Parallel decay of vision genes in subterranean water beetles

Barbara L Langille; Simon M Tierney; Terry Bertozzi; Perry G Beasley-Hall; Tessa M Bradford; Erinn P Fagan-Jeffries; Josephine Hyde; Remko Leijs; Matthew Richardson; Kathleen M Saint; Danielle N Stringer; Adrián Villastrigo; William F Humphreys; Andrew D Austin; Steven J B Cooper

doi:10.1016/j.ympev.2022.107522

Parallel decay of vision genes in subterranean water beetles

Mol Phylogenet Evol. 2022 Aug:173:107522. doi: 10.1016/j.ympev.2022.107522. Epub 2022 May 17.

Authors

Affiliations

¹ Australian Centre for Evolutionary Biology and Biodiversity, Department of Ecology and Evolution, School of Biological Sciences, University of Adelaide, South Australia 5005, Australia. Electronic address: barbara.langille@adelaide.edu.au.
² Australian Centre for Evolutionary Biology and Biodiversity, Department of Ecology and Evolution, School of Biological Sciences, University of Adelaide, South Australia 5005, Australia; Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW 2751, Australia.
³ Australian Centre for Evolutionary Biology and Biodiversity, Department of Ecology and Evolution, School of Biological Sciences, University of Adelaide, South Australia 5005, Australia; Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia.
⁴ Australian Centre for Evolutionary Biology and Biodiversity, Department of Ecology and Evolution, School of Biological Sciences, University of Adelaide, South Australia 5005, Australia.
⁵ Australian Centre for Evolutionary Biology and Biodiversity, Department of Ecology and Evolution, School of Biological Sciences, University of Adelaide, South Australia 5005, Australia; Western Australia Department of Biodiversity Conservation and Attractions, Kensington, WA 6151, Australia.
⁶ Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia.
⁷ Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia; Institute of Evolutionary Biology, Passeig Marítim de la Barceloneta, 37-49, 08003, Spain.
⁸ Western Australian Museum, Locked Bag 40, Welshpool DC, WA 6986, Australia; School of Animal Biology, University of Western Australia, Nedlands, Western Australia, Australia.

PMID: 35595008
DOI: 10.1016/j.ympev.2022.107522

Abstract

In the framework of neutral theory of molecular evolution, genes specific to the development and function of eyes in subterranean animals living in permanent darkness are expected to evolve by relaxed selection, ultimately becoming pseudogenes. However, definitive empirical evidence for the role of neutral processes in the loss of vision over evolutionary time remains controversial. In previous studies, we characterized an assemblage of independently-evolved water beetle (Dytiscidae) species from a subterranean archipelago in Western Australia, where parallel vision and eye loss have occurred. Using a combination of transcriptomics and exon capture, we present evidence of parallel coding sequence decay, resulting from the accumulation of frameshift mutations and premature stop codons, in eight phototransduction genes (arrestins, opsins, ninaC and transient receptor potential channel genes) in 32 subterranean species in contrast to surface species, where these genes have open reading frames. Our results provide strong evidence to support neutral evolutionary processes as a major contributing factor to the loss of phototransduction genes in subterranean animals, with the ultimate fate being the irreversible loss of a light detection system.

Keywords: Dytiscidae; Neutral evolution theory; Pseudogenisation; Regressive evolution; Subterranean beetles; Vision genes.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Coleoptera* / genetics
Evolution, Molecular
Opsins / genetics
Phylogeny
Water

Substances

Opsins
Water