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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. | |
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