Abstract
BackgroundThe self-fertile hermaphrodite worm C. elegans is an important model organism for biology, yet little is known about the origin and persistence of the self-fertilizing mode of reproduction in this lineage. Recent work has demonstrated an extraordinary degree of selfing combined with a high deleterious mutation rate in contemporary populations. These observations raise the question as to whether the mutation load might rise to such a degree as to eventually threaten the species with extinction. The potential for such a process to occur would inform our understanding of the time since the origin of self-fertilization in C. elegans history.ResultsTo address this issue, here we quantify the rate of fitness decline expected to occur via Muller's ratchet for a purely selfing population, using both analytical approximations and globally distributed individual-based simulations from the evolution@home system to compute the rate of deleterious mutation accumulation. Using the best available estimates for parameters of how C. elegans evolves, we conclude that pure selfing can persist for only short evolutionary intervals, and is expected to lead to extinction within thousands of years for a plausible portion of parameter space. Credible lower-bound estimates of nuclear mutation rates do not extend the expected time to extinction much beyond a million years.ConclusionThus we conclude that either the extreme self-fertilization implied by current patterns of genetic variation in C. elegans arose relatively recently or that low levels of outcrossing and other factors are key to the persistence of C. elegans into the present day. We also discuss results for the mitochondrial genome and the implications for C. briggsae, a close relative that made the transition to selfing independently of C. elegans.
Highlights
The self-fertile hermaphrodite worm C. elegans is an important model organism for biology, yet little is known about the origin and persistence of the self-fertilizing mode of reproduction in this lineage
The genomic deleterious mutation rate, USDM, is the key parameter, which we obtained by scaling estimates of the total genomic mutation rate, UTOT by fSDM, the fraction of slightly deleterious mutations
From USDM we infer the rate of deleterious mutation accumulation and extrapolate it to the expected extinction times using estimates of C. elegans reproductive capacity and generation time
Summary
The self-fertile hermaphrodite worm C. elegans is an important model organism for biology, yet little is known about the origin and persistence of the self-fertilizing mode of reproduction in this lineage. Recent work has demonstrated an extraordinary degree of selfing combined with a high deleterious mutation rate in contemporary populations These observations raise the question as to whether the mutation load might rise to such a degree as to eventually threaten the species with extinction. The potential for such a process to occur would inform our understanding of the time since the origin of self-fertilization in C. elegans history. It is important to acquire a better understanding of how long hermaphrodites have persisted in the C. elegans lineage because a recent versus ancient origin of selfing will strongly influence our inferences from comparative analyses and population genetic patterns, and our interpretations about the adaptive nature of phenotypes. We explore this issue by considering the potential for extinction to occur by way of Muller's Ratchet [4,5,6] in the context of parameters that describe how C. elegans evolves
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