Molecular Evidence for Relaxed Selection on the Enamel Genes of Toothed Whales (Odontoceti) with Degenerative Enamel Phenotypes
Abstract
:1. Introduction
2. Materials and Methods
2.1. Gene Sampling
2.2. Taxon Sampling
2.3. BLAST Searches and Procurement of Molecular Data
2.4. Alignments and Inactivating Mutations
2.5. Phylogenetic Analyses
2.6. Collection of Data for Enamel Complexity
2.7. Species Trees
2.8. Ancestral Reconstructions of Enamel Complexity
2.9. Selection Analyses
2.10. Statistical Analyses
3. Results
3.1. Alignments and Gene Trees
3.2. Inactivating Mutations
3.3. Selection Analyses
3.4. Correlation and Regression Analyses
4. Discussion
4.1. Inactivating Mutations in Enamel Genes
4.2. Enamel Degeneration in Phocoenidae
4.3. Enamel Degeneration in Monodontidae
4.4. Enamel Degeneration in Physeteroidea
4.5. Enamel Degeneration in Ziphiidae
4.6. Conclusions and Future Directions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Odontoceti | ||
---|---|---|
Family | Species | Common Name |
Delphinidae | Cephalorhynchus commersonii | Commerson’s dolphin |
Delphinidae | Cephalorhynchus eutropia | Black dolphin/Chilean dolphin |
Delphinidae | Cephalorhynchus heavisidii | Heaviside’s dolphin |
Delphinidae | Cephalorhynchus hectori | Hector’s dolphin |
Delphinidae | Delphinus delphis bairdii | Long-beaked common dolphin |
Delphinidae | Delphinus delphis delphis | Short-beaked dolphin |
Delphinidae | Feresa attenuata | Pygmy killer whale |
Delphinidae | Globicephala macrorhynchus | Short-finned pilot whale |
Delphinidae | Globicephala melas | Long-finned pilot whale |
Delphinidae | Grampus griseus | Risso’s dolphin |
Delphinidae | Lagenodelphis hosei | Fraser’s dolphin |
Delphinidae | Lagenorhynchus albirostris | White-beaked dolphin |
Delphinidae | Leucopleurus acutus | Atlantic white-sided dolphin |
Delphinidae | Lissodelphis borealis | Northern right whale dolphin |
Delphinidae | Lissodelphis peronii | Southern right whale dolphin |
Delphinidae | Orcaella brevirostris | Irrawaddy dolphin |
Delphinidae | Orcaella heinsohni | Australian snubfin dolphin |
Delphinidae | Orcinus orca | Killer whale |
Delphinidae | Peponocephala electra | Melon-headed whale |
Delphinidae | Pseudorca crassidens | False killer whale |
Delphinidae | Sagmatiasobliquidens | Pacific white-sided dolphin |
Delphinidae | Sagmatias obscurus | Dusky dolphin |
Delphinidae | Sousa chinensis | Indo-Pacific humpback dolphin |
Delphinidae | Stenella attenuata | Pantropical spotted dolphin |
Delphinidae | Stenella clymene | Clymene dolphin |
Delphinidae | Stenella coeruleoalba | Striped dolphin |
Delphinidae | Stenella frontalis | Atlantic spotted dolphin |
Delphinidae | Stenella longirostris | Eastern spinner dolphin |
Delphinidae | Steno bredanensis | Rough-toothed dolphin |
Delphinidae | Tursiops aduncus | Indo-Pacific bottlenose dolphin |
Delphinidae | Tursiops truncatus | Common bottlenose dolphin |
Iniidae | Inia geoffrensis | Amazon River dolphin |
Kogiidae | Kogia breviceps | Pygmy sperm whale |
Kogiidae | Kogia sima | Dwarf sperm whale |
Lipotidae | Lipotes vexillifer | Chinese river dolphin/baiji |
Monodontidae | Delphinapterus leucas | Beluga |
Monodontidae | Monodon monoceros | Narwhal |
Phocoenidae | Neophocaena asiaeorientalis | Yangtze finless porpoise |
Phocoenidae | Phocoena phocoena | Harbor porpoise |
Phocoenidae | Phocoena sinus | Vaquita |
Physeteridae | Physeter macrocephalus | Sperm whale |
Platanistidae | Platanista gangetica | Ganges River dolphin |
Platanistidae | Platanista minor | Indus River dolphin |
