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Selfing is the safest sex for Caenorhabditis tropicalis.

ABSTRACT: Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, Caenorhabditis tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple Medea-like elements, genetically consistent with maternal toxin/zygotic antidote systems. Loci with Medea activity harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating Medea elements dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid Medea-mediated outbreeding depression.

SUBMITTER: Noble LM

PROVIDER: S-EPMC7853720 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Selfing is the safest sex for Caenorhabditis tropicalis.

Noble Luke M LM Yuen John J Stevens Lewis L Moya Nicolas N Persaud Riaad R Moscatelli Marc M Jackson Jacqueline L JL Zhang Gaotian G Chitrakar Rojin R Baugh L Ryan LR Braendle Christian C Andersen Erik C EC Seidel Hannah S HS Rockman Matthew V MV

eLife 20210111

Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, Caenorhabditis tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure ...[more]

PMID: 33427200

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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.

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Selfing is the safest sex for Caenorhabditis tropicalis.

Publications

Selfing is the safest sex for <i>Caenorhabditis tropicalis</i>.

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