The genetic architecture of recombination rates is polygenic and differs between the sexes in wild house sparrows (Passer domesticus)

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 favourable 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 (ACC) and intra-chromosomal allelic shuffling () in 13,056 gametes transmitted from 2,653 individuals to their offspring. Females had 1.37 times higher ACC, and 1.55 times higher  than males. ACC and  were heritable in females and males (ACC h2 = 0.23 and 0.11;  h2 = 0.12 and 0.14), but cross-sex additive genetic correlations were low (rA = 0.29 and 0.32 for ACC and ). Conditional bivariate analyses showed that all measures remained heritable after accounting for genetic values in the opposite sex, indicating that sex-specific ACC and  can evolve somewhat independently. Genome-wide models showed that ACC and  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.

Methods
All data were collected from the meta-population of house sparrows inhabiting an 18-island archipelago covering 1600 km2 off the Helgeland coast in Northern Norway (midpoint of 66°32’N, 12°32’E), which has been subject to an individual-based long-term study since 1993. Birds are routinely captured and individually marked from the beginning of May to the middle of August and for approximately one month in the autumn using mist nets (adults and fledged juveniles), or as fledglings in accessible nests during the breeding season. A small (25 µl) blood sample is collected from the brachial vein for DNA from every captured bird. All SNPs used in our analysis were taken from two custom house sparrow Axiom SNP arrays (200K and 70K) based on the resequencing of 33 individual house sparrows, resulting in the dataset here of 65,840 SNPs in 12,965 individuals.. All SNP positions are given relative to the house sparrow genome assembly Passer_domesticus-1.0 (GenBank Assembly GCA_001700915.1).