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 some mammals 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 speciesspecific differences in the determination of recombination. To better understand the evolution of meiosis and general patterns of recombination across diverse taxa, we present a truly comprehensive portrait of recombination across time, combining recently published cross-based contemporary recombination estimates from each of two sister species with newly obtained linkage-disequilibrium-based historic estimates of recombination from both of these species. Using Drosophila pseudoobscura and Drosophila miranda as a model system, we compare recombination rate between species at multiple scales, and we suggest that Drosophila replicate the pattern seen in human-chimpanzee in which recombination rate is conserved at broad scales. We also find evidence of a species-wide recombination modifier(s), 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 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.

High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

“…P-values are 0.05 (*) and 0.01 (**). (Hellsten et al 2013), or Drosophila (Smukowski Heil et al 2015). Specific recombination intensities were different depending on the collection used which could be attributed to the difference in LD patterns at fine scale in the two populations, or differences arising from the complex evolutionary histories of the two genetic pools we used.…”

“…This switch can be detected by genotyping the progenies derived from biparental or multi-parental crosses (for a review see Huang et al 2015) but is limited by a constrained number of COs (Darvasi et al 1993). Statistical approaches were also developed to estimate the population recombination parameter, r, and to computationally infer genome-wide, population-averaged recombination rates (McVean et al 2002(McVean et al , 2004Li and Stephens 2003;Slatkin 2008;Hellsten et al 2013;Smukowski Heil et al 2015). These approaches, also termed "coalescent analysis," rely on linkage disequilibrium (LD) patterns in populations which represent a nonrandom association of alleles at different loci (Lewontin and Kojima 1960).…”

Nonparadoxical evolutionary stability of the recombination initiation landscape in yeast

“…Interestingly, DSB hotspots are well conserved between the Schizosaccharomyces species S. pombe and S. kambucha (~0.5% sequence divergence) (34) despite mapping to sites without known function (35). In contrast, in Drosophila , which lacks a PRDM9-like system but also does not preferentially target recombination to promoters or known functional elements, the fine-scale distribution of recombination appears to evolve rapidly (36). …”

Genomic changes following the reversal of a Y chromosome to an autosome inDrosophila pseudoobscura

“…We downloaded population genomic datasets including 11 D. pseudoobscura individuals from seven different populations and 12 D. miranda individuals from two studies (McGaugh and Noor 2012;Zhou and Bachtrog 2012;Smukowski Heil et al 2015; NCBI accession numbers in Table S6). After trimming with Trim Galore (v0.4.0; http://www.bioinformatics.babraham.ac.uk/projects/trim_galore/), we mapped all reads to the genome using a pipeline modified from Lack et al (2015; https://github.com/justin-lack/Drosophila-Genome-Nexus/blob/master/round1_assembly.pl).…”