Enamel Microstructure in Cetacea: a Case Study in Evolutionary Loss of Complexity

Werth, Alexander J.; Loch, Carolina; Fordyce, R. Ewan

doi:10.1007/s10914-019-09484-7

Cited by 12 publications

(58 citation statements)

References 79 publications

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“…Transitional branches have mixed evolutionary histories that include a period of evolution under purifying selection followed by a period of neutral evolution after selection was relaxed and the phenotype was lost (Meredith et al, 2009). DN/dS values on transitional branches are expected to be intermediate between dN/dS values for background branches and separated into two categories to determine if there is relaxed selection on these enamel genes in odontocetes with complex enamel, i.e., enamel with prismatic radial enamel that may also exhibit Hunter-Schreger bands (HSB) or other decussations (Werth et al, 2020). DN/dS analyses with the dentin genes included three branch categories: #0 background terrestrial cetartiodactyl outgroups plus stem and crown Odontoceti, #1 stem Mysticeti + stem Balaenidae, #2 crown Balaenidae.…”

Section: Selection Analysesmentioning

confidence: 99%

“…Complete coding sequences for all genes were recovered for all the non-cetacean cetartiodactyl outgroup taxa that were sampled, as well as for all odontocete species except for the dwarf and pygmy sperm whales (Kogia spp.) that lack well-developed enamel (Bianucci and Landini, 2006;Werth et al, 2020). Mysticetes that were sampled had varying degrees of completeness for the coding sequences of the nine tooth genes (ACP4, AMBN, AMELX, AMTN, DSPP, ENAM, KLK4, MMP20, ODAPH).…”

Section: Alignments and Gene Treesmentioning

confidence: 99%

“…Tooth loss in mysticetes 15 of Orcinus orca (killer whale), all of the inactivating mutations are in odontocetes that lack complex enamel with well-developed prisms (sensu Werth et al, 2020) and whose enamel (if present) is often worn away in adults. Non-delphinid odontocetes with inactivating mutations in enamel genes include two monodontids (Monodon monoceros, Delphinapterus leucas), two phocoenids (Neophocaena asiaeorientalis, Phocoena phocoena), one ziphiid (Mesoplodon bidens), and three physeteroids (Physeter macrocephalus, Kogia breviceps, K. sima).…”

Section: Inactivating Mutations In Odontocetesmentioning

confidence: 99%

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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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Section: Selection Analysesmentioning

confidence: 99%

Section: Alignments and Gene Treesmentioning

confidence: 99%

Section: Inactivating Mutations In Odontocetesmentioning

confidence: 99%

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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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“…Degeneracy/"devolution": The loss of complex enamel structure (typical of nearly all non-cetacean mammals) is likely linked to the loss of dental function (typical mammalian mastication) in odontocetes; this loss of complexity appears to be an example of "devolution" [94,95]. Because such losses represent potential decline of reversal of evolution, they are often referred to as degeneracy.…”

Section: Examples Of Evolutionary Terms and Conceptsmentioning

confidence: 99%

“…Evolution of complexity: Just as the loss of odontocete enamel relates to loss of complex structure and function, the evolution of echolocation and vocalizing structures and behaviors in various cetaceans relates to the gain of complexity [33,36,95,110,111], as does the origin and evolution of baleen.…”

Section: Examples Of Evolutionary Terms and Conceptsmentioning

confidence: 99%

Cetaceans as Exemplars of Evolution and Evolutionary Ecology: A Glossary

Werth

2020

Oceans

Self Cite

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Extant cetaceans (whales, dolphins, and porpoises) and their extinct ancestors offer some of the strongest and best-known examples of macroevolutionary transition as well as microevolutionary adaptation. Unlike most reviews of cetacean evolution, which are intended to chronicle the timeline of cetacean ancestry, document the current knowledge of cetacean adaptations, or simply validate the brute fact of evolution, this review is instead intended to demonstrate how cetaceans fittingly illustrate hundreds of specific, detailed terms and concepts within evolutionary biology and evolutionary ecology. This review, arrayed in alphabetical glossary format, is not meant to offer an exhaustive listing of case studies or scholarly sources, but aims to show the breadth and depth of cetacean research studies supporting and investigating numerous evolutionary themes.

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Morphological characteristics of the unique periodontal structure in dolphins

Kodera,

Kajinishi,

Uekusa

et al. 2024

The Anatomical Record

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Although toothed whales have dentition peculiar to mammals, little attention has been paid to the periodontal tissues that support these characteristic teeth. In this study, we clarified the anatomical characteristics of the periodontal tissue in several species of Delphinidae through three‐dimensional observation using micro‐computed tomography, histological observations using decalcified sections, and immunohistochemical analysis. The results indicated that the teeth and the periodontal tissues of dolphins are morphologically unique among mammals. The alveolar bone was both crude and spongy. The lamina dura, a radiopaque line observed in the alveolar bone of common mammals, was thin in dolphins, and the teeth were attached to the trabeculae with the periodontal ligament (PDL). The alveolar sockets were massive for the size of the teeth. The PDL, a collagen fiber that fills the periodontal space, was well‐developed and peculiarly divided into two layers. The inner layer fibers radially spread out from the cementum, similar to the PDL in common mammals. However, the outer layer fibers penetrate the spongy bone in a complicated manner. The interstitial space between the inner and outer layers contained nerve fiber bundles that were thicker than those found in the PDL of other mammals. Sensory receptor‐like structures were observed at the terminal ends of the nerve fibers. These findings indicated that the dolphin PDL is more sensitive to dental stimuli than those of other mammals, suggesting that the dolphin dentition plays a functional role as a sensory receptor, similar to tactile hair.

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Enamel Microstructure in Cetacea: a Case Study in Evolutionary Loss of Complexity

Cited by 12 publications

References 79 publications

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

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

Cetaceans as Exemplars of Evolution and Evolutionary Ecology: A Glossary

Morphological characteristics of the unique periodontal structure in dolphins

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