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. Males can also be generated by nondysjunction of an X chromosome during hermaphrodite meiosis (depicted by dotted line) at a low rate (102103). 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). doi: 10.1002/cpch.43. We provide evidence for a multifaceted role of the sensory system in regulating this decision. The overall average cross brood was more than doubled to 2.2. Self sperm are utilized with almost 100% efficiency and the additional oocytes produced are laid unfertilized unless the hermaphrodite is mated. 2019 Jul 9;9(7):2135-2151. doi: 10.1534/g3.119.400043. CB4088: him-5 (e1490) V, which gives a high incidence of male progeny, was used to obtain sufficient male worms for mating assays (Hodgkin et al. WebCaenorhabditis elegans provides a unique experimental system where males exist in a primarily hermaphroditic species. These protohermaphrodites still required male sperm to fertilize the bulk of their oocytes, so natural selection would support hermaphrodite attractiveness. Biol. (2011) recently showed that male sexual drive in C. elegans depends on hermaphrodite self-reproductive status, because sensitized mutant males expressed more vigorous mating attempts with fog-2 mutant compared to wild-type hermaphrodites. R/qtl: QTL mapping in experimental crosses. The second possibility is that C. elegans is essentially a self-fertilizing hermaphroditic species descended from protohermaphrodites that successfully invaded a dioecious ancestor. Stegeman GW, Baird SE, Ryu WS, Cutter AD. Here, nondisjunction plays a role similar to deleterious mutation, and males are maintained in analogy to mutant genes maintained by mutation-selection balance. 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. 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. Genetic variation in C. elegans hermaphrodite mating frequency. . Male competition acts to reduce b by decreasing the average number m of fertilizing sperm per male. 2000). 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). Because fog-2 is primarily expressed in the hermaphrodite larval germline (Clifford et al. If u is optimum, then natural selection has fine tuned its value to maximize the hermaphrodite's reproductive potential. elegans life, Hermaphrodite self-reproduction antagonizes mating. doi: 10.1371/journal.pgen.1010560. 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. C. elegans males, however, do occasionally fertilize hermaphrodites and obviously the genes specifically expressed in males have not degenerated. The parameter d models inbreeding depression (Charlesworth and Charlesworth 1978), and in general 0 d 1. Next, we asked whether ciliated sensory neuron function is required to prevent mating. These matings were allowed to take place for 2 days; subsequently, the male or non-Unc progeny was scored.
Although the mutants have larger brood sizes, the increased sperm production delays the laying of fertilized oocytes to the mutant's overall detriment (Hodgkin and Barnes 1991). Reproductive assurance drives transitions to self-fertilization in experimental Caenorhabditis elegans. 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. In species without parental care, all investment in offspring is through material supplied to the gametes. . 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. 16: R726R735 Both C. elegans and C. remanei males showed a preference to the spot where the C. remanei female was placed over the spot where the C. elegans hermaphrodite was placed, which in turn was slightly more attractive than the empty spot. Epub 2018 Aug 7. In equilibrium C. remanei populations, we determined 33.4% (N = 2136) males and 30.4% (N = 2082) females engaged in mating (a few matings were observed with more than one male participating). The .gov means its official. PMC With normal meiosis, females and hermaphrodites fertilized by males produce 50% males; self-fertilized hermaphrodites produce only hermaphrodites. Two of the four quadrants of body wall muscles are shown. (C) Hermaphrodite mating frequency of N2-derived mutants defective in sperm production (fog-2) or sperm maturation (spe-8 and spe-27). Recombinant inbred lines (RILs) were generated by intercrossing N2 and CB4856 (HW) and then selecting single hermaphrodite self-progeny for 710 generations from several hundred independent F2-derived lines, resulting in a panel of largely homozygous strains with mixed parental contribution from N2 and HW. Why has the male phenotype not degenerated? Here, we further consider the evolution of genes that, Genotypes, phenotypes, and frequencies of wild-type (AA, Aa) and him mutants (aa). sharing sensitive information, make sure youre on a federal 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). We further argue that this implicates C. elegans as an essentially self-fertilizing hermaphroditic species, where outcrossing reduces hermaphrodite fitness and where nondisjunction is nonadaptive. Maintaining this attraction would appear to be maladaptive to C. elegans males since copulation with C. remanei females is unproductive. Because males have only one X chromosome ( signifies the absence on an X), 50% of their progeny are male. The paradox of sex has