All of these results imply that C. elegans males cannot mate efficiently in a normal cultured equilibrium population. With the caveat that these strains were collected over several decades and maintained in laboratory environments, this pattern of behavioral variation suggests that hermaphrodite mating frequency likely varies in natural populations. 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. E-mail: The evolution equation for the male frequency, with a prime denoting the frequency in the next generation, is determined to be, We can further determine the conditions under which males will be maintained in the worm population in the absence of sex chromosomal nondisjunction (, When sex chromosomal nondisjunction occurs (, The assumption of no mating as well as the initial absence of heterozygous genotypes leads to the evolution equation, that hermaphrodites of all genotypes average, The number of zygotes from different matings can be calculated. The brood sizes of selfing N2 and him-5 strains were measured prior to the experiment and found to be approximately equal: For N2, the brood size was 195 26 (134266, N = 40); for him-5, the brood size was 197 28 (118238, N = 27). Caenorhabditis elegans provides a unique experimental system where males exist in a primarily hermaphroditic species. Natural selection, however, also favors males that mate efficiently since this is the only route for male genes to pass into the next generation. 1996). Maintaining this attraction would appear to be maladaptive to C. elegans males since copulation with C. remanei females is unproductive. The mating efficiency of C. elegans is poor. The differences in mating durations are thus determined by the C. remanei female or the C. elegans hermaphrodites and not by the males. 8600 Rockville Pike As expected, we identified a major QTL centered on npr-1 (Figure S3), which encodes a G-protein-coupled receptor with a well-described polymorphism affecting various C. elegans behaviors, including aggregation (de Bono and Bargmann 1998). C. elegans, as a species, appears to be far along the path toward complete self-reproduction, as evidenced by a suite of traits related to the degeneration of outcrossing, termed the selfing syndrome, such as reduced fitness of hybrid genotypes, reduced pheromonal attraction from hermaphrodites, and diminished male function in mating tests (Garcia et al. One hundred fifty-nine RILs were tested in the hermaphrodite mating frequency assay, and partial genotypes of RILs were obtained by scoring a well-defined marker set (Davis et al. (A) The dorsal nerve cord (DNC) and ventral nerve cord (VNC) run along the entire length of the animal from the nerve ring. Moreover, when tested in a separate experiment on very large plates (area = 175 cm2), HW hermaphrodites still exhibited relatively high mating frequency (63%, N = 24 pairs) compared to N2 (9%, N = 22 pairs) (P < 0.001), showing that HW hermaphrodites are highly prone to mating even when the encounter rate is likely to be low. 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. 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. For sexually reproducing animals, selecting optimal mates is essential for maximizing reproductive fitness.

Thus, we speculate that an additional step in the evolution of hermaphroditism is to reinforce self-reproduction through behavioral expression of reduced mating. Hermaphrodite mating frequency segregated among 158 RILs (Figure 3A), and we uncovered two QTL explaining a significant proportion of the phenotypic variation, one major QTL in the middle of chromosome V and one weaker QTL on the right side of chromosome IV, which we named mate-1 and mate-2, respectively (Figure 3B). C. elegans are microscopic nematodes used extensively as a model organism due to their simplicity, allowing researchers to study basic molecular processes in biology. The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS).

2023 Jan 10;11:e14572. We observed that osm-6 mutant hermaphrodites exhibited high mating frequency, similar to HW (Figure 1F). (A) Hermaphrodite, Hermaphrodite mating frequency variation among, Hermaphrodite mating frequency variation among diverse wild-type isolates. QTL mapping was conducted using interval mapping (using the imputation algorithm to account for partial RIL genotypes) as implemented in rQTL (Broman et al. Sexually Dimorphic unc-6/Netrin Expression Controls Sex-Specific Maintenance of Synaptic Connectivity. 2007) suggests that early C. elegans hermaphrodites may have been more attractive or willing to mate with males than they are today. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. Would you like email updates of new search results? This finding suggests variation among isolates regarding how self-reproductive cues are used to regulate mating vs. selfing. Interestingly, the two sexes of C. elegans have conflicting interests: Hermaphrodites want to self and males want to mate. Occasional matings were observed with males displaying an active vulva searching behavior when associated with hermaphrodites. The average brood size of heterozygous AB1/N2 F1 worms was 175 24 (138227, N = 40); the F2 worms had an average brood size of 176 45 (71269, N = 50). Curr. 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. 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. This work was supported from a Harvard Microbial Science Initiative Postdoctoral Fellowship (to A.K.B.) 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.

Why are C. elegans males still attracted to C. remanei females if their conspecific hermaphrodites are no longer attractive? A deterministic model is constructed for the evolution of the frequency of males in the population under the usual simplifying assumptions of very large population size and discrete generations.

elegans. 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. 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. Average values are mean SEM. Epub 2010 Jan 14. By comparison, C. elegans males do not require fog-2 to produce sperm and use two redundant signaling pathways (involving spe-8/spe-27 or try-5) to activate sperm (Smith and Stanfield 2011).

