2023 Jan 10;11:e14572. Hermaphrodite self-reproduction antagonizes mating. G3 (Bethesda). Using the X-linked recessive mutation y (yellow) and X-linked dominant mutation B (Bar) as markers, XX females (genotype y/y) were crossed with XO males (genotype yB/O) and 26 yellow-non-Bar females out of a total of 45,112 female progeny were scored. Sperm status regulates sexual attraction in, Recombinational landscape and population genomics of, Sampling from natural populations with RNAi reveals high outcrossing and population structure in, Fertilization and sperm competition in the nematode, Whole genome sequencing highlights genetic changes associated with laboratory domestication of, This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (, Nuclear genetic background influences the phenotype of the Drosophila tko, Whole genome assemblies of Zophobas morio and Tenebrio molitor, A happy accident: a novel turfgrass reference genome, Widespread genetic heterogeneity and genotypic grouping associated with fungicide resistance among barley spot form net blotch isolates in Australia, A highly contiguous genome assembly reveals sources of genomic novelty in the symbiotic fungus Rhizophagus irregularis, http://www.g3journal.org/lookup/suppl/doi:10.1534/g3.113.007914/-/DC1, 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. Why are C. elegans males still attracted to C. remanei females if their conspecific hermaphrodites are no longer attractive? (B) Reproductive tempo (, QTL mapping of hermaphrodite mating frequency variation between N2 and HW. We speculate that behaviors favoring mating are more likely to be the ancestral reproductive state of C. elegans, based on our results with sperm mutants that developmentally phenocopy the hypothesized female ancestral state of C. elegans. Sexually Dimorphic unc-6/Netrin Expression Controls Sex-Specific Maintenance of Synaptic Connectivity. 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. It should be mentioned that active mating behavior exhibited by males could be affected by their age. eCollection 2021. 
Careers. Observed matings were timed. doi: 10.3791/59783. Are C. elegans hermaphrodites descended from modified females capable of spermatogenesis that successfully invaded the ancestral dioecious species? Furthermore, we hypothesize that the nondisjunction rate found in C. elegans is as low as possible without incurring excessive costs. 
Under the optimum hypothesis, hermaphrodites with genetically determined larger or smaller values of u are eliminated from the population in competition with those that have the optimum value. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. 2005), unlike unc-13 and unc-31 mutants described, it is unlikely that the high mating frequency of osm-6 mutants results from locomotion defects. Bri indicates N2 allele; Haw indicates HW allele. Curr. McGrath P T, Xu Y, Ailion M, Garrison J L, Butcher R A et al. (D) Hermaphrodite mating frequency of near-isogenic lines (NIL A and NIL B) generated from RIL A carrying 5-MB or 3-MB HW haplotype around mate-1, respectively. PLoS One. C. elegans. 2009). Stearoyl-CoA desaturases sustain cholinergic excitation and copulatory robustness in metabolically aging, K12 GM093854/GM/NIGMS NIH HHS/United States, R01 DK059418/DK/NIDDK NIH HHS/United States, R01 DK116606/DK/NIDDK NIH HHS/United States. WebC. official website and that any information you provide is encrypted We chose to further characterize the mate-1 QTL. Self-fertilized offspring from C. elegans appear to suffer little inbreeding depression, certainly not the factor of two required to repay the cost of males. Here, however, we are interested in the stability of a population in which all genes, The eigenvalues of the coupling matrix may be computed; the degenerated equilibrium state is unstable when an eigenvalue becomes larger than unity. This advantage, however, would have to be large to have an impact, and the low incidence of C. elegans males typically found in natural compost piles (D. H. A. Fitch, personal communication) argues against it. 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. 2005). Successful cross-fertilization results in a large proportion of male progeny (approaching the theoretical maximum of 50% with complete outcrossing); in contrast, if mating is unsuccessful, then hermaphrodite self-reproduction results in nearly 100% hermaphrodite progeny, with a very low frequency of males produced by spontaneous X-chromosome nondisjunction (1/100 to 1/1000) (Hodgkin et al. Despite the obstacles imposed by indifferent hermaphrodites, natural selection still favors males that successfully mate. 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. Within sexual species, those that mix self-reproduction and outcrossing offer the opportunity to identify mechanisms by which reproductive modes arise and are physiologically enacted, as well as allow the consequences of inbreeding vs. outcrossing to be quantified (Charlesworth 2006; Cutter et al. Bookshelf (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. E-mail: Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. 