PT  - JOURNAL ARTICLE
AU  - Fantin Carpentier
AU  - Ricardo C. Rodríguez de la Vega
AU  - Michael H. Perlin
AU  - R. Margaret Wallen
AU  - Michael E. Hood
AU  - Tatiana Giraud
TI  - Tempo of degeneration across independently evolved non-recombining regions
AID  - 10.1101/2021.07.20.453045
DP  - 2021 Jan 01
TA  - bioRxiv
PG  - 2021.07.20.453045
4099  - http://biorxiv.org/content/early/2021/07/20/2021.07.20.453045.short
4100  - http://biorxiv.org/content/early/2021/07/20/2021.07.20.453045.full
AB  - Recombination is beneficial over the long term, allowing more effective selection. Despite long-term advantages of recombination, local recombination suppression is known to evolve and lead to genomic degeneration, in particular on sex and mating-type chromosomes, sometimes linked to severe genetic diseases. Here, we investigated the tempo of degeneration in non-recombining regions, i.e., the function curve for the accumulation of deleterious mutations over time, taking advantage of 17 independent events of large recombination suppression identified on mating-type chromosomes of anther-smut fungi, including five newly identified in the present study. Using high-quality genomes assemblies of alternative mating types of 13 Microbotryum species, we estimated the degeneration levels in terms of accumulation of non-optimal codons and non-synonymous substitutions in non-recombining regions. We found a reduced frequency of optimal codons in the non-recombining regions on mating-type chromosomes compared to autosomes. We showed that the lower frequency of optimal codons in non-recombining regions was not due to less frequent GC-biased gene conversion or lower ancestral expression levels compared to recombining regions. We estimated that the frequency of optimal codon usage decreased linearly at a rate of 0.989 per My. The non-synonymous over synonymous substitution rate (dN/dS) increased rapidly after recombination suppression and then reached a plateau. To our knowledge this is the first study to disentangle effects of reduced selection efficacy from GC-biased gene conversion in the evolution of optimal codon usage to quantify the tempo of degeneration in non-recombining regions, leveraging on multiple independent recombination suppression events. Understanding the tempo of degeneration is important for our knowledge on genomic evolution, on the origin of genetic diseases and on the maintenance of regions without recombination.Competing Interest StatementThe authors have declared no competing interest.