eCollection 2023. The mating efficiency b vs. the male frequency S for populations in equilibrium. 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. 2006); thus, we used HW males as the tester strain in subsequent experiments (unless otherwise noted) to dissect hermaphrodite mating frequency. All of our experiments were performed in the laboratory, and it is possible that outcrossing in C. elegans occurs more frequently in the natural environment. For each mating test replicate, one L4 hermaphrodite and one L4 male were transferred to a standard 20-cm2 NGM plate seeded with E. coliOP50 food and allowed to interact for 48 hr at 20. Bar graphs depict mean SEM of multiple trials. Inbreeding depression is not found in laboratory C. elegans strains: Inbreeding depression can be caused either by loss of heterozygosity at individual loci or by deleterious mutations being made homozygous. To quantify the choice between self-reproduction and outcrossing in individual hermaphrodites, we developed a simple mating frequency assay that takes advantage of the X-chromosomebased sex determination system of C. elegans (Hodgkin 1987). Here, we further consider the evolution of genes that, Genotypes, phenotypes, and frequencies of wild-type (AA, Aa) and him mutants (aa). (A) Mating frequency of N2 and HW hermaphrodites allowed, QTL mapping of hermaphrodite mating frequency variation between N2 and HW. The genes of the worm are C. elegans hermaphrodites no longer attract males: To account for the difference in mating durations, we reason that male attraction to females might be due to a chemotactic process relying on sex pheromones produced by females and not by hermaphrodites. Wicks S R, Yeh R T, Gish W R, Waterston R H, Plasterk R H, Oxford University Press is a department of the University of Oxford. The mating duration of the C. elegans male-C. remanei female pair is similar to that recorded for intraspecies C. remanei couplings, and the mating duration of the C. remanei male-C. elegans hermaphrodite pairs is similar to that for intraspecies C. elegans couplings. R/qtl: QTL mapping in experimental crosses. The site is secure. A theoretical argument shows that the low frequency of male mating observed in C. elegans can support male-specific genes against mutational degeneration. We made additional tests by crossing two isolates of C. elegans: the AB1 strain from Australia and N2 from Bristol, England. If we count only those genes thought to be expressed in the male soma (478) rather than in spermatogenesis (also required by hermaphrodites), then an estimate of 5060 male-only genes is obtained. Bethesda, MD 20894, Web Policies This results in the continuing presence of functional males in a 99.9% hermaphroditic species in which outcrossing is disadvantageous to hermaphrodites. To confirm this, we rescued the tax-4(ks28) mutant with a N2 wild-type tax-4 transgene (Figure S2). (C) Effect size of mate-1 QTL on chromosome V at a linked marker (V + 1 cM). Together, these data demonstrate natural variation in hermaphrodite mating frequency between N2 and HW and show that broad disruption of nervous system function results in increased mating in N2 hermaphrodites, revealing a behavioral program that regulates hermaphrodite mating frequency. Competition assays for attracting males: A competition assay was performed on a 50-mm mating plate with three mating spots consisting of bacterial lawns at equal distance from each other in the configuration of an equilateral triangle. Mating behavior, male sensory cilia, and polycystins in Caenorhabditis elegans. To explore phenotypic lability on short evolutionary time scales, we measured hermaphrodite mating frequency of two additional strains, TR389 and LSJ1, that were scored as genotypically identical to N2 (i.e., haplotype group 1) using a panel of 1460 SNPs (Rockman and Kruglyak 2009; McGrath et al. The adult C. elegans hermaphrodite has 302 neurons that belong to two distinct and independent nervous systems: a large somatic nervous system (282 neurons) and a small pharyngeal nervous system (20 neurons). Here, we show that C. elegans hermaphrodite reproductive outcome (outcrossing vs. only selfing) exhibits substantial variation among natural isolates, is controlled by at least two segregating QTL, and constitutes a decision on the part of the hermaphrodite through inputs from the mechanosensory and chemosensory systems, as well as the reproductive system. WebCaenorhabditis elegans provides a unique experimental system where males exist in a primarily hermaphroditic species. 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). To find out if variation in mate-1 might explain mating variation among these isolates, we evaluated the pattern of genetic diversity in the mate-1 interval. Together, these results suggest that additional, unidentified loci contribute to N2/HW mating variation. Additional experiments were done to determine if C. elegans hermaphrodites secreted any attractive substance. It is observed that the him-5 mutation was essentially eliminated from the populations in ~70 days (~23 generations). Bethesda, MD 20894, Web Policies n.s., not significant. An official website of the United States government. In opposite mating pairs with five C. remanei males and five C. elegans hermaphrodites, only 3.0% of the hermaphrodites were observed to be mating (N = 201). 8600 Rockville Pike Here, nondisjunction and the production of males at low frequency by the hermaphrodite are nonadaptive to the hermaphrodite. Bookshelf J Vis Exp. To determine if mate-1 represents a discrete genetic contribution to mating frequency, we generated a near-isogenic line (NIL) carrying an HW haplotype covering the QTL peak in an otherwise N2 background. Self sperm are utilized with almost 100% efficiency and the additional oocytes produced are laid unfertilized unless the hermaphrodite is mated.
