Maintaining this attraction would appear to be maladaptive to C. elegans males since copulation with C. remanei females is unproductive. The above stability condition is similar to one found previously (Otto et al. PLoS Genet. Are C. elegans hermaphrodites descended from modified females capable of spermatogenesis that successfully invaded the ancestral dioecious species? 2022 Dec 27;18(12):e1010560. Bar graphs depict mean SEM of multiple trials. (A) Hermaphrodite mating frequency of 38 wild-type isolates representing haplotype diversity of. **Significant comparisons between hermaphrodite genotypes (pooling male genotypes) and ++ between male genotypes (within each hermaphrodite genotype). The number of progeny produced by each individual was averaged over the total test worms to reflect the fecundity of the parental worms of specific genotype. The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Natural selection acts more strongly on earlier than later produced progeny. elegans is an unsegmented pseudocoelomate and lacks respiratory or circulatory systems. In addition, sperm maturation in C. elegans hermaphrodites requires spe-8 and spe-27 signal transduction (LHernault et al. Intriguingly, N2 hermaphrodites still mated with males at a low frequency even in the smallest arena size (i.e., area = 10 cm2). The mating success of males was further improved when 20 uncoordinated hermaphrodites were used to mate with a single male. To further simplify the model, we make the reasonable assumption that selfed offspring of genotype other than XO and XX (e.g., XXX), which occur at low frequency due to nondisjunction of the sex chromosomes, are nonviable. Here, we explore mechanisms underlying female reproductive choice in the nematode Caenorhabditis elegans, a species in which females have evolved the ability to produce their own self-fertilizing sperm, thereby allowing these "hermaphrodites" the strategic choice to self-reproduce or outcross with males. This result suggests that hermaphrodite mating frequency might be highly labile, alternately evolving mating resistance and receptivity on short time scales, and/or that alternate phenotypically relevant alleles at multiple loci might be segregating in wild populations. (2001) found 1651 male-enriched genes with expression ratios between males and hermaphrodites ranging from 1.5 to 110. These results indicate that some tax-2/tax-4expressing neurons normally promote hermaphrodite mating. (A) Hermaphrodite mating frequency of 38 wild-type isolates representing haplotype diversity of C. elegans. Early works of John Sulston, Robert Horvitz, and John White provided a complete map of the hermaphrodite nervous system, and recently the male nervous system was added. , Oxford University Press is a department of the University of Oxford. Worms to be tested for the competition were placed on one of the two bacterial spots. Observation of matings: Mating behavior in an equilibrium population of C. elegans him-5 mutants and C. remanei was monitored by direct observation every 5 min under a dissecting microscope. The https:// ensures that you are connecting to the C. elegans hermaphrodites reproduce by internal self-fertilization, so that copulation with males is not required for species propagation. doi: 10.7717/peerj.14572. We provide evidence for a multifaceted role of the sensory system in regulating this decision. The closeness of the two nondisjunction rates for the worm and the fly, both below that of mammals, lends some support to our claim that the nondisjunction rate in C. elegans is not significantly elevated. Bar graphs depict mean SEM of multiple trials. The authors thank Dr. Man-Yu Wong for statistical advice, colleagues in the laboratory for critical comments on this manuscript, and an anonymous referee for his extensive comments and important suggestions. These matings were allowed to take place for 2 days; subsequently, the male or non-Unc progeny was scored. 