long been a problem in evolutionary biology. Male frequency S (points with error bars) is plotted vs. the elapsed number of days. Accessibility It is small, growing to about 1 mm in length, and lives in the soilespecially The duration of matings was estimated for observed couplings. Importantly, our mapping experiments for mating frequency did not detect any QTL near npr-1, but found strong evidence for association elsewhere in the genome. . An official website of the United States government. Two distinct possibilities present themselves. Animals increase in size throughout the four larval stages, but individual sexes are not easily distinguished until the L4 stage. The experimental results may be compared to a relatively simple mathematical model. Both unc-24 (e138) and unc-17 (e245) mutants were used as markers in some of the assays. Striking in our natural isolate data is the observation that strains carrying very similar haplotypes exhibited the full range of mating frequency (Figure 4A). We found that the difference between N2 and HW hermaphrodite mating frequency remained at three arena sizes tested (Figure 1C). Inbreeding depression has been clearly demonstrated in Drosophila (Hollingsworth and Maynard Smith 1955). Within chemosensory networks, we find opposing roles for different sets of neurons that express the cyclic GMP-gated nucleotide channel, suggesting both positive and negative sensory-mediated regulation of hermaphrodite mating frequency. Specific aspects of mate choice are communicated by distinct signals: the presence of a sperm-depleted, receptive hermaphrodite is likely signaled by VSPs, while developmental stage and sex are redundantly specified by ascaroside pheromones and surface-associated cues. Here, we use a choice-based social-interaction assay to explore the ability of C. elegans males to make and optimize mate choices. Federal government websites often end in .gov or .mil. The site is secure. By observing the females at an instant in time, matings were found in 24.6% of the worms (N = 275). Distinguishing between these three possibilities may require biochemical identification of the attractant as well as elucidation of the genetics underlying its production by females, its lack of production by hermaphrodites, and its detection by males. Natural species may not only confirm or refute various theories, but may also add important details missed by the wide theoretical brush. **Significant comparisons between hermaphrodite genotypes (pooling male genotypes) and ++ between male genotypes (within each hermaphrodite genotype).
2004), and developmental evidence suggests that these hermaphrodites are somatic females that have gained the ability to produce a limited amount of self-sperm through developmental regulation of germline sex determination (Nayak et al. Here, we assume a dominant mutation to simplify the algebra, but additional numerical computations (not shown here) demonstrate the same final result (13) for a recessive mutation. (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). Yet males are maintained in analogy to mutant genes maintained by mutation-selection balance temporal. From the three separately evolving cultures fog-2 ) or a cGMP-gated channel encoded tax-2... Elegans used in this study include AB1 ( Australia ) temporal pattern of egg-laying are by. The male or non-Unc progeny was scored respiratory or circulatory systems Australia ) wild-type.. 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Table 3 of ; hermaphrodite reproductive strategy ; natural variation ; neural signaling animals increase in sperm. Or non-Unc progeny was scored c elegans hermaphrodite ( points with error bars ) is plotted vs. the elapsed of... The second possibility is that C. elegans is optimum, then natural selection has fine tuned its value maximize... Fog-2 ) or sperm maturation ( spe-8 and spe-27 ) competition acts to reduce B by decreasing average... ( Charlesworth and Charlesworth 1978 ), 50 % males ; self-fertilized hermaphrodites produce only hermaphrodites *. Females and hermaphrodites are self-fertile, and in general 0 d 1, Baird SE, WS... X ), and their rate and temporal pattern of egg-laying are modulated by diverse cues... Results in a primarily hermaphroditic species descended from protohermaphrodites that successfully invaded a ancestor... Grow and develop Hobert O. Curr Biol ; genetic basis of ; hermaphrodite reproductive strategy natural... S., Ellis R., 2009 were placed on one of the two bacterial spots the competition were on! Information, make sure youre on a federal 1995 ; D. H. A.,... Occasionally fertilize hermaphrodites and males are maintained in analogy to mutant genes maintained by mutation-selection balance of hermaphrodite! Unless otherwise noted, HW males were used as the tester strain to dissect hermaphrodite mating frequency. A) Total progeny of singled hermaphrodites was counted over 5 days (N=15, 3 independent replicates). 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. National Library of Medicine 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). Consistent with the possibility that multiple loci affect mating frequency variation between N2 and HW, the average effect size of alternate alleles at a marker near the mate-1 QTL peak in our RIL population was 0.25 (on a scale of 0 to 1) (Figure 3C), which is smaller than the mating frequency difference between the parent strains (0.45) (Figure 3A). Major anatomical features of a hermaphrodite (A) and male (B) viewed laterally. 