Recombining without Hotspots: A Comprehensive Evolutionary Portrait of Recombination in Two Closely Related Species ofDrosophila

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 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 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.

Connecting theory and data to understand recombination rate evolution

“…Patterns of LD indicate that both humans [80,82,137] and bonobos [83] share few recombination hotspots with chimpanzees, implying rapid evolution of recombination rate on the fine (kb) scale. By contrast, recombination rates calculated across larger chromosomal regions (from linkage maps or patterns of LD) usually show higher correlations among closely related species or conspecific populations [11,81,83,135,136,[138][139][140], with statistically divergent intervals comprising a minority of the genome [85]. Intriguingly, recombination hotspots and double-strand break hotspots appear to be evolutionarily stable in finches [141] and budding yeast (respectively) [142], suggesting that the rapid divergence of recombination rate on the fine scale observed in mammals could be the rstb.royalsocietypublishing.org Phil.…”

“…Another empirical observation is that distinct patterns of variation in recombination rate are sometimes observed on different genomic scales. Thus, the tempo and mode of recombination rate evolution may depend on the genomic scale on which it is measured [11,135,136] (figure 1). Patterns of LD indicate that both humans [80,82,137] and bonobos [83] share few recombination hotspots with chimpanzees, implying rapid evolution of recombination rate on the fine (kb) scale.…”

Coevolution between transposable elements and recombination

“…At one extreme of such spatial heterogeneity, C. elegans exhibits chromosome-scale differences in recombination rate with low levels of heterogeneity within chromosomal domains and lacks clearly defined hotspots [40]. Most eukaryotes, however, show some degree of local heterogeneity in recombination, from species in the Drosophila genus with moderate heterogeneity [41,42] to species like A. thaliana [35], yeast [43,44], finches [37], monkeyflowers [38] and dogs [45,46], with clear hotspots typically localized near promoter regions of genes. This latter form of recombination heterogeneity can be explained by a model in which open chromatin is exploited for crossover events, and the rate of hotspot turnover among species is low [ of control and turnover, have been found in some mammalian species with a PRDM9-mediated recombination mechanism that initiates at specific sequence motifs, alters chromatin structure and recruits the recombination machinery [9].…”

The Genomic Architecture of a Rapid Island Radiation: Recombination Rate Variation, Chromosome Structure, and Genome Assembly of the Hawaiian CricketLaupala

“…This pattern is consistent with earlier findings in plants (Anderson et al 2003), invertebrates (Rockman and Kruglyak 2009;Niehuis et al 2010), and vertebrates (Backström et al 2010;Roesti et al 2013;Singhal et al 2015) including humans (Kong et al 2002); but differs from observations in, for example, Drosophila (Kulathinal et al 2008), which show heterogeneity in recombination rates, but not necessarily much higher rates on the periphery of the chromosomes. Commonly invoked drivers of local recombination suppression, such as selection against recombination due to negative epistasis or the maintenance of linkage disequilibrium between mutually beneficial alleles (Smukowski and Noor 2011;Stevison et al 2011;Smukowski Heil et al 2015;Ortiz-Barrientos et al 2016), are not likely to leave chromosome-wide signatures. Rather, the observed U-shaped pattern is more likely attributable to structural properties of chromosomes, such as the location of the centromere and heterochromatin-rich regions (Copenhaver et al 1999;Haupt et al 2001).…”