1996). J Evol Biol. Striking in our natural isolate data is the observation that strains carrying very similar haplotypes exhibited the full range of mating frequency (Figure 4A). The standard condition is 20 cm2 in all other experiments. We consider the dynamics of a population consisting of a mixture of him mutants and wild-type worms, assuming that both phenotypes have the same brood size and differ only in the frequency of selfed spontaneous males. Male competition acts to reduce b by decreasing the average number m of fertilizing sperm per male. To map genetic variation, we created recombinant inbred lines and identified two QTL that explain a large portion of N2 HW variation in hermaphrodite mating frequency. Two two-way competition experiments were performed: one C. elegans hermaphrodite vs. an empty spot, presented in Table 2D, and 10 C. elegans hermaphrodites vs. 10 C. elegans males, presented in Table 2E. Genetic variants of C. elegans used in this study include AB1 (Australia). Bar graphs depict mean SEM of multiple trials. We further note that the observed nondisjunction rate in C. elegans is at a level similar to errors occurring in other cellular functions, e.g., an error rate of 0.031% for amino acid incorporation during translation (Freist et al. If natural selection favored hermaphrodites with an increased level of X chromosome nondisjunction, resulting in the birth of a significant number of spontaneous males, then the rate of nondisjunction in C. elegans hermaphrodites should be significantly higher than that found in C. remanei females, for which X chromosome nondisjunction has no obvious adaptive purpose. Thank you for your interest in spreading the word about bioRxiv. To characterize underlying neural mechanisms, we show that N2 hermaphrodites deficient in mechanosensation or chemosensation (e.g., mec-3 and osm-6 mutants) exhibit high mating frequency, implicating hermaphrodite perception of males as a requirement for low mating frequency. To explore this possibility, we first performed an assay for attracting males with a three-way competition between an empty spot with only a bacterial lawn, a second spot with a C. elegans hermaphrodite, and a third spot with a C. remanei female. The X chromosome nondisjunction rate in D. melanogaster was thus determined to be 0.00058 0.00011, where we have estimated the error from the binomial distribution. If u is minimum, however, then natural selection has favored hermaphrodites with genes that reduce u to a value as small as possible without incurring excessive costs in resources. Thus, as an assay for mating frequency, we placed one virgin L4 hermaphrodite and one virgin L4 male on standard laboratory plates (6-cm diameter with E. coli as food) and scored the sex of the progeny after 2 d of potential interaction (see File S2). Self sperm are utilized with almost 100% efficiency and the additional oocytes produced are laid unfertilized unless the hermaphrodite is mated. C. elegans are microscopic nematodes used extensively as a model organism due to their simplicity, allowing researchers to study basic molecular processes in biology. Specifically, fog-2 appears to be a recently derived C. elegans lineage-specific gene required for hermaphrodites to produce sperm (Nayak et al. 2005) with additional markers (Wicks et al. (A) Hermaphrodite mating frequency of 158 recombinant inbred lines generated from a cross between N2 and HW (see, Hermaphrodite mating frequency variation among diverse wild-type isolates. All genes face a constant mutation pressure and those genes required to build the sensory rays, say, can be maintained only if they enhance the reproductive success of males. Unless otherwise noted, HW males were used as the tester strain to determine the propensity of hermaphrodite genotypes to mate or only self (see File S2 for additional details). Intriguingly, we further show that 40 wild isolates representing C. elegans global diversity exhibit extensive and continuous variation in hermaphrodite reproductive outcome. (A), Hermaphrodite self-reproduction antagonizes mating. elegans is a non-hazardous, non-infectious, non-pathogenic, non-parasitic organism. Genetics 134: 455464 Accessibility It would thus appear that the amount of gene flow from males to future generations is sufficient to prevent the mutational degeneration of the male phenotype even for the limiting case of tight linkage. (A) Mating frequency of N2 and HW hermaphrodites allowed to self-reproduce for 0, 1, 2, or 3 days before being tested with males (0 days is standard condition in all other experiments). Subsequent analysis has shown that these strains harbor a variety of sequence differences relative to N2 as a result of possible laboratory evolution (McGrath et al. 2020 Sep-Dec;34(3-4):259-272. doi: 10.1080/01677063.2020.1837799. In these experiments, uncoordinated hermaphrodites were employed to inhibit migration. We further assume, Mating tableonly males with genotype AA are fertile. (E) Two-way competition between 10 C. elegans hermaphrodites and 10 C. elegans males. 