Abstract
BackgroundPopulation 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).ResultsFor 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0206-5) contains supplementary material, which is available to authorized users.
Highlights
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
Our results indicate that long-term directional selection for recombination-unrelated traits may lead to an increase in recombination rates, and to relaxation of positive interference and appearance of negative interference
An alternative mechanism is fluctuation of linkage disequilibrium (LD) in small populations combined with directional selection, which may lead to higher recombination [19]
Summary
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. Tight linkage between new and/or pre-existing beneficial and deleterious alleles should decrease the efficiency of natural selection, as a consequence of the HillRobertson effect [13], which includes various forms of interference in finite populations [14,15,16,17]. As noted by Barton [21], “... the basic theoretical framework is clear, we still do not know whether selection is generally strong enough, and has the right form, to give a general advantage to sex and recombination” In this respect, it is worth mentioning the important and debated assumption of insufficient recombination as a limit to selection. Numerous studies support this hypothesis [20, 22,23,24,25,26,27,28,29,30], while opposite conclusions have been reached [31,32,33,34,35] based on the idea that a low level of recombination should be sufficient to achieve most of the benefits associated with this process [36]
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