Recombination rates in pigs differ between breeds, sexes and individuals, and are associated with the RNF212, SYCP2, PRDM7, MEI1 and MSH4 loci

Abstract

Background: Recombination is a fundamental part of mammalian meiosis that leads to the exchange of large segments of DNA between homologous chromosomes and is therefore an important driver of genetic diversity in populations. In breeding populations, understanding recombination is of particular interest because it can break up unfavourable linkage phases between alleles and produce novel combinations of alleles that could be exploited in selection. In this study, we used dense single nucleotide polymorphism (SNP) genotype data and pedigree information to analyse individual and sex-specific variation and genetic architecture of recombination rates within and between five commercially selected pig breeds.

Results: In agreement with previous studies, recombination rates were higher in females than in males for all breeds and for all chromosomes, except 1 and 13, for which male rates were slightly higher. Total recombination rate differed between breeds but the pattern of recombination along the chromosomes was well conserved across breeds for the same sex. The autosomal linkage maps spanned a total length of 1731 to 1887 cM for males and of 2231 to 2515 cM for females. Estimates of heritability for individual autosomal crossover count ranged from 0.04 to 0.07 for males and from 0.08 to 0.11 for females. Fourteen genomic regions were found to be associated with individual autosomal crossover count. Of these, four were close to or within candidate genes that have previously been associated with individual recombination rates in pigs and other mammals, namely RNF212, SYCP2 and MSH4. Two of the identified regions included the PRDM7 and MEI1 genes, which are known to be involved in meiosis but have not been previously associated with variation in individual recombination rates.

Conclusions: This study shows that genetic variation in autosomal recombination rate persists in domesticated species under strong selection, with differences between closely-related breeds and marked differences between the sexes. Our findings support results from other studies, i.e., that individual crossover counts are associated with the RNF212, SYCP2 and MSH4 genes in pig. In addition, we have found two novel candidate genes associated with the trait, namely PRDM7 and MEI1.

Fig. 1

Illustration of the full sib family structures. The focal individuals (FID) are the parents, in black, and the crossover events studied are those in the gametes transmitted from the FID to the offspring

Fig. 2

Relationship between the physical (Mb) and genetic (cM) length of the chromosomes. The relationship between the genetic length in cM (x-axis) and physical length in Mb (y-axis) is plotted for each chromosome by breed and sex. The relationship is plotted with robust locally weighted regression using the Lowess smoother in R

Fig. 3

Male autosomal linkage maps by breed. Genetic positions of the SNPs in cM are plotted against their physical positions in Mb. Chromosome numbers are given in the facet headers

Fig. 4

Female autosomal linkage maps by breed. Genetic positions of the SNPs in cM are plotted against their physical positions in Mb. Chromosome numbers are given in the facet headers

Fig. 5

Comparison of male linkage maps (blue) and female linkage maps (red) of the large white breed. Genetic positions of the SNPs in cM are plotted against their physical positions in Mb. Chromosome numbers are given in the facet headers

Fig. 6

Distribution of the autosomal crossover count by breed and sex. The blue boxes are counts for males and red boxes are counts for females for each breed. The midline is the median and the box is from the 25th percentile to the 75th percentile

Fig. 7

Genome-wide associations between SNPs and autosomal crossover count. Genome-wide associations between SNPs and autosomal crossover count for each breed and sex. The dotted line is the statistical significance threshold = 0.05/number of markers per analysis. The Y axis is the negative logarithm of the p-value and the x axis is the physical positions of SNPs with alternating colors from autosome 1 to 18