Contrasting Gene Decay in Subterranean Vertebrates: Insights from Cavefishes and Fossorial Mammals

Abstract

Evolution sometimes proceeds by loss, especially when structures and genes become dispensable after an environmental shift relaxes functional constraints. Subterranean vertebrates are outstanding models to analyze this process, and gene decay can serve as a readout. We sought to understand some general principles on the extent and tempo of the decay of genes involved in vision, circadian clock and pigmentation in cavefishes. The analysis of the genomes of two Cuban species belonging to the genus Lucifuga provided evidence for the largest loss of eye-specific genes and non-visual opsin genes reported so far in cavefishes. Comparisons with a recently evolved cave population of Astyanax mexicanus and three species belonging to the Chinese tetraploid genus Sinocyclocheilus revealed the combined effects of the level of eye regression, time and genome ploidy on eye-specific gene pseudogenization. The limited extent of gene decay in all these cavefishes and the very small number of loss of function (LoF) mutations per pseudogene suggest that their eye degeneration may not be very ancient, ranging from early to late Pleistocene. This is in sharp contrast with the identification of several vision genes carrying many LoF mutations in ancient fossorial mammals, further suggesting that blind fishes cannot thrive more than a few million years in cave ecosystems.

Evolutionary dynamics of the OR gene repertoire in teleost fishes: evidence of an association with changes in olfactory epithelium shape

“…4). Interestingly, the correlation was higher when considering only the shortest terminal branches (R > 0.7 with maximum branch length < We ran simulations of sequence evolution involving nucleotide substitutions and small indels taking into account their relative frequencies estimated in a study of gene decay in teleosts (Policarpo, et al 2020). We found that about half of the pseudogenes were not detected after ~ 40 millions of generations (supplementary fig.…”

“…In order to estimate the time necessary for making a pseudogene undetectable through the accumulation of substitutions and small indels, we ran simulations in which an intact OR sequence accumulated nucleotide substitutions (at a rate of 10-8 per generation) and indels at a rate of 0.05 x 10 -8 per generation as estimated previously (Policarpo, et al 2020). We also took into account the transition/transversion ratio and the relative frequency of indels ranging from 1 and 9 bp in length (more details on the numerical values used for the simulations are given in the Python script available at https://github.com/MaximePolicarpo/ Olfactory_receptor_genes).…”

“…expansion of RH1 gene repertoires (Musilova, et al 2019). In some cavefishes living in total darkness, loss of vision allowed the decay of many eye-specific genes (Policarpo, et al 2020).…”

“…For example, several deep-sea fishes independently evolved rod opsin-based dim light vision relying on the expansion of RH1 gene repertoires (Musilova, et al 2019). In some cavefishes living in total darkness, loss of vision allowed the decay of many eye-specific genes (Policarpo, et al 2020). Much less is known about the evolution of olfaction and the dynamics of the OR gene repertoire size.…”

BASE: a novel workflow to integrate non-ubiquitous genes in comparative genomics analyses for selection

“…While d S are assumed to evolve neutrally, d N are expected to be exposed to selection, as they change the aminoacidic structure of proteins. Despite some of these assumption have been challenged (Davydov et al, 2019; He et al, 2020), analyses based on codon models have proved themselves as key approaches in comparative genomics, such as investigating positive selection connected to evolutionary innovations (Parker et al 2013; Zhang et al 2014; Li et al 2014) or testing the relaxation of selective constraints after trait decay (Liu et al 2019; Policarpo et al 2020). In other instances, these approaches have been used to observe genome-wide effects linked to events such as shifts in environmental niches or the loss of recombination in asexual genomes (Plazzi et al, 2017; Bast et al 2018).…”