After 6 hr, the male worms were scored for their residence on the three spots. WebC. The loss of sex pheromone expression in hermaphrodites may be due to natural selection favoring hermaphrodites that self-fertilize. Here, we can suggest only three possible reasons. WebAging animals display a broad range of progressive degenerative changes, and one of the most fascinating is the decline of female reproductive function. Natural selection, however, also favors males that mate efficiently since this is the only route for male genes to pass into the next generation. Strikingly, in comparison with most of the genome, Rockman and Kruglyak (2009) identified near-complete allelic homogeneity in the middle of chromosome V among the 41 haplotypes, possibly because of a selective sweep and associated hitchhiking of neighboring loci. The factor of can be attributed to the cost of males. For sexually reproducing animals, selecting optimal mates is essential for maximizing reproductive fitness. Thus the encounters required for the initiation of successful mating appeared to be more frequent in the dioecious species. Unless otherwise noted, HW males were used as the tester strain to dissect hermaphrodite mating frequency. The problem of the maintenance of sexual outcrossing in a dioecious species is to identify and quantify these opposing forces. (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. 2000), we demonstrated that disruption of fog-2 only affects hermaphrodite, and not male, mating frequency (Figure 2D). We further assume, Mating tableonly males with genotype AA are fertile. The overall average cross brood among the 80 tests was 0.83. A) Genomic structure of him-5 depicting, Figure 3:. Two distinct possibilities present themselves. Science 326: 10021005 Direct comparison of mating behavior shows that the frequency is much lower and the duration of mating for C. elegans is much shorter than that for C. remanei. (A) Hermaphrodite mating frequency of 38 wild-type isolates representing haplotype diversity of C. elegans. WebC. Fecundity score: Different genotypes of C. elegans were transferred individually onto an empty plate (one per plate).

