Standing Genetic Variation Drives Repeatable Experimental Evolution in Outcrossing Populations of Saccharomyces cerevisiae

Abstract

In "evolve-and-resequence" (E&R) experiments, whole-genome sequence data from laboratory-evolved populations can potentially uncover mechanisms of adaptive change. E&R experiments with initially isogenic, asexually reproducing microbes have repeatedly shown that beneficial de novo mutations drive adaptation, and these mutations are not shared among independently evolving replicate populations. Recent E&R experiments with higher eukaryotes that maintain genetic variation via sexual reproduction implicate largely different mechanisms; adaptation may act primarily on pre-existing genetic variation and occur in parallel among independent populations. But this is currently a debated topic, and generalizing these conclusions is problematic because E&R experiments with sexual species are difficult to implement and important elements of experimental design suffer for practical reasons. We circumvent potentially confounding limitations with a yeast model capable of shuffling genotypes via sexual recombination. Our starting population consisted of a highly intercrossed diploid Saccharomyces cerevisiae initiated from four wild haplotypes. We imposed a laboratory domestication treatment on 12 independent replicate populations for 18 weeks, where each week included 2 days as diploids in liquid culture and a forced recombination/mating event. We then sequenced pooled population samples at weeks 0, 6, 12, and 18. We show that adaptation is highly parallel among replicate populations, and can be localized to a modest number of genomic regions. We also demonstrate that despite hundreds of generations of evolution and large effective population sizes, de novo beneficial mutations do not play a large role in this adaptation. Further, we have high power to detect the signal of change in these populations but show how this power is dramatically reduced when fewer timepoints are sampled, or fewer replicate populations are analyzed. As ours is the most highly replicated and sampled E&R study in a sexual species to date, this evokes important considerations for past and future experiments.

Estimating effective population size from temporal allele frequency changes in experimental evolution

“…Long time series have recently become available for some E&R experiments (Barrick et al 2009;Burke et al 2010Burke et al , 2014. Standard N e estimators (Krimbas and Tsakas 1971; Nei and Tajima 1981; Waples 1989) assume a small number of generations ðtÞ and approximate N e using 2N e t=F: If, however, t=N e is larger, using this approximation can lead to severe bias ( Figure S2).…”

Evolution of stickleback in 50 years on earthquake-uplifted islands

“…For example, evolution in new habitats may be limited by waiting times for new beneficial mutations (9)(10)(11). Even when adaptation occurs from standing genetic variation, evolution via selection of numerous independent loci of small effect may be time consuming (12)(13)(14)(15)(16). We know, however, that evolution can occur rapidly, particularly under artificial selection or in human-altered landscapes (17)(18)(19)(20)(21).…”

Social wasps are a Saccharomyces mating nest

“…However, several recent findings have called this hypothesis into question. Evidence of interspecific hybridization (4-6), a high level of strain heterozygosity (7,8), and prion transmission (9) have suggested that outbreeding could occur more frequently than previously estimated (9).We calculated the outbreeding rate from the heterozygosity level at polymorphic sites in three genes selected as able to reproduce the topology generated with the genomes of S. cerevisiae (10). Calculation of the outbreeding rate was carried out only on diploid strains for which the sequences of the three genes were available (n = 34; SI Appendix, Table S1), and was based on a modified model, accounting for the possibility of diploid individuals to derive either from intra-ascus mating or from outcrossing (11).…”

“…However, several recent findings have called this hypothesis into question. Evidence of interspecific hybridization (4-6), a high level of strain heterozygosity (7,8), and prion transmission (9) have suggested that outbreeding could occur more frequently than previously estimated (9).…”