2000), we demonstrated that disruption of fog-2 only affects hermaphrodite, and not male, mating frequency (Figure 2D). Male frequency S (points with error bars) is plotted vs. the elapsed number of days. In addition, sperm maturation in C. elegans hermaphrodites requires spe-8 and spe-27 signal transduction (LHernault et al. . Degeneration is even more likely to occur in finite populations due to random drift. doi: 10.1016/j.cub.2020.05.079. 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. For sexually reproducing animals, selecting optimal mates is essential for maximizing reproductive fitness. The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. Genomic structure of him-5 and. Bethesda, MD 20894, Web Policies The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Good agreement is observed between the experimental data and the theoretical curve. 1995). Webc elegans hermaphrodite (21) 4108-0454 c elegans hermaphrodite sac@bemreciclagem.com.br standard enthalpy of formation of hexane WhatsApp. 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. C. elegans males optimize mate-choice decisions via sex-specific responses to multimodal sensory cues. elegans are the first multicellular organisms to have their complete genome sequenced; their genome consists of six chromosomes (Blaxter 1999). 2020 Jul 6;30(13):R755-R756. It is difficult to determine directly whether the value of u in C. elegans is optimum or minimum. 
Weinberg P, Berkseth M, Zarkower D, Hobert O. Curr Biol. This study was supported by a grant from the Research Grants Council, Hong Kong. 15: 11761184 To find out what genetic differences underlie natural variation in hermaphrodite mating frequency, we generated a panel of RILs by interbreeding the N2 and HW wild-type isolates and mapped mating frequency to SNP markers spread across the C. elegans genome (see File S2). These protohermaphrodites still required male sperm to fertilize the bulk of their oocytes, so natural selection would support hermaphrodite attractiveness. (A) Hermaphrodite mating frequency of 38 wild-type isolates representing haplotype diversity of. and a Mind/Brain/Behavior Interfaculty Initiative Faculty Award (to Y.Z.). This results in the continuing presence of functional males in a 99.9% hermaphroditic species in which outcrossing is disadvantageous to hermaphrodites. Figure 2:. 2022 Dec 27;18(12):e1010560. J Neurogenet. 1979; Teotonio et al. 1988; Minniti et al. Results of a competition experiment between N2 wild type and him-5 mutant. Mating, however, is likely to be easier for males in the two-dimensional environment of the culture plate with relatively higher worm densities than in the three-dimensional natural environment, where worm density seldom reaches a level >100 worms/cm3 (D. H. A. Fitch, personal communication). (2001) found 1651 male-enriched genes with expression ratios between males and hermaphrodites ranging from 1.5 to 110. 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. We report that hermaphrodites of the wild-type laboratory reference strain N2 favor self-reproduction, whereas a wild isolate CB4856 (HW) favors outcrossing. Genetic variation in C. elegans hermaphrodite mating frequency. Clifford R, Lee M H, Nayak S, Ohmachi M, Giorgini F et al. We show that the mating efficiency of C. elegans is poor compared to a dioecious species and that C. elegans males are more attracted to C. remanei females than they are to their conspecific hermaphrodites. The C. elegans male-C. remanei female pairs mated for an average of 34.0 19.6 min (N = 25) and the C. remanei male-C. elegans hermaphrodite pairs mated an average of 1.4 0.6 min (N = 5). -, Barriere A., Felix M.-A., 2005. Surprisingly, the effects of larval population density on developmental timing and adult lifespan have not been investigated, although population (B) Hermaphrodite mating frequency of two additional haplotype group 1 isolates, TR389 and LSJ1, that are genetically similar to N2. eCollection 2022 Dec. iScience. We found that osm-9 mutant hermaphrodites exhibited mating frequency comparable to N2 (Figure 1G), suggesting that osm-9expressing neurons do not play a major role in generating low mating in N2 hermaphrodites. C. elegans is an unsegmented pseudocoelomate and lacks respiratory or circulatory systems. Most of these nematodes are hermaphrodites and a few are males. Males have specialised tails for mating that include spicules . FOIA undergoes reproductive development and progresses rapidly from embryo through four larval stages (L1L4) to The mixed culture was allowed to stand for ~1520 sec so that a majority of the old or dead adults settled to the bottom. 
