Loss of olfaction in sea snakes provides new perspectives on the aquatic adaptation of amniotes

Abstract

Marine amniotes, a polyphyletic group, provide an excellent opportunity for studying convergent evolution. Their sense of smell tends to degenerate, but this process has not been explored by comparing fully aquatic species with their amphibious relatives in an evolutionary context. Here, we sequenced the genomes of fully aquatic and amphibious sea snakes and identified repertoires of chemosensory receptor genes involved in olfaction. Snakes possess large numbers of the olfactory receptor ( OR ) genes and the type-2 vomeronasal receptor ( V2R ) genes, and expression profiling in the olfactory tissues suggests that snakes use the ORs in the main olfactory system (MOS) and the V2Rs in the vomeronasal system (VNS). The number of OR genes has decreased in sea snakes, and fully aquatic species lost MOS which is responsible for detecting airborne odours. By contrast, sea snakes including fully aquatic species retain a number of V2R genes and a well-developed VNS for smelling underwater. This study suggests that the sense of smell also degenerated in sea snakes, particularly in fully aquatic species, but their residual olfactory capability is distinct from that of other fully aquatic amniotes. Amphibious species show an intermediate status between terrestrial and fully aquatic snakes, implying their importance in understanding the process of aquatic adaptation.

Convergent evolution of olfactory and thermoregulatory capacities in small amphibious mammals

“…1). Our observation of repeated reduction of olfactory surface area is also consistent with convergent enrichment in pseudogenes as well as reduction of the number of functional OR genes in amphibious and aquatic vertebrate genomes (26)(27)(28)(29)(30)(31)39). We demonstrated that small amphibious mammals convergently lost a part of their olfactory capacities.…”

“…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.…”

New Environment, New Invaders—Repeated Horizontal Transfer of LINEs to Sea Snakes

“…1990 ; Camacho et al. 2009 ) to perform a nucleotide search for the consensus sequences of each subfamily in the genomes of two closely related terrestrial elapids ( N. scutatus and P. textilis ) (provided by Richard Edwards), and a more distantly related semi-marine elapid ( L. colubrina ) ( Kishida et al. 2019 ).…”

“…Similar to the search of closely related terrestrial species, we used megablast to perform reciprocal searches for the consensus sequences of the seven Aipysurus LINE subfamilies in the genomes of H. melanocephalus and Emydocephalus annulatus ( Kishida 2019 ), and assembled transcriptomes from various tissues of A. laevis , A. tenuis , and H. major from Crowe-Riddell et al. (2019) .…”

Swim with the tide: Tactics to maximize prey detection by a specialist predator, the greater sea snake (Hydrophis major)

“…Aquatic habitats largely eliminate substrate-deposited chemical trails, promoting reliance on other types of cues (such as visual ones [17]). However, many marine organisms (including fish) produce waterborne chemicals that may be detectable by a snake's highly specialized vomeronasal system [18,19], and three species of sea snakes have been reported to use chemical cues from their prey to select foraging sites (Emydocephalus annulatus [20]; Hydrophis melanocephalus and H. ornatus [21]. Thus, although the threedimensional nature of the aquatic environment reduces the usefulness of substrate-deposited cues, it allows other kinds of chemical cues to be widely disseminated.…”