Experimental evolution of recombination and crossover interference in Drosophila caused by directional selection for stress-related traits

Abstract

Background: Population genetics predicts that tight linkage between new and/or pre-existing beneficial and deleterious alleles should decrease the efficiency of natural selection in finite populations. By decoupling beneficial and deleterious alleles and facilitating the combination of beneficial alleles, recombination accelerates the formation of high-fitness genotypes. This may impose indirect selection for increased recombination. Despite the progress in theoretical understanding, interplay between recombination and selection remains a controversial issue in evolutionary biology. Even less satisfactory is the situation with crossover interference, which is a deviation of double-crossover frequency in a pair of adjacent intervals from the product of recombination rates in the two intervals expected on the assumption of crossover independence. Here, we report substantial changes in recombination and interference in three long-term directional selection experiments with Drosophila melanogaster: for desiccation (~50 generations), hypoxia, and hyperoxia tolerance (>200 generations each).

Results: For all three experiments, we found a high interval-specific increase of recombination frequencies in selection lines (up to 40-50% per interval) compared to the control lines. We also discovered a profound effect of selection on interference as expressed by an increased frequency of double crossovers in selection lines. Our results show that changes in interference are not necessarily coupled with increased recombination.

Conclusions: Our results support the theoretical predictions that adaptation to a new environment can promote evolution toward higher recombination. Moreover, this is the first evidence of selection for different recombination-unrelated traits potentially leading, not only to evolution toward increased crossover rates, but also to changes in crossover interference, one of the fundamental features of recombination.

Fig. 1

Change in recombination rates (± SE) in D. melanogaster caused by directional selection for desiccation tolerance. Significant increases in recombination rates were observed in selection lines (red) compared to control (blue) in intervals cv-v and v-f of chromosome X; net-dp, cn-kn, and c-px of chromosome 2; and h-th of chromosome 3. Asterisks indicate significant differences between selection and control at 0.01 and 0.001 levels using false discovery rate adjusted P values

Fig. 2

Change in recombination rates (±SE) in D. melanogaster caused by directional selection for (a) hypoxia and (b) hyperoxia tolerance. Significant increases in recombination rates were observed in hypoxia selection variant (red) compared to control (blue) in intervals y-cv, cv-v, and v-f of chromosome X; net-dp and dp-b of chromosome 2; and cu-sr and sr-e of chromosome 3. In hyperoxia selection variant, a significant increase in recombination rate was observed in all tested intervals of chromosome X, while only dp-b interval in chromosome 2 and in no interval of chromosome 3. Asterisks indicate significant differences between selection and control variants at 0.05 and 0.001 levels using false discovery rate adjusted P values