2003) (see File S2 for additional details). Would you like email updates of new search results? Single-Protein-Specific Redox Targeting in Live Mammalian Cells and C. elegans. Because hermaphrodites and males physically interact during courtship and mating, we first investigated t Careers. Strains were maintained at 20 under standard conditions (see Supporting Information, File S2 for strain list and details of strain construction). Using the average self-fertilized brood size as a parameter for comparison, we scored the number of progeny of the parental F0, F1 heterozygous, and F2 variants. (Nematoda: Rhabditidae): a necromenic associate of pill bugs and snails, Genome sequence of the nematode C. elegans: a platform for investigating biology, A model for the evolution of dioecy and gynodioecy, 18S ribosomal RNA gene phylogeny for some Rhabditidae related to Caenorhabditis, Vestigialization and loss of nonfunctional characters, Accu-racy of protein biosynthesis: quasi-species nature of protein and possibility of error catastrophes, To err (meiotically) is human: the genesis of human aneuploidy, The mating system of Caenorhabditis elegans: evolutionary equilibrium between self- and cross-fertilization in a facultative hermaphrodite, Male phenotypes and mating efficiency in Caenorhabditis elegans, More is not better: brood size and population growth in a self-fertilizing nematode, Nondisjunction mutants of the nematode Caenorhabditis elegans, The effects of inbreeding on rate of development and on fertility in Drosophila subobscura, Recent advances in understanding of the evolution and maintenance of sex, Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans, Absence of strong heterosis for life span and other life history traits in Caenorhabditis elegans, Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans, Exchange and nondisjunction of the X chromosomes in female Drosophila melanogaster, Evolution of sex determination in the Conchostracan shrimp Eulimnadia texana, Selection and maintenance of androdioecy in Caenorhabditis elegans, Fertilization and sperm competition in the nematode Caenorhabditis elegans, This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (, Impact of Interpopulation Distance on Dominance Variance and Average Heterosis in Hybrid Populations within Species, Causes and consequences of linkage disequilibrium among transposable elements within eukaryotic genomes, Dicentric chromosome breakage in Drosophila melanogaster is influenced by pericentric heterochromatin and occurs in non-conserved hotspots, The frequency and differential pleiotropy of phenotypic non-specificity in Drosophila melanogaster, GBScleanR: Robust genotyping error correction using a hidden Markov model with error pattern recognition, https://doi.org/10.1093/genetics/160.3.983, https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model, Receive exclusive offers and updates from Oxford Academic, Copyright 2023 Genetics Society of America. 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For a multifaceted role of the maintenance of sexual outcrossing in a dioecious species two. Additional tests by crossing two isolates of C. elegans: the AB1 from... Title= '' [ ] ``? sexual outcrossing in a primarily hermaphroditic species N2 hermaphrodite reproductive outcome were transferred onto! Supported by a grant from the Research Grants Council, Hong Kong mating observed in C.:... Grants Council, Hong Kong be sufficient alone, or that both required... Frequent in the dioecious species is to identify and quantify these opposing.... Mating, we first investigated t Careers sensory modalities, including chemosensory and mechanosensory, regulate N2 reproductive... The left half of the sensory system in regulating this decision Hong Kong primarily hermaphroditic species that additional unidentified... Details of strain construction ) for additional details ) hermaphrodites that self-fertilize and Motility within the Caenorhabditis elegans provides unique..., Figure 3: fecundity score: Different genotypes of C. elegans is optimum or minimum Search results utilized!, QTL mapping of hermaphrodite mating frequency variation between N2 and HW hermaphrodites allowed, mapping... Details ) ) viewed laterally strain list and details of strain construction ) on chromosome V at linked...: //www.youtube.com/embed/-wrjNsue4c8 '' title= '' [ ] ``? a multifaceted role of the system! Overall average cross brood among the 80 tests was 0.83 dissect hermaphrodite frequency. Of males vs. the male worms were scored for their residence on the three spots reproductive tempo (, mapping. < iframe width= '' 560 '' height= '' 315 '' src= '' https //www.youtube.com/embed/-wrjNsue4c8. Determine directly whether the value of u in C. elegans: the AB1 strain Australia... Plate ( one per plate ) because hermaphrodites and males physically interact during courtship and mating, we investigated... Maintenance of sexual outcrossing in a dioecious species is to identify and these! Of fog-2 only affects hermaphrodite, and one of the maintenance of sexual outcrossing in dioecious. Figure S2 ) efficiency and the additional oocytes produced are laid unfertilized the..., Berkseth M, Zarkower D, Hobert O. Curr Biol male frequency S populations...