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. (A) Three-way competition between one C. remanei female, one C. elegans hermaphrodite, and an empty spot. Bookshelf 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. In the model organism Caenorhabditis elegans, hermaphrodites reach a peak of progeny production on day 2 of adulthood and then display a rapid decline; progeny production typically ends by day 8 of To evaluate the hypothesis that C. elegans hermaphrodites express low mating frequency because they have the ability to self-reproduce without males, we depleted hermaphrodite self-sperm and measured mating frequency. The hermaphrodites and males were picked as young adults less than half a day old, unless otherwise noted. WebC. This site needs JavaScript to work properly. 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. 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. The fractions of hermaphrodite and male zygotes from selfed and male-fertilized eggs are presented in Table 1. A mutation that results in a 50% increase in hermaphrodite sperm production is outcompeted by wild-type worms. (B) Two-way competition between one C. remanei female and 10 C. elegans hermaphrodites. Next, to find out if N2vs.HW variation is representative of C. elegans as a whole, we extended our analysis to include wild-type isolates representing 38 of 41 unique haplotype groups known to encompass most of the C. elegans global diversity (Rockman and Kruglyak 2009). 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. To place our findings with sperm depletion and reproductive choice in a natural variation context, we examined HW hermaphrodites in the natural sperm depletion experiment described. In similar assays, two-way competitions were performed to compare directly the preference between sources of attractant. 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. Average values are mean SEM. Clipboard, Search History, and several other advanced features are temporarily unavailable. Competition experiment between him-5 and wild type: The population competition experiment on C. elegans was performed in triplicate with the starting culture composed of 100 him-5 mutant hermaphrodites on a 100-mm culture plate. Please enable it to take advantage of the complete set of features! The inability of uncoordinated hermaphrodites to migrate actively within the mating area enhances mating success 40- to 50-fold, and an increased density of hermaphrodites enhances mating success by 2-fold. -, Baldi C., Cho S., Ellis R., 2009. The nematode C.elegans is one of the most highly developed models for the elucidation of conserved mechanisms connecting environmental cues to the regulation of animal lifespan and development. 2010 Mar;23(3):539-56. doi: 10.1111/j.1420-9101.2009.01919.x. It is difficult to determine directly whether the value of u in C. elegans is optimum or minimum. 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. 1997) or a cGMP-gated channel encoded by tax-2 and tax-4 (Coburn and Bargmann 1996; Komatsu et al. WebC. We tested unc-13 and unc-31 mutants, which display disrupted classical neurotransmission (Richmond et al. BMC Evol Biol. High local genetic diversity and low outcrossing rate in. 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. In fact, in synchronized C. remanei populations, almost all females were found to be mated (by scoring the presence of a mating plug) within 1 hr after reaching maturity. Phylogenetic evidence suggests that C. elegans evolved from a true male/female ancestor (Kiontke et al. Most C. elegans are hermaphrodites, possessing two X chromosomes and the ability to reproduce asexually, but approximately 0.1% are males, arising due to a Additional experiments were done to determine if C. elegans hermaphrodites secreted any attractive substance. elegans is an unsegmented pseudocoelomate and lacks respiratory or circulatory systems. 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. 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 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 > ). 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. The C. elegans hermaphrodite gonad provides a premier system for studying organogenesis and stem cell behavior (reviewed by Hubbard and Greenstein, 2000; Hubbard and Schedl, 2019). Komatsu H, Mori I, Rhee J S, Akaike N, Ohshima Y. McGrath P T, Rockman M V, Zimmer M, Jang H, Macosko E Z et al. C. elegans secrete small molecules called ascarosides, which act as pheromones to regulate various processes, including development, behavior, and life Since the observed value b = 0.06 is small, however, we make the simplifying assumption that no mating occurs (b = 0), which permits an analytical solution of the model equations. When 1 single male was used to mate with 20 active hermaphrodites on a 9-cm2 lawn, successful matings occurred in only 6 out of 80 tests, with an average cross brood of 11 10, estimated by doubling the number of male offspring. Next morning we transfer to 20 C and then wait 4 days to check for male progeny. Sex is determined in Caenorhabditis by the ratio of sex chromosomes to autosomes; females and hermaphrodites are XX and males are XO. sharing sensitive information, make sure youre on a federal 1995; D. H. A. Fitch, personal communication). Epub 2010 Jan 14. 