The olfactory receptor gene repertoires in secondary-adapted marine vertebrates: evidence for reduction of the functional proportions in cetaceans

Abstract

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.

Somatosensation, Echolocation, and Underwater Sniffing: Adaptations Allow Mammals Without Traditional Olfactory Capabilities to Forage for Food Underwater

“…Functional olfactory receptor gene repertoires were reduced independently in the multiple origins of aquatic mammals (Niimura, 2009). Semiaquatic mammals, on the other hand, have variably maintained their olfactory receptor genes and olfactory structures (Kishida et al, 2007). For instance, while Trichechus manatus (West Indian manatee) displays evidence of a rudimentary olfactory system (Mackay-Sim et al, 1985), seals have a main olfactory bulb and an accessory olfactory bulb associated with a vomeronasal organ (Freitag et al, 1998).…”

“…Members of the order Cetacea either have rudimentary olfactory systems, or lack an olfactory system altogether (Tyack, 2000). Kishida et al (2007) demonstrated that members of Cetacea, including the dwarf sperm whale (Kogia sima), Dall's porpoise (Phocoenoides dalli), and the Minke whale (Balaenoptera acutorostrata) all have a significantly higher number of non-functional olfactory receptor pseudogenes than their close terrestrial relatives. This suggests a diminished role of olfaction, as the number of pseudogenes is inversely proportional to olfactory functionality.…”

Evolution of GPCR: Change and continuity

“…Some studies have tried to infer causalities, for example the loss of olfactory GPCR [95] in response to the advent of trichromatic vision in primates [96]. Large scale degeneration of olfactory GPCR genes is found in cetaceans (dolphins, whales), which have secondarily adapted to a marine habitat and have lost or greatly reduced their sense of smell acquired in terrestrial environments [97]. Taken together, using phylogenetic data, it is difficult to prove how variation of a gene has generated an evolutionary advantage under certain environmental circumstances.…”

Sensory Perception in Cetaceans: Part I—Current Knowledge about Dolphin Senses As a Representative Species

“…In bowhead whales (Balaena mysticetus), a complex olfactory bulb and olfactory tracts are present and more than half of the OR genes are intact, suggesting a potentially functional sense of smell (Thewissen et al, 2011;Kishida et al, 2015a). However, OR genes are reported to be functionally reduced by pseudogenization in Odontoceti (Kishida et al, 2007). Bottlenose dolphins possess only two class I and ten class II OR genes that are intact, as well as a single vomeronasal receptor type 1 gene (Kishida et al, 2015b).…”