Pontoporiidae | Pontoporia blainvillei | Franciscana/La Plata dolphin |
Ziphiidae | Berardius arnuxii | Arnoux’s beaked whale |
Ziphiidae | Berardius bairdii | Baird’s beaked whale |
Ziphiidae | Hyperoodon ampullatus | Northern bottlenose whale |
Ziphiidae | Hyperoodon planifrons | Southern bottlenose whale |
Ziphiidae | Indopacetus pacificus | Tropical bottlenose whale |
Ziphiidae | Mesoplodon bidens | Sowerby’s beaked whale |
Ziphiidae | Mesoplodon bowdoini | Andrew’s beaked whale |
Ziphiidae | Mesoplodon carlhubbsi | Hubb’s beaked whale |
Ziphiidae | Mesoplodon densirostris | Blainville’s beaked whale |
Ziphiidae | Mesoplodon europaeus | Gervais’ beaked whale |
Ziphiidae | Mesoplodon ginkgodens | Ginkgo-toothed beaked whale |
Ziphiidae | Mesoplodon grayi | Gray’s beaked whale |
Ziphiidae | Mesoplodon layardii | Strap-toothed whale |
Ziphiidae | Mesoplodon mirus | True’s beaked whale |
Ziphiidae | Mesoplodon perrini | Perrin’s beaked whale |
Ziphiidae | Mesoplodon peruvianus | Pygmy beaked whale |
Ziphiidae | Mesoplodon stejnegeri | Stejneger’s beaked whale |
Ziphiidae | Tasmacetus shepherdi | Shepherd’s beaked whale |
Ziphiidae | Ziphius cavirostris | Cuvier’s beaked whale |
Mysticeti | ||
Balaenidae | Balaena mysticetus | Bowhead whale |
Balaenidae | Eubalaena australis | Southern right whale |
Balaenidae | Eubalaena glacialis | North Atlantic right whale |
Balaenidae | Eubalaena japonica | North Pacific right whale |
Balaenopteridae | Balaenoptera acutorostrata | Common minke whale |
Balaenopteridae | Balaenoptera bonaerensis | Antarctic minke whale |
Balaenopteridae | Balaenoptera borealis | Sei whale |
Balaenopteridae | Balaenoptera musculus | Blue whale |
Balaenopteridae | Balaenoptera physalus | Fin whale |
Balaenopteridae | Balaenoptera ricei | Rice’s whale |
Balaenopteridae | Megaptera novaeangliae | Humpback whale |
Eschrichtiidae | Eschrichtus robustus | Gray whale |
Neobalaenidae | Caperea marginata | Pygmy right whale |
Terrestrial and Semiaquatic Cetartiodactyl Outgroups | ||
Bovidae | Bison bison | American bison |
Bovidae | Bos taurus | Wild yak |
Bovidae | Bubalus bubalis | Water buffalo |
Bovidae | Capra hircus | Domestic goat |
Bovidae | Ovis aries | Domestic sheep |
Camelidae | Camelus bactrianus | Bactrian camel |
Camelidae | Vicugna pacos | Alpaca |
Cervidae | Elaphurus davidianus | Pere David’s deer |
Cervidae | Odocoileus virginianus | White-tailed deer |
Giraffidae | Giraffa camelopardalis | Giraffe |
Giraffidae | Okapia johnstoni | Okapi |
Hippopotamidae | Choeropsis liberiensis | Pygmy hippopotamus |
Hippopotamidae | Hippopotamus amphibius | River hippopotamus |
Moschidae | Moschus moschiferus | Siberian musk deer |
Suidae | Sus scrofa | Wild boar |
Tayassuidae | Catagonus wagneri | Chacoan peccary |
Tragulidae | Tragulus javanicus | Java mouse-deer |
Odontoceti Species | Werth Enamel Complexity |
---|---|
Berardius bairdii | 2 |
Cephalorhynchus hectori | 4 |
Delphinapterus leucas | 2.5 (2/3) |
Delphinus delphis bairdii | 4 |
Delphinus delphis delphis | 4 |
Globicephala macrorhynchus | 4 |
Globicephala melas | 4 |
Grampus griseus | 4 |
Inia geoffrensis | 5 |
Kogia breviceps | 2 |
Kogia sima | 2 * |
Lagenodelphis hosei | 4 |
Leucopleurus acutus | 4 |
Lagenorhynchus albirostris | 4 |
Sagmatias obscurus | 4 |
Mesoplodon densirostris | 1.5 (1/2) |
Monodon monoceros | 1 * |
Neophocaena asiaeorientalis | 3 * |
Orcaella brevirostris | 4 |
Orcinus orca | 4 |
Phocoena phocoena | 3 |
Physeter macrocephalus | 1.5 (1/2) |
Platanista gangetica | 5 |
Platanista minor | 5 * |
