Regressed but not gone: Patterns of vision gene loss and retention in subterranean mammals

Abstract

Regressive evolution involves the degradation of formerly useful traits as organisms invade novel ecological niches. In animals, committing to a strict subterranean habit can lead to regression of the eyes, likely due to a limited exposure to light. Several lineages of subterranean mammals show evidence of such degeneration, which can include decreased organization of the retina, malformation of the lens and subcutaneous positioning of the eye. Advances in DNA sequencing have revealed that this regression co-occurs with a degradation of genomic loci encoding visual functions, including protein-coding genes. Other dim light-adapted vertebrates with normal ocular anatomy, such as nocturnal and aquatic species, also demonstrate evidence of visual gene loss, but the absence of comparative studies has led to the untested assumption that subterranean mammals are special in the degree of this genomic regression. Additionally, previous studies have shown that not all vision genes have been lost in subterranean mammals, but it is unclear whether they are under relaxed selection and will ultimately be lost, are maintained due to pleiotropy or if natural selection is favoring the retention of the eye and certain critical underlying loci. Here I report that vision gene loss in subterranean mammals tends to be more extensive in quantity and differs in distribution from other dim light-adapted mammals, although some committed subterranean mammals demonstrate significant overlap with nocturnal microphthalmic species. In addition, blind subterranean mammals retain functional orthologs of non-pleiotropic visual genes that are evolving at rates consistent with purifying selection. Together, these results suggest that although living underground tends to lead to major losses of visual functions, natural selection is maintaining genes that support the eye, perhaps as an organ for circadian and/or circannual entrainment.