Complete Inactivation of Sebum-Producing Genes Parallels the Loss of Sebaceous Glands in Cetacea

Abstract

Genomes are dynamic biological units, with processes of gene duplication and loss triggering evolutionary novelty. The mammalian skin provides a remarkable case study on the occurrence of adaptive morphological innovations. Skin sebaceous glands (SGs), for instance, emerged in the ancestor of mammals serving pivotal roles, such as lubrication, waterproofing, immunity, and thermoregulation, through the secretion of sebum, a complex mixture of various neutral lipids such as triacylglycerol, free fatty acids, wax esters, cholesterol, and squalene. Remarkably, SGs are absent in a few mammalian lineages, including the iconic Cetacea. We investigated the evolution of the key molecular components responsible for skin sebum production: Dgat2l6, Awat1, Awat2, Elovl3, Mogat3, and Fabp9. We show that all analyzed genes have been rendered nonfunctional in Cetacea species (toothed and baleen whales). Transcriptomic analysis, including a novel skin transcriptome from blue whale, supports gene inactivation. The conserved mutational pattern found in most analyzed genes, indicates that pseudogenization events took place prior to the diversification of modern Cetacea lineages. Genome and skin transcriptome analysis of the common hippopotamus highlighted the convergent loss of a subset of sebum-producing genes, notably Awat1 and Mogat3. Partial loss profiles were also detected in non-Cetacea aquatic mammals, such as the Florida manatee, and in terrestrial mammals displaying specialized skin phenotypes such as the African elephant, white rhinoceros and pig. Our findings reveal a unique landscape of “gene vestiges” in the Cetacea sebum-producing compartment, with limited gene loss observed in other mammalian lineages: suggestive of specific adaptations or specializations of skin lipids.

Molecular evolution of gland cell types and chemical interactions in animals

“…Although certain glands are conserved across large, ancient taxonomic groupsmammary glands and insect oenocytes being examples (Blomquist and Bagneres, 2010;Chung and Carroll, 2015;Makki et al, 2014;Oftedal, 2002) such examples are few, and are dwarfed by the myriad unique exocrine glands common only to specific taxa of lower rank (Blum, 1996; http:// www.pherobase.com). Moreover, even highly conserved glands can be subject to repeated loss, as evidenced by the absence of mammalian sebaceous glands in cetaceans, hippos, elephants and naked mole rats (Lopes-Marques et al, 2019).…”

The dopamine receptor D5gene shows signs of independent erosion in toothed and baleen whales

“…Reductive episodes have been widely documented across the tree of life contributing to organismal divergence and physiological and morphological adaptation to environmental cues (Albalat & Cañestro, 2016; Braun, 2003; Jeffery, 2009; Olson, 1999). In agreement, gene loss mechanisms seem pervasive in lineages that endured drastic habitat transitions in the course of evolution, such as Cetacea, entailing niche-specific adaptations (Huelsmann et al, 2019; Lachner et al, 2017; Lopes-Marques et al, 2018; Lopes-Marques et al, 2019a; McGowen, Gatesy & Wildman, 2014; Nery, Arroyo & Opazo, 2014; Sharma et al, 2018; Strasser et al, 2015). Thus, our findings suggest that these species are natural KOs for this dopamine receptor and might offer valuable insights into the mechanisms of some forms of essential hypertension.…”

Losing Genes: The Evolutionary Remodeling of Cetacea Skin

“…This is particularly relevant in the context of gene loss and the unique phenotype adaptations of Cetacea. Recently, a surge of studies has specifically demonstrated the relevance of disabling mutations in the coding region of genes as a source of adaptive success in land to water habitat transitions (e.g., Meyer et al, 2018;Huelsmann et al, 2019;Lopes-Marques et al, 2019b). This evolutionary trend of gene reduction has been particularly prevalent in the gene families involved in skin physiology (Figure 1), with a minimum of 36 described events of gene inactivation, and strongly correlate with specific Cetacea phenotypic traits (e.g., keratins and absence of pelage).…”