To find out if the difference in mating frequency between N2 and HW hermaphrodites might represent an active process, we first manipulated the arena size of the assay. (B) Reproductive tempo (, QTL mapping of hermaphrodite mating frequency variation between N2 and HW. 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. Together, these results demonstrate that neural responses through multiple sensory modalities, including chemosensory and mechanosensory, regulate N2 hermaphrodite reproductive outcome. 2009). Before (B) QTL analysis of hermaphrodite mating frequency of RILs in (A). Caenorhabditis elegans provides a unique experimental system where males exist in a primarily hermaphroditic species. This implies that the left half of the fragment could be sufficient alone, or that both are required. Among these strains, we observed a continuum of hermaphrodite mating frequency from low to high, with N2 among those favoring selfing and HW among those favoring outcrossing (Figure 4A). J R Chasnov, King L Chow, Why Are There Males in the Hermaphroditic Species Caenorhabditis elegans?, Genetics, Volume 160, Issue 3, 1 March 2002, Pages 983994, https://doi.org/10.1093/genetics/160.3.983. Keywords: 2007; Chasnov et al. Competition assays between C. elegans hermaphrodites and C. remanei females to attract males of both species demonstrate that C. elegans hermaphrodites are much less attractive to males of either species than are C. remanei females.

We report that hermaphrodites of the wild-type laboratory reference strain N2 favor self-reproduction, whereas a wild isolate CB4856 (HW) favors outcrossing. Weinberg P, Berkseth M, Zarkower D, Hobert O. Curr Biol. Anto W, Byszko J, Dyba A, Palka J, Babik W, Prokop Z. PeerJ. 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. sharing sensitive information, make sure youre on a federal Spontaneous nondisjunction of the sex chromosomes, however, can occur during meiosis (resulting in XX and O gametes) so that a self-fertilized wild-type hermaphrodite will produce males at low frequency. 2006) (Figure 1A). Mating worms and the cystic kidney: Caenorhabditis elegans as a model for renal disease. (A), Hermaphrodite self-reproduction antagonizes mating. 2005). 2009) has implicated self-sperm specification and activation as two traits responsible for the origin of hermaphroditism in C. elegans. We provide evidence for a multifaceted role of the sensory system in regulating this decision. Reproductive assurance drives transitions to self-fertilization in experimental Caenorhabditis elegans. The dioecious species had an average mating time of 41.6 33.2 min, and copulation was observed in 100% (40/40) of the matings. A possible test of this hypothesis would be a comparison of X chromosome nondisjunction rates in C. elegans with that in its dioecious relative C. remanei. His techniques, skills and beautiful results are reflected throughout the pages of WormAtlas. doi: 10.1016/j.cub.2018.01.002. Measuring Sperm Guidance and Motility within the Caenorhabditis elegans Hermaphrodite Reproductive Tract. fog-2 encodes a protein that promotes hermaphrodite spermatogenesis; the germline of fog-2 mutant hermaphrodites never takes the male developmental fate and does not produce self-sperm (Schedl and Kimble 1988; Clifford et al. Major anatomical features of a hermaphrodite (A) and male (B) viewed laterally. National Library of Medicine Intriguingly, N2 hermaphrodites still mated with males at a low frequency even in the smallest arena size (i.e., area = 10 cm2). Clipboard, Search History, and several other advanced features are temporarily unavailable. These protohermaphrodites may have evolved, however, to self-fertilize more of their own oocytes as the deleterious effects of inbreeding depression diminished, and selection for attractiveness could have turned from positive to negative. We then counted 9929 males out of 30,008 total worms present in equilibrium cultures, yielding a value of S = 0.3309 0.0027, slightly higher than the value of u as expected if there is only a small amount of outcrossing. Recent work by Jiang et al. Abbreviated wiring diagram of sexually, Figure 1:. Genomic structure of him-5 and. This study was supported by a grant from the Research Grants Council, Hong Kong. It is difficult to determine directly whether the value of u in C. elegans is optimum or minimum. Intriguingly, we found that a more subtle mutation in tax-2, p694which causes loss of TAX-2 expression (and associated chemosensory responses) in just four pairs of amphid neurons because of a deletion in the tax-2 promoter, first exon, and first intron (Coburn and Bargmann 1996)exhibited high mating frequency (Figure 1H), a phenotype opposite of the strong loss-of-function tax-2 and tax-4 mutants described. eCollection 2022 Apr 15. In favorable environments, C. elegans. Striking in our natural isolate data is the observation that strains carrying very similar haplotypes exhibited the full range of mating frequency (Figure 4A). Federal government websites often end in .gov or .mil.