Recombining without hotspots: A comprehensive evolutionary portrait of recombination in two closely related species of Drosophila

Abstract

Meiotic recombination rate varies across the genome within and between individuals, populations, and species in virtually all taxa studied. In almost every species, this variation takes the form of discrete recombination hotspots, determined in Metazoans by a protein called PRDM9. Hotspots and their determinants have a profound effect on the genomic landscape, and share certain features that extend across the tree of life. Drosophila, in contrast, are anomalous in their absence of hotspots, PRDM9, and other species-specific differences in the determination of recombination. To better understand the evolution of meiosis and general patterns of recombination across diverse taxa, we present what may be the most comprehensive portrait of recombination to date, combining contemporary recombination estimates from each of two sister species along with historic estimates of recombination using linkage-disequilibrium-based approaches derived from sequence data from both species. Using Drosophila pseudoobscura and Drosophila miranda as a model system, we compare recombination rate between species at multiple scales, and we replicate the pattern seen in human-chimpanzee that recombination rate is conserved at broad scales and more divergent at finer scales. We also find evidence of a species-wide recombination modifier, resulting in both a present and historic genome wide elevation of recombination rates in D. miranda, and identify broad scale effects on recombination from the presence of an inter-species inversion. Finally, we reveal an unprecedented view of the distribution of recombination in D. pseudoobscura, illustrating patterns of linked selection and where recombination is taking place. Overall, by combining these estimation approaches, we highlight key similarities and differences in recombination between Drosophila and other organisms.\n\nAuthor SummaryRecombination, or crossing over, describes an essential exchange of genetic material that occurs during egg and sperm development and has consequences for the proper segregation of chromosomes, and for the evolution of genomes and genomic features. In our study, we compare genome wide recombination rate in two closely related species of the fruit fly Drosophila to understand if and how recombination changes over time. We find that recombination does indeed change, we observe globally increased recombination in one species, and differences in regional recombination likely reflecting the result of a chromosomal rearrangement in both species. Moreover, we show that the extent that recombination changes is dependent on the physical scale at which recombination is measured, likely reflecting selection pressures on recombination distribution and replicating a pattern seen in human-chimpanzee recombination. Apart from between-species differences, we note several ways in which the Drosophila recombination landscape has changed since Drosophila diverged from other organisms. In contrast to species of fungi, plants, and animals, Drosophila recombination is not concentrated in discrete regions known as hotspots, nor is it increased near the start of genes, suggesting that despite the importance of the recombination process, the determinants of recombination have been shifting over evolutionary time.