Convergent degeneration of olfactory receptor gene repertoires in marine mammals

Abstract

Background: Olfactory receptors (ORs) can bind odor molecules and play a crucial role in odor sensation. Due to the frequent gains and losses of genes during evolution, the number of OR members varies greatly among different species. However, whether the extent of gene gains/losses varies between marine mammals and related terrestrial mammals has not been clarified, and the factors that might underlie these variations are unknown. Results: To address these questions, we identified more than 10,000 members of the OR family in 23 mammals and classified them into 830 orthologous gene groups (OGGs) and 281 singletons. Significant differences occurred in the number of OR repertoires and OGGs among different species. We found that all marine mammals had fewer OR genes than their related terrestrial lineages, with the fewest OR genes found in cetaceans, which may be closely related to olfactory degradation. ORs with more gene duplications or loss events tended to be under weaker purifying selection. The average gain and loss rates of OR genes in terrestrial mammals were higher than those of mammalian gene families, while the average gain and loss rates of OR genes in marine mammals were significantly lower and much higher than those of mammalian gene families, respectively. Additionally, we failed to detect any one-to-one orthologous genes in the focal species, suggesting that OR genes are not well conserved among marine mammals. Conclusions: Marine mammals have experienced large numbers of OR gene losses compared with their related terrestrial lineages, which may result from the frequent birth-and-death evolution under varied functional constrains. Due to their independent degeneration, OR genes present in each lineage are not well conserved among marine mammals. Our study provides a basis for future research on the olfactory receptor function in mammals from the perspective of evolutionary trajectories.

Convergent evolution of olfactory and thermoregulatory capacities in small amphibious mammals

“…olfactory bulb and cribriform plate, two components of olfaction, compared to their terrestrial relatives (24)(25)(26). Aquatic vertebrates also have a smaller repertoire of functional olfactory receptor (OR) genes than terrestrial vertebrates (27)(28)(29)(30)(31)(32). Nevertheless, how pervasive, consistent, and strong these putative convergences and trade-offs are remains unknown.…”

Diversity, function and evolution of aquatic vertebrate genomes

“…This obvious change of HoxC gene is potentially caused by two rounds of genome-wide replication in early vertebrates (Damas et al, 2018;Venkatesh et al, 2014), as one of the duplicated homologous regions occurred a large number of gene deletions, maintained the status consistent with early vertebrate differentiation. In previous research, vertebrate OR genes can be classified into two types, which are further classified to 11 groups (Figure 7, α-λ) corresponding to the 11 ancestral OR genes of the most common recent ancestor among vertebrate species (Freitag et al, 1998;Gaillard et al, 2004;Liu et al, 2019a;Niimura and Nei, 2005). We identified the OR genes in 62 representative aquatic and terrestrial species, where Amphibia species (such as xenopus and axolotl) possessed approximately 1000 OR genes in the genome, which is much more than other species.…”

A field study of chemical senses in bottlenose dolphins and pilot whales

“…However, they lack the dorsal domain of the olfactory bulb, an area known to induce innate avoidance behavior against odors of predators and spoiled foods (Kishida, Thewissen, Hayakawa, Imai, & Agata, 2015). The number of genes coding for the olfactory receptors (OR), i.e., the sensory receptors of the main olfactory system, is low in this taxonomic group compared to their close terrestrial relatives (Kishida et al, 2015;Liu et al, 2019). However, the proportion of OR pseudogenes varies greatly among different species, with some having about 65% of their OR genes still functional (Liu et al, 2019).…”

“…The number of genes coding for the olfactory receptors (OR), i.e., the sensory receptors of the main olfactory system, is low in this taxonomic group compared to their close terrestrial relatives (Kishida et al, 2015;Liu et al, 2019). However, the proportion of OR pseudogenes varies greatly among different species, with some having about 65% of their OR genes still functional (Liu et al, 2019). Several authors have thus suggested they could use chemicals such as DMS as long-distance cues while foraging or navigating in the pelagic environment (Drake et al, 2015;Hagelin, Straley, Nielson, & Szabo, 2012;Thewissen et al, 2011;Torres, 2017).…”