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Rapid decline in fitness of mutation accumulation lines of gonochoristic (outcrossing) Caenorhabditis nematodes.

ABSTRACT: Evolutionary theory predicts that the strength of natural selection to reduce the mutation rate should be stronger in self-fertilizing than in outcrossing taxa. However, the relative efficacy of selection on mutation rate relative to the many other factors influencing the evolution of any species is poorly understood. To address this question, we allowed mutations to accumulate for ?100 generations in several sets of "mutation accumulation" (MA) lines in three species of gonochoristic (dieocious) Caenorhabditis (C. remanei, C. brenneri, C. sp. 5) as well as in a dioecious strain of the historically self-fertile hermaprohodite C. elegans. In every case, the rate of mutational decay is substantially greater in the gonochoristic taxa than in C. elegans (?4× greater on average). Residual heterozygosity in the ancestral controls of these MA lines introduces some complications in interpreting the results, but circumstantial evidence suggests the results are not primarily due to inbreeding depression resulting from residual segregating variation. The results suggest that natural selection operates to optimize the mutation rate in Caenorhabditis and that the strength (or efficiency) of selection differs consistently on the basis of mating system, as predicted by theory. However, context-dependent environmental and/or synergistic epistasis could also explain the results.

SUBMITTER: Baer CF

PROVIDER: S-EPMC3001279 | biostudies-literature | 2010 Nov

REPOSITORIES: biostudies-literature

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Rapid decline in fitness of mutation accumulation lines of gonochoristic (outcrossing) Caenorhabditis nematodes.

Baer Charles F CF Joyner-Matos Joanna J Ostrow Dejerianne D Grigaltchik Veronica V Salomon Matthew P MP Upadhyay Ambuj A

Evolution; international journal of organic evolution 20101101 11

Evolutionary theory predicts that the strength of natural selection to reduce the mutation rate should be stronger in self-fertilizing than in outcrossing taxa. However, the relative efficacy of selection on mutation rate relative to the many other factors influencing the evolution of any species is poorly understood. To address this question, we allowed mutations to accumulate for ∼100 generations in several sets of "mutation accumulation" (MA) lines in three species of gonochoristic (dieocious ...[more]

PMID: 20649813

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Project description:BackgroundOutcrossing between populations can exert either positive or negative effects on offspring fitness. Cyclically parthenogenetic rotifers, like other continental zooplankters, show high genetic differentiation despite their high potential for passive dispersal. Within this context, the effects of outcrossing may be relevant in modulating gene flow between populations through selection for or against interpopulation hybrids. Nevertheless, these effects remain practically unexplored in rotifers. Here, the consequences of outcrossing on the rotifer Brachionus plicatilis were investigated. Cross-mating experiments were performed between a reference population and three alternative populations that differed in their genetic distance with regard to the former. Two offspring generations were obtained: F1 and BC ('backcross'). Fitness of the outcrossed offspring was compared with fitness of the offspring of the reference population for both generations and for three different between-population combinations. Four fitness components were measured throughout the rotifer life cycle: the diapausing egg-hatching proportion, clone viability (for the clones originating from diapausing eggs), initial net growth rate R for each viable clone, and the proportion of male-producing clones. Additionally, both the parental fertilisation proportion and a compound fitness measure, integrating the complete life cycle, were estimated.ResultsIn the F1 generation, hybrid vigour was detected for the diapausing egg-hatching proportion, while R was lower in the outcrossed offspring than in the offspring of the reference population. Despite these contrasting results, hybrid vigour was globally observed for the compound measure of fitness. Moreover, there was evidence that this vigour could increase with the genetic differentiation of the outcrossed populations. In the BC generation, the hybrid vigour detected for the egg-hatching proportion in the F1 generation reverted to outbreeding depression. By contrast, signs of hybrid vigour were observed for clone viability and R. The opposing trends observed for different life-cycle stages yielded a global pattern of hybrid vigour in the BC generation for two out of the three between-population comparisons.ConclusionsResults suggest that outbreeding depression does not constitute a barrier to gene flow. In newly-founded populations, where the population size is still small, dilution of immigrants should be low. Thus, a lack of outbreeding depression would allow gene flow to have an impact on the genetic composition of these populations.

Dataset Information

Rapid decline in fitness of mutation accumulation lines of gonochoristic (outcrossing) Caenorhabditis nematodes.

Publications

Rapid decline in fitness of mutation accumulation lines of gonochoristic (outcrossing) Caenorhabditis nematodes.

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