Unprecedented Female Mutation Bias in the Aye-Aye, a Highly Unusual Lemur From Madagascar

Authors

Richard J Wang
Yadira Peña-García
Muthuswamy Raveendran
R Alan Harris
Thuy-Trang Nguyen
Marie-Claude Gingras
Yifan Wu
Lesette Perez
Anne D Yoder
Joe H Simmons
Jeffrey Rogers
Matthew W Hahn

Language

English

Publication Date

2-1-2025

Journal

PLoS Biology

DOI

10.1371/journal.pbio.3003015

PMID

39919095

PMCID

PMC11819580

PubMedCentral® Posted Date

2-7-2025

PubMedCentral® Full Text Version

Post-print

Abstract

Every mammal studied to date has been found to have a male mutation bias: male parents transmit more de novo mutations to offspring than female parents, contributing increasingly more mutations with age. Although male-biased mutation has been studied for more than 75 years, its causes are still debated. One obstacle to understanding this pattern is its near universality-without variation in mutation bias, it is difficult to find an underlying cause. Here, we present new data on multiple pedigrees from two primate species: aye-ayes (Daubentonia madagascariensis), a member of the strepsirrhine primates, and olive baboons (Papio anubis). In stark contrast to the pattern found across mammals, we find a much larger effect of maternal age than paternal age on mutation rates in the aye-aye. In addition, older aye-aye mothers transmit substantially more mutations than older fathers. We carry out both computational and experimental validation of our results, contrasting them with results from baboons and other primates using the same methodologies. Further, we analyze a set of DNA repair and replication genes to identify candidate mutations that may be responsible for the change in mutation bias observed in aye-ayes. Our results demonstrate that mutation bias is not an immutable trait, but rather one that can evolve between closely related species. Further work on aye-ayes (and possibly other lemuriform primates) should help to explain the molecular basis for sex-biased mutation.

Keywords

Animals, Female, Male, Madagascar, Mutation, Mutation Rate, Pedigree, Strepsirhini, Papio anubis

Published Open-Access

yes

Recommended Citation

Wang, Richard J; Peña-García, Yadira; Raveendran, Muthuswamy; et al., "Unprecedented Female Mutation Bias in the Aye-Aye, a Highly Unusual Lemur From Madagascar" (2025). Faculty and Staff Publications. 5084.
https://digitalcommons.library.tmc.edu/baylor_docs/5084