Sex-differences in the genetic architecture of individual recombination rates in wild house sparrows (Passer domesticus)

Abstract

AbstractMeiotic recombination is a fundamental feature of sex and an important driver of diversity in eukaryotic genomes. It ensures proper chromosome disjunction, increases responses to selection, and prevents mutation accumulation; however, it is also mutagenic and can break up favourable haplotypes built up by selection. This cost/benefit dynamic is likely to vary depending on mechanistic and evolutionary contexts, and indeed, recombination rates show huge variation within and between chromosomes, individuals, sexes, populations, and species. Identifying the genetic architecture of recombination rates is a key step in understanding the causes and consequences of this variation. Here, we investigate broad-scale recombination landscapes and individual crossover (CO) rates in a wild population of house sparrowsPasser domesticus). We integrated pedigree data with ∼61K SNPs to identify autosomal CO counts (ACC) and intra-chromosomal allelic shufflingin 2,802 gametes. Females had longer autosomal genetic maps (2558.1cM vs 2069.6cM), 1.37 times higher ACC, and 1.46 times higherthan males. ACC was heritable in females (h2= 0.23) but not in males, indicating genetic independence of male and female crossover rates. Conversely,was heritable in males (h2= 0.07), but not in females. Neither measure was associated with age or common environment effects. Genome-wide association studies of female ACC and malefound no significant loci, but ∼2% of SNPs had non-zero effects on female ACC. Our results suggest that recombination rates in house sparrows are polygenic and driven by many small-effect loci that may act incis(e.g. local recombination hotspots and modifiers) ortrans(global recombination modifiers). This work shows that recombination rates have evolutionary potential in wild birds, and provides a foundation for understanding associations between recombination rates, genome architecture, and individual fitness.