Pontoporia blainvillei | 4 |
Pseudorca crassidens | 4 |
Stenella attenuata | 4 |
Stenella clymene | 4 |
Stenella coeruleoalba | 4 |
Stenella frontalis | 4 |
Steno bredanensis | 4 |
Tursiops truncatus | 4 |
Ziphius cavirostris | 1 |
Outgroups | |
Bos mutus | 5 * |
Camelus bactrianus | 5 * |
Hippopotamus amphibius | 5 * |
Sus scrofa | 5 * |
Odontoceti Taxon | Enamel Gene and Mutation |
---|---|
Kogiidae (K. breviceps + K. sima) | ACP4: E1-3, 11: NBR/NRM; AMELX: E2: 47I, In2Do:GG; ENAM: E8: 2403D, 3751-3752D; KLK4: WGD (NBR/NRM) |
Phocoenidae (N. asiaeorientalis + P. phocoena + P. sinus) | AMTN: In2Ac:AT; KLK4: E2: 73-75S |
Plastanista (P. gangetica + P. minor) | AMTN: E3: NBR |
Hyperoodon (H. ampullatus + H. planifrons) | AMTN: E8: 566D |
Monodontidae (D. leucas + M. monoceros) | AMELX: In2Do: AT |
Berardius arnuxii | AMELX: E7: NBR/NRM; ENAM: E8: 648I |
Berardius bairdii | MMP20: E5:1095-1097S |
Delphinapterus leucas | ACP4: E7: 674D; AMTN: E8: 576D |
Hyperoodon ampullatus | ENAM: In6Do: TT |
Hyperoodon planifrons | AMELX: E7: NBR/NRM |
Kogia breviceps | ACP4: E9: 900D; E10: 1100I; AMBN: In7Ac: AT; In9Ac: AT; AMELX: E2: SCM; AMTN: E8: 377D; ENAM: In6Do: CT |
Kogia sima | AMBN: WGD (NBR/NRM); ENAM: E1-6: NBR/NRM |
Mesoplodon bidens | ACP4: E2: 145-148I, E5: 537-544D, In8Ac: GG |
Mesoplodon densirostris | ACP4: E5: 537-539S (allelic variation); AMTN: E5: 249-252I (allelic variation) |
Mesoplodon grayi | ACP4: E8: 802I (allelic variation); AMELX: In2Ac: GG/AG (allelic variation) |
Mesoplodon layardii | KLK4: In2Do: CG/GT (allelic variation) |
Mesoplodon perrini | AMTN: E8-9: NRM (no stop) |
Mesoplodon peruvianus | AMELX: E7: NBR/NRM; AMTN: E8: 376I |
Monodon monoceros | ACP4: In6Do: AT; AMBN: E11: 1214-1216S; KLK4: E4: 503-505S |
Orcinus orca | ENAM: In4Do: AT/GT (allelic variation) |
Physeter macrocephalus | ACP4: E4: 427D; E9: 1015D; E10: 1132D (allelic variation) |
Tasmacetus shepherdi | KLK4: E5: 767-769TCM |
Ziphius cavirostris | KLK4: In3Ac: GG |
X | Y | Rho | p Value * |
---|---|---|---|
Mutations/MYRs | ACCTRAN | −0.60348 | 2.01199 × 10-8 |
Mutations/MYRs | DELTRAN | −0.59215 | 4.28415 × 10-8 |
Mutations/MYRs | MPR | −0.59544 | 3.44991 × 10-8 |
dN/dS CF1 | ACCTRAN | −0.53289 | 2.80955 × 10-5 |
dN/dS CF2 | ACCTRAN | −0.53113 | 3.01979 × 10-5 |
dN/dS CF1 | DELTRAN | −0.51396 | 5.98125 × 10-5 |
dN/dS CF2 | DELTRAN | −0.51202 | 6.44745 × 10-5 |
dN/dS CF1 | MPR | −0.52024 | 4.67864 × 10-5 |
dN/dS CF2 | MPR | −0.51842 | 5.02687 × 10-5 |
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Randall, J.G.; Gatesy, J.; McGowen, M.R.; Springer, M.S. Molecular Evidence for Relaxed Selection on the Enamel Genes of Toothed Whales (Odontoceti) with Degenerative Enamel Phenotypes. Genes 2024, 15, 228. https://doi.org/10.3390/genes15020228
Randall JG, Gatesy J, McGowen MR, Springer MS. Molecular Evidence for Relaxed Selection on the Enamel Genes of Toothed Whales (Odontoceti) with Degenerative Enamel Phenotypes. Genes. 2024; 15(2):228. https://doi.org/10.3390/genes15020228
Chicago/Turabian StyleRandall, Jason G., John Gatesy, Michael R. McGowen, and Mark S. Springer. 2024. "Molecular Evidence for Relaxed Selection on the Enamel Genes of Toothed Whales (Odontoceti) with Degenerative Enamel Phenotypes" Genes 15, no. 2: 228. https://doi.org/10.3390/genes15020228
APA StyleRandall, J. G., Gatesy, J., McGowen, M. R., & Springer, M. S. (2024). Molecular Evidence for Relaxed Selection on the Enamel Genes of Toothed Whales (Odontoceti) with Degenerative Enamel Phenotypes. Genes, 15(2), 228. https://doi.org/10.3390/genes15020228