Natural selection shapes variation in genome-wide recombination rate in Drosophila pseudoobscura

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 whole-genome
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) at the 200-400kb scale, recombination rate appears to
vary largely genome wide, rather than in specific intervals and (3)
interpopulation differences in recombination rate may be the result of
local adaptation.