Natural Selection Shapes Variation in Genome-wide Recombination Rate in Drosophila pseudoobscura

Abstract

While recombination is widely recognized to be a key modulator of numerous evolutionary phenomena, we have a poor understanding of how recombination rate itself varies and evolves within a species. Here, we performed a comprehensive study of recombination rate (rate of meiotic crossing over) in two natural populations of Drosophila pseudoobscura from Utah and Arizona, USA. We used an amplicon sequencing approach to obtain high-quality genotypes in approximately 8000 individual backcrossed offspring (17 mapping populations with roughly 530 individuals each), for which we then quantified crossovers. Interestingly, variation in recombination rate within and between populations largely manifested as differences in genome-wide recombination rate rather than remodeling of the local recombination landscape.Comparing populations, we discovered individuals from the Utah population displayed on average 8% higher crossover rates than the Arizona population, a statistically significant difference. Using a QST-FST analysis, we found that this difference in crossover rate was dramatically higher than expected under neutrality, indicating that this difference may have been driven by natural selection. Finally, using a combination of short and long read wholegenome sequencing, we found no significant association between crossover rate and structural variation at the 200-400kb scale. Our results demonstrate that (1) there is abundant variation in genome-wide crossover rate in natural populations (2) interpopulation differences in recombination rate may be the result of local adaptation, and (3) the observed variation among individuals in recombination rate is primarily driven by global regulators of crossover rate, with little detected variation in recombination rate among strains across specific tracts of individual chromosomes.

Phenotypic and genotypic parallel evolution in parapatric ecotypes ofSenecio

“…Additionally, common FST -based approaches, including those used within this study can fail to detect other structural aspects of the genome that can be involved in adaptation (Wellenreuther et al, 2019), including copy number variation (Schrider et al, 2016;Nelson et al, 2019), local recombination rate variation (Reeve et al, 2016;Ortiz-Barrientos & James, 2017;Samuk et al, 2020), inversions (Kirkpatrick & Barton, 2006;Lowry & Willis, 2010;Faria et al, 2019), and transposons (González & Petrov, 2009;Schrader & Schmitz, 2019). Furthermore, the alleles contributing to adaptation are also difficult to detect if adaptation has proceeded by many alleles of small effect, which may be quite common in highly polygenic traits (Yeaman, 2015).…”

Adaptive Divergence of Meiotic Recombination Rate in Ecological Speciation

“…Although studies investigating intra- and inter-specific recombination rate divergence are not uncommon (reviewed in Smukowski and Noor [2011] ), this kind of studies are usually deficient in an ecological understanding of the speciation process or lack the population-level sampling required for inferring the driving forces of recombination rate differentiation. However, a recent study examining two ecologically different populations of Drosophila pseudoobscura found that the divergence of genome-wide recombination rate is due to natural selection ( Samuk et al. 2020 ).…”

“…Another challenge in understanding the relationship between ecological shifts, directional selection, and recombination rate evolution is that multipopulation data on recombination rate is largely lacking (but see Saleem et al. 2001 and Samuk et al. 2020 ).…”

Variants atRNF212andRNF212Bare associated with recombination rate variation in Soay sheep (Ovis aries)

“…Variation in recombination rate is likely to arise across taxa with variation in genome size and chromosome number (Stapley et al, 2017); in addition, the evolutionary costs and benefits of recombination may vary depending on the selective context, again leading to the expectation of recombination rate variation within and between populations (Otto and Barton, 2001;Otto and Lenormand, 2002). Indeed, cytogenetic and linkage mapping studies have shown that recombination rates can vary by orders of magnitude within and between chromosomes (Myers et al, 2005), individuals (Kong et al, 2004), populations (Samuk et al, 2020), sexes (Lenormand and Dutheil, 2005) and species (Stapley et al, 2017).…”