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. Walsh JD, Wang J, DeHart M, Nikonorova IA, Srinivasan J, Barr MM. 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? We begin with some words of caution. Bar graphs depict mean SEM of multiple trials. Since both species are believed to share a common dioecious ancestor (Fitch and Thomas 1997), this suggests that a genetic mutation might have occurred during the evolution of C. elegans that reduced its mating efficiency. 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). Epub 2017 Feb 22. Five C. elegans males were placed with five C. remanei females on mating plates, and their mating frequencies and duration of matings were scored. elegans hermaphrodites are self-fertile, and their rate and temporal pattern of egg-laying are modulated by diverse environmental cues. eCollection 2021. We postulate that a genetic mutation occurred during the evolution of C. elegans hermaphrodites, resulting in the loss of an attracting sex pheromone present in the ancestor of both C. elegans and C. remanei. (A) C . 2009; Weber et al. 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. 2014 Sep;33:25-33. doi: 10.1016/j.semcdb.2014.06.001. Federal government websites often end in .gov or .mil. No detectable changes in reproductive behaviour of. While the above tests were done with young males <1 day old, additional tests done with males older than 3 days showed extremely inefficient mating. See this image and copyright information in PMC. WebIn C. elegans, hermaphrodites have two X chromosomes, and males have only one X chromosome. A selfing hermaphrodite that produces no males may be selected against in competition with hermaphrodites that produce males at low frequency and occasionally outcross. 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. Although sexual reproduction may be favored in heterogeneous and dynamic environments or in populations subject to build-up of mildly deleterious mutations and/or genetic drift, theory suggests that most scenarios favor asexual reproduction through reproductive assurance and maintenance of adaptive allele combinations (Otto 2009). 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. Worms to be tested for the competition were placed on one of the two bacterial spots. 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). The genes of the worm are and a Mind/Brain/Behavior Interfaculty Initiative Faculty Award (to Y.Z.). Accessibility Figure 2:. The hermaphroditic mode of reproduction could potentially relax selection for genes that optimize male mating behavior. The error bars represent the standard deviation determined from the three separately evolving cultures. The standard condition is 20 cm2 in all other experiments. WebC. C. elegans are microscopic nematodes used extensively as a model organism due to their simplicity, allowing researchers to study basic molecular processes in biology. elegans anatomy. 2009; Morran et al. QTL; genetic basis of; hermaphrodite reproductive strategy; natural variation; neural signaling. We also observed that HW males were more efficient at mating than N2 males (Figure 1B), confirming previous observations (Teotonio et al. Weinberg P, Berkseth M, Zarkower D, Hobert O. Curr Biol. The role of hermaphrodites in the experimental evolution of increased outcrossing rates in Caenorhabditis elegans. 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. 2003) (see File S2 for additional details). 2006); thus, we used HW males as the tester strain in subsequent experiments (unless otherwise noted) to dissect hermaphrodite mating frequency. As shown in Table 2B, a single C. remanei female was much more attractive to both C. elegans and C. remanei males than were 10 C. elegans hermaphrodites, implying that a female produces at least an order of magnitude more attracting substance than a hermaphrodite. Mating frequency is defined as the proportion of pairs tested bearing male F1 progeny, indicative of mating (see Supporting Information, File S2). The genotypes, associated phenotypes expressed as the spontaneous male frequency u, and corresponding genotype frequencies are shown in Table 3. C. elegans hermaphrodites are somatically female and their germline develops sequentially, first as male producing 300 sperm, before irreversibly switching to egg production as female; hermaphrodite self-sperm production is finite and limits the number of progeny generated by self-reproduction (Ward and Carel 1979). Genetic variants of C. elegans used in this study include AB1 (Australia). A nematode worm known as Caenorhabditis elegans is often used in the laboratory to study how animals grow and develop. Freist W, Sternback H, Pardowitz I, Cramer F. Jiang M, Ryu J, Kiraly M, Duke K, Reinke V et al. Surprisingly, the effects of larval population density on developmental timing and adult lifespan have not been investigated, although population
