IntroductionWhile olfaction is one of the most important senses in most terrestrial mammals, it is absent in modern toothed whales (Odontoceti, Cetacea). Furthermore, behavioral evidence suggests that gustation is very limited. In contrast, their aquatic sistergroup, baleen whales (Mysticeti) retain small but functional olfactory organs, and nothing is known about their gustation. It is difficult to investigate mysticete chemosensory abilities because experiments in a controlled setting are impossible.ResultsHere, we use the functional regionalization of the olfactory bulb (OB) to identify the loss of specific olfactory functions in mysticetes. We provide the whole-genome sequence of a mysticete and show that mysticetes lack the dorsal domain of the OB, an area known to induce innate avoidance behavior against odors of predators and spoiled foods. Genomic and fossil data suggest that mysticetes lost the dorsal domain of the OB before the Odontoceti-Mysticeti split. Furthermore, we found that all modern cetaceans are revealed to have lost the functional taste receptors.ConclusionThese results strongly indicate that profound changes in the chemosensory capabilities had occurred in the cetacean lineage during the period when ancestral whales migrated from land to water.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-014-0002-z) contains supplementary material, which is available to authorized users.
An olfactory receptor (OR) multigene family is responsible for the well-developed sense of smell possessed by terrestrial tetrapods. Mammalian OR genes had diverged greatly in the terrestrial environment after the fish-tetrapod split, indicating their importance to land habitation. In this study, we analysed OR genes of marine tetrapods (minke whale Balaenoptera acutorostrata, dwarf sperm whale Kogia sima, Dall's porpoise Phocoenoides dalli, Steller's sea lion Eumetopias jubatus and loggerhead sea turtle Caretta caretta) and revealed that the pseudogene proportions of OR gene repertoires in whales were significantly higher than those in their terrestrial relative cattle and also in sea lion and sea turtle. On the other hand, the pseudogene proportion of OR sequences in sea lion was not significantly higher compared with that in their terrestrial relative (dog). It indicates that secondary perfectly adapted marine vertebrates (cetaceans) have lost large amount of their OR genes, whereas secondarysemi-adapted marine vertebrates (sea lions and sea turtles) still have maintained their OR genes, reflecting the importance of terrestrial environment for these animals.
Although there are several isolated references to the olfactory anatomy of mysticetes, it is usually thought that olfaction is rudimentary in this group. We investigated the olfactory anatomy of bowhead whales and found that these whales have a cribriform plate and small, but histologically complex olfactory bulb. The olfactory bulb makes up approximately 0.13% of brain weight, unlike odontocetes where this structure is absent. We also determined that 51% of olfactory receptor genes were intact, unlike odontocetes, where this number is less than 25%. This suggests that bowheads have a sense of smell, and we speculate that they may use this to find aggregations of krill on which they feed.
Carnivora is a successful taxon in terms of dietary diversity. We investigated the dietary adaptations of carnivoran dentition and the developmental background of their dental diversity, which may have contributed to the success of the lineage. A developmental model was tested and extended to explain the unique variability and exceptional phenotypes observed in carnivoran dentition. Carnivorous mammalian orders exhibited two distinct patterns of dietary adaptation in molars and only Carnivora evolved novel variability, exhibiting a high correlation between relative molar size and the shape of the first molar. Studies of Bmp7-hetero-deficient mice, which may exhibit lower Bmp7 expression, suggested that Bmp7 has pleiotropic effects on these two dental traits. Its effects are consistent with the pattern of dietary adaptation observed in Carnivora, but not that observed in other carnivorous mammals. A molecular evolutionary analysis revealed that Bmp7 sequence evolved by natural selection during ursid evolution, suggesting that it plays an evolutionary role in the variation of carnivoran dentition. Using mouse experiments and a molecular evolutionary analysis, we extrapolated the causal mechanism of the hitherto enigmatic ursid dentition (larger M2 than M1 and M3). Our results demonstrate how carnivorans acquired novel dental variability that benefits their dietary divergence.
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