responses, and so on. 25 Layers of the epidermis include the stratum basale, stratum spinosum, stratum granulosum, and stratum corneum, while the Sirenia and Cetacea species lack stratum granulosum. 2 The skin of manatees is completely cornified, with an extremely thick stratum corneum in which the cells of this layer lack nuclei, unlike the cetaceans, where cells in the stratum corneum retain nuclei and are not fully keratinized.…”

TRPV3 Ion Channel: From Gene to Pharmacology

“…Trpv3 knockout mice have a thickened stratum spinosum and defective stratum granulosum and stratum corneum [16], which is consistent with the cetacean phenotype. This assumes that trpv3 degradation is a genomic trace of epidermal development in aquatic and semiaquatic mammals [17].…”