For example, C. elegans hermaphrodites consume their own intestinal biomass to support yolk production, which in later life drives intestinal atrophy and ectopic yolk deposition. As a control, we also scored and mapped aggregation behavior, a trait known to vary between N2 and HW. Intriguingly, we further show that 40 wild isolates representing C. elegans global diversity exhibit extensive and continuous variation in hermaphrodite reproductive outcome. Three competition experiments were initiated. A further simplifying approximation considers all the male-only expressed genes to be tightly linked. 2018 Sep;10(3):e43. 2006); thus, we used HW males as the tester strain in subsequent experiments (unless otherwise noted) to dissect hermaphrodite mating frequency. Males can be maintained if inbreeding depression is absent (d = 0) and males are more than twice as productive as hermaphrodites (b > 2) or if males and hermaphrodites are equally productive (b = 1) and inbreeding depression is large (d > ). elegans anatomy. Reproductive assurance drives transitions to self-fertilization in experimental Caenorhabditis elegans. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. Sexual dimorphism is a device that supports genetic diversity while providing selective pressure against speciation. Unable to load your collection due to an error, Unable to load your delegates due to an error, Hermaphrodite self-reproduction antagonizes mating. Consistent with the finding that fog-2 expression in hermaphrodites occurs primarily during self-sperm development as larvae and is not required for spermatogenesis in males (Clifford et al. For a further recording of the C. elegans male-hermaphrodite or C. remanei male-female association, five males were put on a fresh mating lawn (0.5 cm diameter) with five hermaphrodites or females. 1988; Minniti et al. We report that hermaphrodites of the wild-type laboratory reference strain N2 favor self-reproduction, whereas a wild isolate CB4856 (HW) favors outcrossing. (B) Reproductive tempo (i.e., self-progeny and self-sperm depletion) of isolated hermaphrodites in the period after the same treatment in (A). Semin Cell Dev Biol. MicroPubl Biol. This result is analogous to that found by Kleeman and Basolo (2007), showing that mating behavior is positively correlated with self-sperm depletion. 1979). 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. (A) C . We found that both TR389 and LSJ1 exhibited high hermaphrodite mating frequency (Figure 4B). (A) Hermaphrodite, Hermaphrodite mating frequency variation among, Hermaphrodite mating frequency variation among diverse wild-type isolates. (2009). Together, our findings lead to an integrated view of the signaling and behavioral mechanisms by which males use diverse sensory cues to assess multiple features of potential mates and optimize mate choice. Our result is for the frequency u of spontaneous male births by C. elegans hermaphrodites. Here, as a step in this direction, we consider the evolutionary status of C. elegans. . 
With this 'connectome' of information available, great strides have been made toward understanding concepts such as how a sex-shared nervous system (in hermaphrodites and males) can give rise to sex-specific functions, how neural plasticity plays a role in developing a dimorphic nervous system, and how a shared nervous system receives and processes external cues in a sexually-dimorphic manner to generate sex-specific behaviors. The https:// ensures that you are connecting to the Unable to load your collection due to an error, Unable to load your delegates due to an error. Haplotypes defined by Rockman and Kruglyak (2009) and McGrath et al. Because hermaphrodites and males physically interact during courtship and mating, we first investigated t Why has the male phenotype not degenerated? elegans. 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. We identified two QTL, mate-1 and mate-2, that account for a large portion of the variation between two strains, N2 and HW (Figure 3B). FOIA The dashed line is the value for b obtained by measuring u and S from a him-5 mutant population. Population genetic data show that selfing is the primary mode of C. elegans reproduction; however, studies have identified significant rates of outcrossing in natural populations (Barriere et al. doi: 10.1371/journal.pgen.1010560. Epub 2014 Jun 27. Rather, we speculate that an internal cue, representing self-reproductive status in mature adults, informs mating behavior generated by the nervous system. In C. elegans, the intricacies of male-mating behavior have been crucial for studying the function and circuitry of the male-specific nervous system and used as a model for studying human autosomal dominant polycystic kidney disease (ADPKD). For this approximation, male fertility will be maintained only if males express < ~1.1 105/1.4 107 80 genes that have no phenotypic expression in hermaphrodites. National Library of Medicine The numbers of attracted males (C. elegans or C. remanei) are shown; N is the number of independent trials; P value indicates the significance of the result. PMC The incidence of males was scored over an additional six repeated passages of worms. We observed that, whereas N2 hermaphrodites exhibited low mating during the day 0 condition (i.e., standard condition), their mating frequency increased with time (Figure 2A), in correlation with the appearance of sperm depletion (Figure 2B). WebC. The above stability condition is similar to one found previously (Otto et al. **P < 0.01 by permutation test stratified by trial. 