Eyes underground: regression of visual protein networks in subterranean mammals

Regressive evolution involves the degeneration of formerly useful structures in a lineage over time, and may be accompanied by the molecular decay of phenotype-specific genes. The mammalian eye has repeatedly undergone degeneration in taxa that occupy dim-light environments including subterranean habitats. Here we assess whether a decrease in the amount of light that reaches the retina is associated with increased regression of retinal genes, whether the phototransduction and visual cycle pathways degrade in a predictable pattern, and if the timing of retinal gene loss is associated with the entrance of mammalian lineages into subterranean environments. Sequence data were obtained from the publically available genomes of the Cape golden mole (Chrysochloris asiatica), naked mole-rat (Heterocephalus glaber) and star-nosed mole (Condylura cristata) for 65 genes associated with phototransduction, the visual cycle, and other retinal functions. Gene sequences were inspected for inactivating mutations and, when present, pseudogene sequences were compared to sequences from subaerial outgroup species. To test whether retinal degeneration is correlated with historical entrances into subterranean environments, estimated dates of retinal gene inactivation were compared to the fossil record and phylogenetic inferences of ancestral fossoriality. Our results show that (1) lower levels of light available to the retina correspond with an increase in the number of retinal pseudogenes, (2) retinal protein networks generally degrade in a predictable manner, although the extensive loss of cone phototransduction genes in Heterocephalus raises further questions regarding SWS1-cone monochromacy versus functional rod monochromacy in this species, and (3) inactivation dates of retinal genes usually post-date inferred entrances into subterranean habitats.