Sex enhances adaptation by unlinking beneficial from detrimental mutations in experimental yeast populations

Abstract

BackgroundThe maintenance of sexuality is a classic problem in evolutionary biology because it is a less efficient mode of reproduction compared with asexuality; however, many organisms are sexual. Theoretical work suggests sex facilitates natural selection, and experimental data support this. However, there are fewer experimental studies that have attempted to determine the mechanisms underlying the advantage of sex. Two main classes of hypotheses have been proposed to explain its advantage: detrimental mutation clearance and beneficial mutation accumulation. Here we attempt to experimentally differentiate between these two classes by evolving Saccharomyces cerevisiae populations that differ only in their ability to undergo sex, and also manipulate mutation rate. We cannot manipulate the types of mutation that occur, but instead propagate populations in both stressful and permissive environments and assume that the extent of detrimental mutation clearance and beneficial mutation incorporation differs between them.ResultsAfter 300 mitotic generations interspersed with 11 rounds of sex we found there was no change or difference in fitness between sexuals and asexuals propagated in the permissive environment, regardless of mutation rate. Sex conferred a greater extent of adaptation in the stressful environment, and wild-type and elevated mutation rate sexual populations adapted equivalently. However, the asexual populations with an elevated mutation rate appeared more retarded in their extent of adaptation compared to asexual wild-type populations.ConclusionsSex provided no advantage in the permissive environment where beneficial mutations were rare. We could not evaluate if sex functioned to clear detrimental mutations more effectively or not here as no additional fitness load was observed in the mutator populations. However, in the stressful environment, where detrimental mutations were likely of more consequence, and where beneficial mutations were apparent, sex provided an advantage. In the stressful environment asexuals were increasingly constrained in their extent of adaptation with increasing mutation rate. Sex appeared to facilitate adaptation not just by more rapidly combining beneficial mutations, but also by unlinking beneficial from detrimental mutations: sex allowed selection to operate on both types of mutations more effectively compared to asexual populations.

Genomics and the making of yeast biodiversity

“…Although asexual strains achieve higher laboratory fitness [15], they seem not to persist or undergo frequent cladogenesis. Sex may increase the rate of adaptation to novel environments and help purge deleterious alleles [16,17]. Thus, most yeast clades harbor at least some sexual taxa, which likely reflect their ancestral states.…”

Higher rates of sex evolve during adaptation to more complex environments

“…Furthermore, it can break down negative linkage that builds up in finite populations under selection (16), indirectly favoring more genetic mixing (17,18). Experimental studies have demonstrated that populations with sex adapt faster than asexual ones (19)(20)(21)(22). Furthermore, experimental evolution studies focusing on the within-population evolution of sex (12), as well as of recombination (23) and selfing (24), support the theory that genetic mixing is favorable during adaptation.…”

Growth phase-specific evolutionary benefits of natural transformation in Acinetobacter baylyi

“…It is likely that the different outcomes of the abovementioned reports on evolutionary benefits of natural transformation are due to species-specific differences in the selective forces maintaining natural transformation and/or variation in the experimental setups. Recent experimental evidence suggests conditional benefits of recombination as demonstrated under stressful growth conditions in sexually reproducing yeast (Gray and Goddard, 2012), and recently for S. pneumoniae where periods of stress offset the initial costs of competence (Engelmoer et al, 2013).…”