Dataset Information

Sex and Mitonuclear Adaptation in Experimental Caenorhabditis elegans Populations.

ABSTRACT: To reveal phenotypic and functional genomic patterns of mitonuclear adaptation, a laboratory adaptation study with Caenorhabditis elegans nematodes was conducted in which independently evolving lines were initiated from a low-fitness mitochondrial electron transport chain (ETC) mutant, gas-1 Following 60 generations of evolution in large population sizes with competition for food resources, two distinct classes of lines representing different degrees of adaptive response emerged: a low-fitness class that exhibited minimal or no improvement compared to the gas-1 mutant ancestor, and a high-fitness class containing lines that exhibited partial recovery of wild-type fitness. Many lines that achieved higher reproductive and competitive fitness levels were also noted to evolve high frequencies of males during the experiment, consistent with adaptation in these lines having been facilitated by outcrossing. Whole-genome sequencing and analysis revealed an enrichment of mutations in loci that occur in a gas-1-centric region of the C. elegans interactome and could be classified into a small number of functional genomic categories. A highly nonrandom pattern of mitochondrial DNA mutation was observed within high-fitness gas-1 lines, with parallel fixations of nonsynonymous base substitutions within genes encoding NADH dehydrogenase subunits I and VI. These mitochondrial gene products reside within ETC complex I alongside the nuclear-encoded GAS-1 protein, suggesting that rapid adaptation of select gas-1 recovery lines was driven by fixation of compensatory mitochondrial mutations.

SUBMITTER: Wernick RI

PROVIDER: S-EPMC6404257 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Sex and Mitonuclear Adaptation in Experimental Caenorhabditis elegans Populations.

Wernick Riana I RI Christy Stephen F SF Howe Dana K DK Sullins Jennifer A JA Ramirez Joseph F JF Sare Maura M Penley McKenna J MJ Morran Levi T LT Denver Dee R DR Estes Suzanne S

Genetics 20190122 3

To reveal phenotypic and functional genomic patterns of mitonuclear adaptation, a laboratory adaptation study with Caenorhabditis elegans nematodes was conducted in which independently evolving lines were initiated from a low-fitness mitochondrial electron transport chain (ETC) mutant, gas-1 Following 60 generations of evolution in large population sizes with competition for food resources, two distinct classes of lines representing different degrees of adaptive response emerged: a ...[more]

PMID: 30670540

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Project description:BACKGROUND: The 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. RESULTS: After 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. CONCLUSIONS: Sex 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.

Project description:BACKGROUND:Classic 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. RESULTS:Using 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. CONCLUSIONS:Taken 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.

Dataset Information

Sex and Mitonuclear Adaptation in Experimental Caenorhabditis elegans Populations.

Publications

Sex and Mitonuclear Adaptation in Experimental <i>Caenorhabditis elegans</i> Populations.

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