Genomic and anatomical comparisons of skin support independent adaptation to life in water by cetaceans and hippos

Springer, Mark S.; Guerrero‐Juarez, Christian F.; Huelsmann, Matthias; Collin, Matthew A.; Danil, Kerri; McGowen, Michael R.; Oh, Ji Won; Ramos, Raúl; Hiller, Michael; Plikus, Maksim V.; Gatesy, John

doi:10.1016/j.cub.2021.02.057

Cited by 34 publications

(50 citation statements)

References 118 publications

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“…To explore this possibility further, we scanned all available mammalian sequences including extant marine mammals. We found that both ALOX12B and ALOXE3 are also inactivated in extant cetaceans through gene loss (ALOX12B) and the accumulation of premature stop codons, deletions, or frameshifts (ALOXE3) but are active in pinnipeds (19,20), sea otter, polar bear, and extant sirenians (Fig. 2, A and B, and section SM3).…”

Section: Resultsmentioning

confidence: 87%

Genomic basis for skin phenotype and cold adaptation in the extinct Steller’s sea cow

et al. 2022

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Steller’s sea cow, an extinct sirenian and one of the largest Quaternary mammals, was described by Georg Steller in 1741 and eradicated by humans within 27 years. Here, we complement Steller’s descriptions with paleogenomic data from 12 individuals. We identified convergent evolution between Steller’s sea cow and cetaceans but not extant sirenians, suggesting a role of several genes in adaptation to cold aquatic (or marine) environments. Among these are inactivations of lipoxygenase genes, which in humans and mouse models cause ichthyosis, a skin disease characterized by a thick, hyperkeratotic epidermis that recapitulates Steller’s sea cows’ reportedly bark-like skin. We also found that Steller’s sea cows’ abundance was continuously declining for tens of thousands of years before their description, implying that environmental changes also contributed to their extinction.

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Section: Resultsmentioning

confidence: 87%

Genomic basis for skin phenotype and cold adaptation in the extinct Steller’s sea cow

et al. 2022

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“…At the genomic level, molecular evolutionary studies provide evidence for Tooth loss in mysticetes 3 both positive selection and extensive gene loss in association with the transition from land to water. These changes are linked to a variety of anatomical structures and organ systems that were modified in the ancestor of Cetacea including the skin, limbs, lungs, pineal gland, brain, brown fat, eyes, ears, vomeronasal organ, and nose (Gatesy et al, 2013;Nery et al, 2013;McGowen et al, 2014McGowen et al, , 2020bGaudry et al, 2017;Sharma et al, 2018;Huelsmann et al, 2019;Thermudo et al, 2020;Emerling et al, 2021;Springer and Gatesy, 2018;Springer et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Molecular Evolutionary Analyses of Tooth Genes Support Sequential Loss of Enamel and Teeth in Baleen Whales (Mysticeti)

Randall¹,

Gatesy

Springer³

2021

Preprint

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The loss of teeth and evolution of baleen racks in Mysticeti was a profound transformation that permitted baleen whales to radiate and diversify into a previously underutilized ecological niche of bulk filter-feeding on zooplankton and other small prey. Ancestral state reconstructions suggest that teeth were lost in the common ancestor of crown Mysticeti. Genomic studies provide some support for this hypothesis and suggest that the genetic toolkit for enamel production was inactivated in the common ancestor of living baleen whales. However, molecular studies to date have not provided direct evidence for the complete loss of teeth, including their dentin component, on the stem mysticete branch. Given these results, several questions remain unanswered: (1) Were teeth lost in a single step or did enamel loss precede dentin loss? (2) Was enamel lost early or late on the stem mysticete branch? (3) If enamel and dentin/tooth loss were decoupled in the ancestry of baleen whales, did dentin loss occur on the stem mysticete branch or independently in different crown mysticete lineages? To address these outstanding questions, we compiled and analyzed complete protein-coding sequences for nine tooth-related genes from cetaceans with available genome data. Seven of these genes are associated with enamel formation (ACP4, AMBN, AMELX, AMTN, ENAM, KLK4, MMP20) whereas two other genes are either dentin-specific (DSPP) or tooth-specific (ODAPH) but not enamel-specific. Molecular evolutionary analyses indicate that all seven enamel-specific genes have inactivating mutations that are scattered across branches of the mysticete tree. Three of the enamel genes (ACP4, KLK4, MMP20) have inactivating mutations that are shared by all mysticetes. The two genes that are dentin-specific (DSPP) or tooth-specific (ODAPH) do not have any inactivating mutations that are shared by all mysticetes, but there are shared mutations in Balaenidae as well as in Plicogulae (Neobalaenidae + Balaenopteroidea). These shared mutations suggest that teeth were lost at most two times. Shared inactivating mutations and dN/dS analyses, in combination with cetacean divergence times, were used to estimate inactivation times of genes and by proxy enamel and tooth phenotypes. The results of these analyses are most compatible with a two-step model for the loss of teeth in the ancestry of living baleen whales: enamel was lost very early on the stem Mysticeti branch followed by the independent loss of dentin (and teeth) in the common ancestors of Balaenidae and Plicogulae, respectively. These results imply that some stem mysticetes, and even early crown mysticetes, may have had vestigial teeth comprised of dentin with no enamel. Our results also demonstrate that all odontocete species (in our study) with absent or degenerative enamel have inactivating mutations in one or more of their enamel genes.

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“…Fig. S8 ), but a recent study estimated that KPRP was intact in the last common ancestor of Whippomorpha (cetaceans and hippopotamuses) 30 , 31 .…”

Section: Resultsmentioning

confidence: 93%

Gene duplications and gene loss in the epidermal differentiation complex during the evolutionary land-to-water transition of cetaceans

Holthaus

Lachner

Ebner

et al. 2021

Sci Rep

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Major protein components of the mammalian skin barrier are encoded by genes clustered in the Epidermal Differentiation Complex (EDC). The skin of cetaceans, i.e. whales, porpoises and dolphins, differs histologically from that of terrestrial mammals. However, the genetic regulation of their epidermal barrier is only incompletely known. Here, we investigated the EDC of cetaceans by comparative genomics. We found that important epidermal cornification proteins, such as loricrin and involucrin are conserved and subtypes of small proline-rich proteins (SPRRs) are even expanded in numbers in cetaceans. By contrast, keratinocyte proline rich protein (KPRP), skin-specific protein 32 (XP32) and late-cornified envelope (LCE) genes with the notable exception of LCE7A have been lost in cetaceans. Genes encoding proline rich 9 (PRR9) and late cornified envelope like proline rich 1 (LELP1) have degenerated in subgroups of cetaceans. These data suggest that the evolution of an aquatic lifestyle was accompanied by amplification of SPRR genes and loss of specific other epidermal differentiation genes in the phylogenetic lineage leading to cetaceans.

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Genomic and anatomical comparisons of skin support independent adaptation to life in water by cetaceans and hippos

Cited by 34 publications

References 118 publications

Genomic basis for skin phenotype and cold adaptation in the extinct Steller’s sea cow

Genomic basis for skin phenotype and cold adaptation in the extinct Steller’s sea cow

Molecular Evolutionary Analyses of Tooth Genes Support Sequential Loss of Enamel and Teeth in Baleen Whales (Mysticeti)

Gene duplications and gene loss in the epidermal differentiation complex during the evolutionary land-to-water transition of cetaceans

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