Extreme Recombination Frequencies Shape Genome Variation and Evolution in the Honeybee, Apis mellifera

Andreas Wallberg (1) , Sylvain Glémin (2, 3) , Matthew T Webster

1 Department of Medical Biochemistry and Microbiology, Science for Life Laboratory
2 GPIA - Génome, populations, interactions, adaptation
3 UMR ISEM - Institut des Sciences de l'Evolution de Montpellier

Meiotic recombination is a fundamental cellular process, with important consequences for evolution and genome integrity. However, we know little about how recombination rates vary across the genomes of most species and the molecular and evolutionary determinants of this variation. The honeybee, Apis mellifera, has extremely high rates of meiotic recombina-tion, although the evolutionary causes and consequences of this are unclear. Here we use patterns of linkage disequilibrium in whole genome resequencing data from 30 diploid hon-eybees to construct a fine-scale map of rates of crossing over in the genome. We find that, in contrast to vertebrate genomes, the recombination landscape is not strongly punctate. Crossover rates strongly correlate with levels of genetic variation, but not divergence, which indicates a pervasive impact of selection on the genome. Germ-line methylated genes have reduced crossover rate, which could indicate a role of methylation in suppressing recombi-nation. Controlling for the effects of methylation, we do not infer a strong association between gene expression patterns and recombination. The site frequency spectrum is strongly skewed from neutral expectations in honeybees: rare variants are dominated by AT-biased mutations, whereas GC-biased mutations are found at higher frequencies, indicative of a major influence of GC-biased gene conversion (gBGC), which we infer to generate an allele fixation bias 5-50 times the genomic average estimated in humans. We uncover further evidence that this repair bias specifically affects transitions and favours fixation of CpG sites. Recombination, via gBGC, therefore appears to have profound consequences on genome evolution in honeybees and interferes with the process of natural selection. These findings have important implications for our understanding of the forces driving molecular evolution.

Domaines: Génomique, Transcriptomique et Protéomique [q-bio.GN]; Bio-Informatique, Biologie Systémique [q-bio.QM]; Evolution [q-bio.PE]; Génétique des populations [q-bio.PE]; Génétique animale

Andreas Wallberg, Sylvain Glémin, Matthew T Webster. Extreme Recombination Frequencies Shape Genome Variation and Evolution in the Honeybee, Apis mellifera. PLoS Genetics, 2015, 11, ⟨10.1371/journal.pgen.1005189⟩. ⟨hal-02369486⟩