Meiotic, genomic and evolutionary properties of crossover distribution in Drosophila yakuba

Abstract

The number of crossovers and their location across genomes are highly regulated during meiosis, yet the key components controlling them are fast evolving, hindering our understanding of the mechanistic causes and evolutionary consequences of changes in crossover rates. Drosophila melanogaster has been a model species to study meiosis for more than a century, with an available high-resolution crossover map that is, nonetheless, missing for closely related species, thus preventing evolutionary context. Here, we applied a novel and highly efficient approach to generate whole-genome high-resolution crossover maps in D. yakuba and tackle multiple questions that benefit from being addressed collectively within an appropriate phylogenetic framework, in our case the D. melanogaster species subgroup. The genotyping of more than 1,600 individual meiotic events allowed us to identify several key distinct properties relative to D. melanogaster. We show that together with higher crossover rates than D. melanogaster, D. yakuba has a stronger centromere effect and stronger crossover assurance than any Drosophila species analyzed to date. We also report the presence of an active crossover-associated meiotic drive mechanism for the X chromosome that results in the preferential inclusion in oocytes of chromatids with crossovers. Our evolutionary and genomic analyses suggest that the genome-wide landscape of crossover rates in D. yakuba has been fairly stable and captures a significant signal of the ancestral crossover landscape for the whole D. melanogaster subgroup, even informative for the D. melanogaster lineage. Contemporary crossover rates in D. melanogaster, on the other hand, do not recapitulate ancestral crossovers landscapes. As a result, the temporal stability of crossover landscapes observed in D. yakuba makes this species an ideal system for applying population genetic models of selection and linkage, given that these models assume temporal constancy in linkage effects. Our studies emphasize the importance of generating multiple high-resolution crossover rate maps within a coherent phylogenetic context to broaden our understanding of crossover control during meiosis and to improve studies on the evolutionary consequences of variable crossover rates across genomes and time. AUTHOR SUMMARYMeiotic recombination is a fundamental cellular process required for the formation of gametes in most eukaryotic organisms. Recombination also plays a fundamental role in evolution, increasing rates of adaptation. Paradoxically for such an essential process, key components evolve fast, and model organisms differ vastly in number of recombination events and distribution across chromosomes. This variation has limited our understanding of how recombination is controlled or why it can vary according to environmental cues. D. melanogaster has been a model species to study meiosis and recombination for more than a century and, in this study, we applied a new and highly efficient whole-genome genotyping scheme to identify recombination properties for a closely species, D. yakuba, thus providing an informative counterpoint and needed phylogenetic context. Our results describe important differences relative to D. melanogaster, including the first description of a mechanism favoring the segregation of recombinant chromatids to the functional egg pole under benign conditions. We argue that such a mechanism may also be active in other species. Moreover, our studies suggest that D. yakuba has maintained its recombination landscape for a longer time than D. melanogaster, indicating that the former species may be more adequate for evolutionary analyses. Combined, we show the importance of tackling the current siloed approach that focuses on model species with a more comprehensive analysis that requires the inclusion of closely related species when studying the causes and consequences of recombination variation.