2000), we demonstrated that disruption of fog-2 only affects hermaphrodite, and not male, mating frequency (Figure 2D). G3 (Bethesda). . Sexually Dimorphic unc-6/Netrin Expression Controls Sex-Specific Maintenance of Synaptic Connectivity. We examined an osm-6 mutant, which has altered morphology of ciliated sensory neurons resulting in reduced perception of a variety of stimuli, including olfactory and gustatory cues (Collet et al. 1996). Despite the ease of this asexual self-fertilisation, the hermaphrodite still prefers to be fertilised by a different male. As a test of this hypothesis, we conducted a competition experiment using a wild-type N2 strain to compete against a mutant him-5 strain. n.s., not significant. The dashed line is the value for b obtained by measuring u and S from a him-5 mutant population. Genomic structure of him-5 and mutagenesis strategy. In a 9-cm2 lawn mating test, there were 23 successful matings in 30 tests, with an average cross brood per mating of 55 23 and an overall average of 42. official website and that any information you provide is encrypted PLoS One. We chose to further characterize the mate-1 QTL. The evolution from females to hermaphrodites results in a sexual conflict over mating in androdioecious nematode worms and clam shrimp. WebHere, using C. elegans as a model organism, we study the roles of a recently discovered enzyme at the heart of metabolism in mammalian cells, glycerol-3-phosphate The free-living nematode worm Caenorhabditis elegans reproduces primarily as a self-fertilizing hermaphrodite, yet males are maintained in wild-type populations at low frequency. Rather, we speculate that an internal cue, representing self-reproductive status in mature adults, informs mating behavior generated by the nervous system. It is also possible that we have missed some advantage of outcrossing that appears intermittently and perhaps only in the natural environment. We found that the difference between N2 and HW hermaphrodite mating frequency remained at three arena sizes tested (Figure 1C). eCollection 2022 Apr 15. elegans hermaphrodites are self-fertile, and their rate and temporal pattern of egg-laying are modulated by diverse environmental cues. A parthenogenetic female or a self-fertilizing hermaphrodite that produces no male offspring could potentially double her number of grandchildren (Maynard Smith 1978) and invade a dioecious population unless there are opposing selective forces. To characterize underlying neural mechanisms, we show that N2 hermaphrodites deficient in mechanosensation or chemosensation (e.g., mec-3 and osm-6 mutants) exhibit high mating frequency, implicating hermaphrodite perception of males as a requirement for low mating frequency. Anto W, Byszko J, Dyba A, Palka J, Babik W, Prokop Z. PeerJ. 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His techniques, skills and beautiful results are reflected throughout the pages of WormAtlas. Bar graphs depict mean SEM of multiple trials. This site needs JavaScript to work properly. Careers. Since the mating efficiency b is much less than unity, C. elegans males are not nearly as productive as the males of a dioecious species. Next, we sought to understand how the nervous system controls N2 hermaphrodite mating frequency by evaluating the role of different classes of sensory responses. Together, our findings demonstrate that C. elegans hermaphrodites actively regulate the choice between selfing and crossing, highlight the existence of natural variation in hermaphrodite choice, and lay the groundwork for molecular dissection of this evolutionarily important trait. The opposite effects of loss-of-function of osm-6 or tax-2/tax-4 raised the possibility that different sets of sensory neurons may play opposing roles in regulating hermaphrodite mating. In this article, however, guided by a mathematical model of the C. elegans genetic system, we perform laboratory observations and experiments that show that hermaphrodites have lost their attractiveness to males, resulting in a low frequency of outcrossing. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. [11] Most of these nematodes are hermaphrodites and a few are males. Intriguingly, we found opposite effects on mating frequency for two sets of sensory neurons expressing TAX channels (Figure 1, G and H). In similar assays, two-way competitions were performed to compare directly the preference between sources of attractant. (2009). Freist W, Sternback H, Pardowitz I, Cramer F. Jiang M, Ryu J, Kiraly M, Duke K, Reinke V et al. 1994). Epub 2018 Feb 8. WebC. Arena sizes tested ( Figure 1C ) some advantage of outcrossing that intermittently... 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