In a parallel test with a mating lawn of 0.5 cm diameter, 100% successful matings were achieved (N = 30), with an average cross brood of 120 45. Additional experiments were done to determine if C. elegans hermaphrodites secreted any attractive substance. National Library of Medicine It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. 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. Collet J, Spike C A, Lundquist E A, Shaw J E, Herman R K. Davis M W, Hammarlund M, Harrach T, Olsen S, Jorgensen E M. Kiontke K, Gavin N P, Raynes Y, Roehrig C, Piano F et al. We can rephrase these two possibilities as the following question: Is the frequency u of male offspring produced by nondisjunction in a selfing hermaphrodite optimum or minimum? E-mail: Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. undergoes reproductive development and progresses rapidly from embryo through four larval stages (L1L4) to See this image and copyright information in PMC. 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. C. elegans has been used as a model organism to study human diseases ranging from Parkinsons disease to mitochondrial diseases, as well as studying the The parameter d models inbreeding depression (Charlesworth and Charlesworth 1978), and in general 0 d 1. Because the nematode C. elegans reproduces mostly Single-Protein-Specific Redox Targeting in Live Mammalian Cells and C. elegans. We observed that both unc-13 and unc-31 mutant hermaphrodites exhibited high mating frequency, similar to HW (Figure 1D). Egg-laying behavior has served as an important phenotypic assay for the genetic dissection of

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Genetic variants of C. elegans used in this study include AB1 (Australia). elegans anatomy. 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. 2011), and our results show that hermaphrodite mating frequency can be a labile trait, possibly because of a large mutational target of genes that regulate reproductive decision. This site needs JavaScript to work properly. We find that males use a combination of volatile sex pheromones (VSPs), ascaroside pheromones, surface-bound chemical cues, and other signals to robustly assess a variety of features of potential mates. A lack of mating vigor comparable to C. elegans would likely drive a dioecious species extinct. (B) Reproductive tempo (i.e., self-progeny and self-sperm depletion) of isolated hermaphrodites in the period after the same treatment in (A). It is small, growing to about 1 mm in length, and lives in the soilespecially We also show that the ability to self-reproduce negatively regulates hermaphrodite mating. We have thus argued that males are not present in the C. elegans species because of any advantage to outcrossing, as is usually supposed. In humans, aneuploidythe most common types being trisomy 21 (causing Down's syndrome) and sex chromosome trisomiesoccurs in 0.3% of all newborns, and it is estimated that 5% of all human conceptions are aneuploid (Hassold and Hunt 2001). NOTE: Your email address is requested solely to identify you as the sender of this article. The mating success of males was further improved when 20 uncoordinated hermaphrodites were used to mate with a single male. eCollection 2022 Apr 15. A theoretical argument shows that the low frequency of male mating observed in C. elegans can support male-specific genes against mutational degeneration. Epub 2017 Feb 22. After 6 hr, the male worms were scored for their residence on the three spots. 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. Unable to load your collection due to an error, Unable to load your delegates due to an error. Our results indicate a small preference for live worms over an empty spot (the P values indicate only marginal significance), but no preference for hermaphrodites over males. -. We now review the laboratory facts before addressing the question posed by this article's title: No obvious fitness advantage of outcrossed offspring is observed. 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. 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.

2005; Baldi et al. Clipboard, Search History, and several other advanced features are temporarily unavailable. Early works of John Sulston, Robert Horvitz, and If so, then why are there still males present in the C. elegans species? The gain of self-reproduction through self-sperm production is expected to select for reduction in the mating drive of these newly evolved hermaphrodites. 1998). The site is secure. To explore this possibility, we conducted cross-species mating tests between males and females or hermaphrodites. elegans life, Hermaphrodite self-reproduction antagonizes mating. Webc elegans hermaphrodite (21) 4108-0454 c elegans hermaphrodite sac@bemreciclagem.com.br standard enthalpy of formation of hexane WhatsApp. 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). In fact, the ability of C. elegans to both self-fertilize and outcross has rendered it a powerful genetic model for developmental studies, and well-established laboratory procedures as well as readily available mutants facilitate experimentation. HHS Vulnerability Disclosure, Help Ten to 12 young males (C. elegans him-5 or C. remanei) were transferred to the center of the plate equally distant from the three bacterial spots. The wild isolates and different genetic strains used in this study were kindly provided by the Caenorhabditis Genetics Center, Minnesota, which is supported by the National Institutes of Health National Center for Research Resources. Curr Biol. The hermaphrodites and males were picked as young adults less than half a day old, unless otherwise noted. as a good in vivo model system in the field of radiation biology. The male-specificity of these behavioral responses is determined by both male-specific neurons and the male state of sex-shared circuits, and we reveal an unexpected role for the sex-shared ASH sensory neurons in male attraction to endogenously produced hermaphrodite ascarosides. Careers.

