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Mol Ecol. 2019 Apr;28(8):2013-2028. doi: 10.1111/mec.15022. Epub 2019 Feb 15.

Phototactic tails: Evolution and molecular basis of a novel sensory trait in sea snakes.

Author information

1
School of Biological Sciences, The University of Adelaide, Adelaide, South Australia, Australia.
2
Department of Biology, University of Florida, Gainesville, Florida.
3
School of Earth Sciences, University of Bristol, Bristol, UK.
4
School of Biological Sciences and Oceans Institute, University of Western Australia, Crawley, Western Australia, Australia.
5
Centre for Ophthalmology and Vision Science, Lions Eye Institute, University of Western Australia, Nedlands, Western Australia, Australia.
6
Robinson Research Institute, University of Adelaide, North Adelaide, South Australia, Australia.
7
Bioinformatics Hub, University of Adelaide, Adelaide, South Australia, Australia.
8
South Australian Health and Medical Research Institute (SAHMRI), Adelaide, South Australia, Australia.
9
Department of Life Sciences, The Natural History Museum, London, UK.

Abstract

Dermal phototaxis has been reported in a few aquatic vertebrate lineages spanning fish, amphibians and reptiles. These taxa respond to light on the skin of their elongate hind-bodies and tails by withdrawing under cover to avoid detection by predators. Here, we investigated tail phototaxis in sea snakes (Hydrophiinae), the only reptiles reported to exhibit this sensory behaviour. We conducted behavioural tests in 17 wild-caught sea snakes of eight species by illuminating the dorsal surface of the tail and midbody skin using cold white, violet, blue, green and red light. Our results confirmed phototactic tail withdrawal in the previously studied Aipysurus laevis, revealed this trait for the first time in A. duboisii and A. tenuis, and suggested that tail photoreceptors have peak spectral sensitivities between blue and green light (457-514 nm). Based on these results, and an absence of photoresponses in five Aipysurus and Hydrophis species, we tentatively infer that tail phototaxis evolved in the ancestor of a clade of six Aipysurus species (comprising 10% of all sea snakes). Quantifying tail damage, we found that the probability of sustaining tail injuries was not influenced by tail phototactic ability in snakes. Gene profiling showed that transcriptomes of both tail skin and body skin lacked visual opsins but contained melanopsin (opn4x) in addition to key genes of the retinal regeneration and phototransduction cascades. This work suggests that a nonvisual photoreceptor (e.g., Gq rhabdomeric) signalling pathway underlies tail phototaxis, and provides candidate gene targets for future studies of this unusual sensory innovation in reptiles.

KEYWORDS:

dermal photoreception; dermal phototaxis; extraocular; melanopsin; sea snakes

PMID:
30767303
DOI:
10.1111/mec.15022

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