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Parallel genome-wide fixation of ancestral alleles in partially outcrossing experimental populations of Caenorhabditis elegans.

ABSTRACT: Experimental evolution studies, coupled with new advances in DNA sequencing technology, have become a powerful tool for exploring how populations respond to selection at the genomic level. Recent experiments in microbes typically have found evidence for multiple novel mutations, which are usually fixed. In contrast, in animal model systems, evolutionary responses seem to involve more modest changes in the frequencies of pre-existing alleles, probably because these populations outcross and are usually initialized with greater levels of standing variation. In this experiment, I used whole-genome resequencing to estimate allele frequencies and look for novel substitutions in experimentally evolved populations of Caenorhabditis elegans. These populations were founded with a fixed pair of deleterious mutations introgressed into multiple wild genetic backgrounds and allowed to evolve for 50 generations with a mixed mating system. There is evidence for some recombination between ancestral haplotypes, but selective sweeps seem to have resulted in the fixation of large chromosomal segments throughout most of the genome. In addition, a few new mutations were detected. Simulations suggest that strong selection and low outcrossing rates are likely explanations for the observed outcomes, consistent with earlier work showing large fitness increases in these populations over 50 generations. These results also show clear parallels to population genetic patterns in C. elegans in nature: recent selective sweeps, high linkage disequilibrium, and low effective recombination rates. Thus, the genomic consequences of selection depend heavily on the biology of the organism in question, including its mating system and levels of genetic variation.

SUBMITTER: Chandler CH

PROVIDER: S-EPMC4169157 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Parallel genome-wide fixation of ancestral alleles in partially outcrossing experimental populations of Caenorhabditis elegans.

Chandler Christopher H CH

G3 (Bethesda, Md.) 20140701 9

Experimental evolution studies, coupled with new advances in DNA sequencing technology, have become a powerful tool for exploring how populations respond to selection at the genomic level. Recent experiments in microbes typically have found evidence for multiple novel mutations, which are usually fixed. In contrast, in animal model systems, evolutionary responses seem to involve more modest changes in the frequencies of pre-existing alleles, probably because these populations outcross and are us ...[more]

PMID: 24989146

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Project description:BackgroundWhy most organisms reproduce via outcrossing rather than selfing is a central question in evolutionary biology. It has long ago been suggested that outcrossing is favoured when it facilitates adaptation to novel environments. We have previously shown that the experimental evolution of increased outcrossing rates in populations of the male-hermaphrodite nematode Caenorhabditis elegans were correlated with the experimental evolution of increased male fitness. However, it is unknown whether outcrossing led to adaptation, and if so, which fitness components can explain the observed increase in outcrossing rates.ResultsUsing experimental evolution in six populations with initially low standing levels of genetic diversity, we show with head-to-head competition assays that population-wide fitness improved during 100 generations. Since outcrossing rates increased during the same period, this result demonstrates that outcrossing is adaptive. We also show that there was little evolution of hermaphrodite fitness under conditions of selfing or under conditions of outcrossing with unrelated tester males. We nonetheless find a positive genetic correlation between hermaphrodite self-fitness and population-wide fitness, and a negative genetic correlation between hermaphrodite mating success and population-wide fitness. These results suggest that the several hermaphrodite traits measured are fitness components. Tradeoffs expressed in hermaphrodites, particularly noticed between self-fitness and mating success, may in turn explain their lack of change during experimental evolution.ConclusionsOur findings indicate that outcrossing facilitates adaptation to novel environments. They further indicate that the experimental evolution of increased outcrossing rates depended little on hermaphrodites because of fitness tradeoffs between selfing and outcrossing. Instead, the evolution of increased outcrossing rates appears to have resulted from unhindered selection on males.

Project description:BackgroundClassic population genetics theory predicts that mixed reproductive systems, where self reproduction (selfing) and outcrossing co-exist, should not be as common as they are in nature. One means of reconciling theory with observations is to recognize that sexual conflict between males and hermaphrodites and/or constraints in the allocation of resources towards sex functions in hermaphrodites can balance the fitness components of selfing and outcrossing.ResultsUsing experimental evolution in Caenorhabditis elegans, we test whether the adaptive maintenance of partial selfing is due to sexual conflict and/or to the evolution of sex allocation towards male function in hermaphrodites. For this, we characterized the reproductive schedule and longevity patterns in hermaphrodites under selfing and under outcrossing with naïve males that did not have the opportunity to evolve with them. A shift in reproductive schedule towards earlier reproduction would be indicative of adaptation in our imposed life-cycle, while longevity is expected to evolve as a response to the harm that males impinge on hermaphrodites upon mating. To determine adaptation in the absence of constraints in sex allocation, we also characterized the life history of females that reproduced during experimental evolution through obligate mating with males. As expected with adaptation, we find that after 100 generations of experimental evolution, selfing hermaphrodites and females showed improved reproduction at earlier ages. We did not observe similar reproductive shifts in outcrossed hermaphrodites. We further find increased longevity in outcrossed females after evolution but not in outcrossed hermaphrodites, a result that indicates that sexual conflicts were likely more prevalent under male-female evolution than under male-hermaphrodite evolution.ConclusionsTaken together, our findings suggest that the adaptive maintenance of partial selfing during C. elegans experimental evolution resulted from the evolution of sex allocation towards male function in hermaphrodites.

Project description: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.

Dataset Information

Parallel genome-wide fixation of ancestral alleles in partially outcrossing experimental populations of Caenorhabditis elegans.

Publications

Parallel genome-wide fixation of ancestral alleles in partially outcrossing experimental populations of Caenorhabditis elegans.

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