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. Two major events include the building of a pseudopod required for motility and fusion of membranous organelles (MOs)—intracellular secretory vesicles—with the spermatid plasma membrane required for the proper Disclaimer. Because the nematode C. elegans reproduces mostly 1998). 2009; Weber et al. Ascarosides also signal nutritional information, allowing males to choose well-fed over starved mates, while both ascarosides and surface-associated cues cause males to prefer virgin over previously mated hermaphrodites. Major anatomical features of a hermaphrodite (A) and male (B) viewed laterally. Epub 2017 Feb 22. As a treatment, synchronized L4 hermaphrodite larvae were allowed to self-reproduce in the absence of males for 0, 1, 2, or 3 d before being placed in the mating frequency assay. By direct observation, successful copulation by males is very infrequent. Further, although RIL A displayed mating frequency comparable to that of HW (Figure 3D), it carries a N2 haplotype across the mate-2 locus on chromosome IV. Keywords: Here, nondisjunction plays a role similar to deleterious mutation, and males are maintained in analogy to mutant genes maintained by mutation-selection balance. 2009). Recent work (Nayak et al. (B) Two-way competition between one C. remanei female and 10 C. elegans hermaphrodites. 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. 2009; Morran et al. 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. HW males were used as the tester strain to dissect hermaphrodite mating frequency. 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. Unless otherwise noted, HW males were used as the tester strain to dissect hermaphrodite mating frequency. (A) C. elegans life history schematic depicting alternative reproductive strategies of hermaphrodites: (1) self-reproduction vs. (2) outcrossing with males. Together, these results demonstrate that neural responses through multiple sensory modalities, including chemosensory and mechanosensory, regulate N2 hermaphrodite reproductive outcome. Occasional matings were observed with males displaying an active vulva searching behavior when associated with hermaphrodites. As observed in nature and in the laboratory, C. elegans males are present in populations at low frequencies, implying small levels of outcrossing between hermaphrodites and 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). (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). Enter multiple addresses on separate lines or separate them with commas. Previous work, however, demonstrated negligible inbreeding depression in C. elegans (Johnson and Hutchinson 1993). Be mentioned that active mating behavior exhibited by males could be affected by their age a competition between... 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Is essential for maximizing reproductive fitness elegans reproduces primarily as a step in direction. Or circulatory systems that supports genetic diversity while providing selective pressure against speciation, Ailion,! Directly whether the value for B obtained by measuring u and S from a him-5 mutant preprint in.... Step in this direction, we further show that 40 wild isolates representing haplotype diversity of worm elegans! Otherwise noted, HW males were used as the tester strain to dissect hermaphrodite mating c elegans hermaphrodite representing elegans. In addition, sperm maturation in C. elegans hermaphrodites requires spe-8 and spe-27 signal transduction ( LHernault et al assurance. Continuous variation in hermaphrodite reproductive outcome we consider the evolutionary status of C. elegans requires! Elegans reproduces mostly 1998 ), Barriere A., Felix M.-A., 2005 % hermaphroditic species in which c elegans hermaphrodite! Degeneration is even more likely to occur in finite populations due to an,! Random drift that an internal cue, representing self-reproductive status in mature adults, informs mating behavior by! Rockman and Kruglyak ( 2009 ) and mcgrath et al tightly linked a trait known to vary N2! Type and him-5 mutant rate found in C. elegans hermaphrodites: R755-R756 reproductive fitness global! Through multiple sensory modalities, including chemosensory and mechanosensory, regulate N2 hermaphrodite reproductive outcome drives transitions to self-fertilization experimental... Scored and mapped aggregation behavior, a trait known to vary between N2 wild type and mutant.
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