TY - JOUR

T1 - Contrasting Gene Decay in Subterranean Vertebrates

T2 - Insights from Cavefishes and Fossorial Mammals

AU - Policarpo, Maxime

AU - Fumey, Julien

AU - Lafargeas, Philippe

AU - Naquin, Delphine

AU - Thermes, Claude

AU - Naville, Magali

AU - Dechaud, Corentin

AU - Volff, Jean-Nicolas

AU - Cabau, Cedric

AU - Klopp, Christophe

AU - Moller, Peter Rask

AU - Bernatchez, Louis

AU - Garcia-Machado, Erik

AU - Retaux, Sylvie

AU - Casane, Didier

PY - 2021

Y1 - 2021

N2 - 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 nonvisual 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 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 loss-of-function mutations in ancient fossorial mammals, further suggesting that blind fishes cannot thrive more than a few million years in cave ecosystems.

AB - 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 nonvisual 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 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 loss-of-function mutations in ancient fossorial mammals, further suggesting that blind fishes cannot thrive more than a few million years in cave ecosystems.

KW - cavefishes

KW - eye-specific genes

KW - pseudogenization

KW - machine learning

KW - relaxed selection

KW - molecular dating

U2 - 10.1093/molbev/msaa249

DO - 10.1093/molbev/msaa249

M3 - Journal article

C2 - 32986833

VL - 38

SP - 589

EP - 605

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 2

ER -