The Genetic Architecture of Recombination Rates is Polygenic and Differs Between the Sexes in Wild House Sparrows ( <i>Passer domesticus</i> )

Meiotic recombination through chromosomal crossing-over is a fundamental feature of sex and an important driver of genomic diversity. It ensures proper disjunction, allows increased selection responses, and prevents mutation accumulation; however, it is also mutagenic and can break up favorable haplotypes. This cost-benefit dynamic is likely to vary depending on mechanistic and evolutionary contexts, and indeed, recombination rates show huge variation in nature. Identifying the genetic architecture of this variation is key to understanding its causes and consequences. Here, we investigate individual recombination rate variation in wild house sparrows (Passer domesticus). We integrate genomic and pedigree data to identify autosomal crossover counts (ACCs) and intrachromosomal allelic shuffling (r¯intra) in 13,056 gametes transmitted from 2,653 individuals to their offspring. Females had 1.37 times higher ACC, and 1.55 times higher r¯intra than males. ACC and r¯intra were heritable in females and males (ACC h2 = 0.23 and 0.11; r¯intra h2 = 0.12 and 0.14), but cross-sex additive genetic correlations were low (rA = 0.29 and 0.32 for ACC and r¯intra). Conditional bivariate analyses showed that all measures remained heritable after accounting for genetic values in the opposite sex, indicating that sex-specific ACC and r¯intra can evolve somewhat independently. Genome-wide models showed that ACC and r¯intra are polygenic and driven by many small-effect loci, many of which are likely to act in trans as global recombination modifiers. Our findings show that recombination rates of females and males can have different evolutionary potential in wild birds, providing a compelling mechanism for the evolution of sexual dimorphism in recombination.

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Journal
Molecular Biology and Evolution
Published
2024-08-23
DOI
https://doi.org/10.1093/molbev/msae179
Citations
14
Primary Topic
Evolution and Genetic Dynamics
Type
article
Field-Weighted Citation Impact
7.70

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article

The Genetic Architecture of Recombination Rates is Polygenic and Differs Between the Sexes in Wild House Sparrows ( Passer domesticus )

Henrik Jensen, Hamish A. Burnett, Cathrine Brekke, Thor Harald Ringsby et al.
14 citations
Molecular Biology and Evolution
Evolution and Genetic Dynamics
7.70
article

The Genetic Architecture of Recombination Rates is Polygenic and Differs Between the Sexes in Wild House Sparrows ( Passer domesticus )

Henrik Jensen, Hamish A. Burnett, Cathrine Brekke, Thor Harald Ringsby, Ingerid J. Hagen, Bertrand Servin, Lucy Peters, Arild Husby, Susan E. Johnston, Alina K. Niskanen, John McAuley
article en
14 citations

Abstract

Meiotic recombination through chromosomal crossing-over is a fundamental feature of sex and an important driver of genomic diversity. It ensures proper disjunction, allows increased selection responses, and prevents mutation accumulation; however, it is also mutagenic and can break up favorable haplotypes. This cost-benefit dynamic is likely to vary depending on mechanistic and evolutionary contexts, and indeed, recombination rates show huge variation in nature. Identifying the genetic architecture of this variation is key to understanding its causes and consequences. Here, we investigate individual recombination rate variation in wild house sparrows (Passer domesticus). We integrate genomic and pedigree data to identify autosomal crossover counts (ACCs) and intrachromosomal allelic shuffling (r¯intra) in 13,056 gametes transmitted from 2,653 individuals to their offspring. Females had 1.37 times higher ACC, and 1.55 times higher r¯intra than males. ACC and r¯intra were heritable in females and males (ACC h2 = 0.23 and 0.11; r¯intra h2 = 0.12 and 0.14), but cross-sex additive genetic correlations were low (rA = 0.29 and 0.32 for ACC and r¯intra). Conditional bivariate analyses showed that all measures remained heritable after accounting for genetic values in the opposite sex, indicating that sex-specific ACC and r¯intra can evolve somewhat independently. Genome-wide models showed that ACC and r¯intra are polygenic and driven by many small-effect loci, many of which are likely to act in trans as global recombination modifiers. Our findings show that recombination rates of females and males can have different evolutionary potential in wild birds, providing a compelling mechanism for the evolution of sexual dimorphism in recombination.

Molecular Biology and EvolutionVol. 41(9)
Uppsala University (SE), École Nationale Vétérinaire de Toulouse (FR), Université Fédérale de Toulouse Midi-Pyrénées (FR), Norwegian University of Science and Technology (NO), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Centre for Immunity, Infection and Evolution (GB), Norwegian Biodiversity Information Centre (NO), Norwegian Institute for Nature Research (NO), Génétique Physiologie et Systèmes d'Elevage (FR), University of Oulu (FI), University of Edinburgh (GB)
Royal Society, Norges Forskningsråd, Darwin Trust of Edinburgh
Openalex Percentile: Top 2%
Evolution and Genetic Dynamics
7.70
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