Eye gene transcriptomes of diving water beetles: a contrast of surface and subterranean photic niches (#63)
The entry of animals into aquifers constitutes a form of niche creation, and two tribes of closely related Australian diving beetles (Dytiscidae) have independently invaded such closed groundwater systems from surface waters on multiple occasions. The subterranean lineages display convergent phenotypes common to aphotic cave habitats (eye loss and pale integumentation), and this group provides ideal comparative opportunities to explore the ‘regressive evolution’ of vision from a molecular perspective. Here we present data from the sequenced transcriptomes of two surface and three subterranean species, and focus on 45-candidate protein coding genes related to phototransduction and eye pigmentation. Forty-three candidate genes were found to be transcribed in surface and/or subterranean species. Four of the candidate genes were expressed in all surface species, but were absent from all subterranean transcriptomes, namely UV opsin, a non-visual ciliary opsin, a visual arrestin Arr1 and the myosin III gene ninaC. These gene products play interrelated roles in phototransduction cascades. One subterranean species transcribed the visual long wavelength opsin and the major visual arrestin Arr2, albeit in an aphotic environment. Both distance and likelihood tests of selection on these transcripts show no significant differences compared to surface relatives and evidence of purifying selection acting on these two genes. Overall, the results provide evidence for parallel loss of eye gene function in subterranean species, but also show that the vast majority of ‘eye genes’ retain their expression in aphotic environments. We discuss the possibility of pleiotropic roles, as opposed to incipient stages of pseudogene development, relative to the natural and evolutionary history of these beetles.