As a consequence, under laboratory conditions hermaphrodites that both self and outcross produce substantially more progeny than hermaphrodites that only self (Ward and Carrel 1979). A further simplifying approximation considers all the male-only expressed genes to be tightly linked. 2020 Sep-Dec;34(3-4):259-272. doi: 10.1080/01677063.2020.1837799. 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. If, for instance, C. elegans males never successfully mate with hermaphrodites, then an adaptive organ such as the sensory rays would be expected to degenerate, and C. elegans might evolve into a hermaphroditic species without males. This result is analogous to that found by Kleeman and Basolo (2007), showing that mating behavior is positively correlated with self-sperm depletion. Here, nondisjunction and the production of males at low frequency by the hermaphrodite are nonadaptive to the hermaphrodite. The result (10), with U = 0.3257 and n = D/3, where D is the number of elapsed days in the experiment, 3 days is the estimate for the generation length of C. elegans, and c = 0.02 (2 wild-type and 100 him-5 hermaphrodites at n = 0), can be compared directly to the laboratory measurements and is the solid curve in Figure 2. With the emergence of CRISPR, a seemingly limitless tool for generating genomic mutations with pinpoint precision, the C. elegans model system will continue to be a useful instrument for pioneering research in the fields of behavior, reproductive biology, and neurogenetics. 1997) or a cGMP-gated channel encoded by tax-2 and tax-4 (Coburn and Bargmann 1996; Komatsu et al. This implies that the left half of the fragment could be sufficient alone, or that both are required. Despite the ease of this asexual self-fertilisation, the hermaphrodite still prefers to be fertilised by a different male. (This result in itself is puzzling because the substantially larger nondisjunction rate for him-5 should result in autosomal nondisjunctions as well as zygotes with sex chromosome genotypes O, XXX, and XXXX. Some of the experiments were repeated using unc-17 or wild-type hermaphrodites to confirm that the results were independent of the specific Unc mutants employed in the assays. Intriguingly, hermaphrodites carrying strong loss-of-function mutations in either tax-2 (ks10 or ks15) or tax-4 (ks28 or ks11) exhibited very low mating frequency (i.e., even lower than N2) (Figure 1G). C. elegans males mate effectively with C. remanei females: Our observations make it evident that the dioecious species C. remanei is more efficient at mating than C. elegans. 2009). Furthermore, we hypothesize that the nondisjunction rate found in C. elegans is as low as possible without incurring excessive costs. Observed matings were timed. Although almost all tested isolates carry a Bristol (i.e., N2) allele across the mate-1 region, yet we observed continuous variation in hermaphrodite mating frequency (Figure 4A), we conclude that the mate-1 QTL identified between N2 and HW cannot solely explain the pattern of phenotypic diversity observed across this panel of isolates. (C) Two-way competition between one dead C. remanei female and an empty spot. It is largely unknown how behaviors evolve after a major shift in life history. Our results highlight the coexistence of self-reproduction and outcrossing in C. elegans as a strategic game and identify hermaphrodite behavior as an important axis of variation regulating this trade-off. The question we address here is: How often must males successfully mate with hermaphrodites to prevent male genes from degenerating? Hermaphrodite mating frequency variation among diverse wild-type isolates.

The fractions of hermaphrodite and male zygotes from selfed and male-fertilized eggs are presented in Table 1. Fecundity score: Different genotypes of C. elegans were transferred individually onto an empty plate (one per plate). Accordingly, we consider a wild-type gene A expressed only in males such that male genotypes AA average m fertilizing sperm per male, and male genotypes Aa and aa average none; i.e., these genotypes are sterile because of degeneration. WebC. Search for other works by this author on: Corresponding author: Department of Biology, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong. 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. C. elegans secrete small molecules called ascarosides, which act as pheromones to regulate various processes, including development, behavior, and life 2001). After intervals of 23 days, when the food was finished or the cultures had a large number of L1 larvae, the worms were washed off the plate into a 1.5-ml Eppendorf tube. Because hermaphrodites and males physically interact during courtship and mating, we first investigated the requirement of a set of mechanosensory neurons to prevent mating in N2 hermaphrodites. Surprisingly, the effects of larval population density on developmental timing and adult lifespan have not been investigated, although population Bethesda, MD 20894, Web Policies 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. Our results exemplify the simple idea that without a substantial number of matings between males and hermaphrodites, a hermaphrodite that produces a male instead of a hermaphrodite reduces its effective fecundity. Phylogenetic evidence suggests that their common ancestor was dioecious (Fitch and Thomas 1997) so that an evolutionary study of these two species may serve as a useful model for understanding the maintenance of outcrossing against invasion by selfing hermaphrodites. 2006); thus, we used HW males as the tester strain in subsequent experiments (unless otherwise noted) to dissect hermaphrodite mating frequency. 4) These advantages make . The duration of matings was estimated for observed couplings. Mating worms and the cystic kidney: Caenorhabditis elegans as a model for renal disease. doi: 10.1002/cpch.43. Thus the encounters required for the initiation of successful mating appeared to be more frequent in the dioecious species. McCloskey RJ, Fouad AD, Churgin MA, Fang-Yen C. J Neurophysiol. 2009; Morran et al. eCollection 2023. PLoS One. -, Barriere A., Felix M.-A., 2005. Two distinct possibilities present themselves. We begin with some words of caution.

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