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. HHS Vulnerability Disclosure, Help n.s., not significant. Surprisingly, the effects of larval population density on developmental timing and adult lifespan have not been investigated, although population Because the nematode C. elegans reproduces mostly by self-fertilization, little is known about its mate-choice behaviors. Rather, hermaphrodites no longer attract males and obtain higher fitness by selfing. If so, then why are there still males present in the C. elegans species? Although the optimum reproductive strategy for a C. elegans hermaphrodite is to first self-fertilize its oocytes until all internal sperm are used and then outcross, natural selection acting on attractiveness alone cannot attain this optimum. It is difficult to determine directly whether the value of u in C. elegans is optimum or minimum. -, Broman K. W., Wu H., Sen S., Churchill G. A., 2003. An official website of the United States government. The fractions of hermaphrodite and male zygotes from selfed and male-fertilized eggs are presented in Table 1. Measurement of u and S and determination of b for a mutant him-5 strain: To obtain an estimate of the mating efficiency b used in the mathematical model, we took advantage of the mutant him-5 strain, which had been reported to produce ~30% males among the progeny of selfed hermaphrodites due to a high nondisjunction rate (Hodgkin et al. Zygotes with two X chromosomes develop as hermaphrodites, whereas zygotes with only one X chromosome develop as males. 2018 Feb 19;28(4):623-629.e3. 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. Male frequency S (points with error bars) is plotted vs. the elapsed number of days. Accessibility Our result is for the frequency u of spontaneous male births by C. elegans hermaphrodites. Two distinct possibilities present themselves. 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. Black points denote phenotypes of RILs with genotype data at this marker; gray points denote phenotypes of remaining RILs with imputed genotypes at this marker. 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). However, it is unlikely that the mate-1 locus is solely responsible for the observed continuous, quantitative phenotypic variation in the mating frequency among other wild-type isolates (Figure 4A), because the middle of chromosome V that spans the mate-1 locus exhibits almost no variation among these strains and nearly all strains carry an N2 allele (Rockman and Kruglyak 2009). Attractive hermaphrodites, however, may be mated quickly with the disadvantage that early progeny are 50% males, whereas early progeny of unattractive hermaphrodites are likely to be selfed and are thus 100% hermaphrodites. We observed that NIL A exhibited mating frequency significantly higher than N2 (Figure 3D), confirming that mate-1(HW) is sufficient to increase hermaphrodite mating. Early works of John Sulston, Robert Horvitz, and 2009). C. elegans are microscopic nematodes used extensively as a model organism due to their simplicity, allowing researchers to study basic molecular processes in biology. Hermaphrodites self-reproduce through internal self-fertilization with their own sperm and can outcross with males. J Exp Biol. 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). 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). The reproductive outcome of the interaction (i.e., outcrossing or only selfing) was quantified by scoring the presence or absence of males among the F1 progeny; presence of male progeny (typically 20100 among hundreds) was scored as "mating success," and absence of male progeny (2 males, but usually zero) was scored as "mating failure" (Figure S1). Please enable it to take advantage of the complete set of features! (E) Two-way competition between 10 C. elegans hermaphrodites and 10 C. elegans males. 2005) with additional markers (Wicks et al. Furthermore, as shown in Table 2C, when the C. remanei female was killed by a hot worm pick the carcass did not elicit the same attraction, suggesting that the attractant was emitted only by live females. (B) Reproductive tempo (i.e., self-progeny and self-sperm depletion) of isolated hermaphrodites in the period after the same treatment in (A). 2009). WebC. , Oxford University Press is a department of the University of Oxford. Plates where the female or hermaphrodite migrated from her home spot were discarded. In similar assays, two-way competitions were performed to compare directly the preference between sources of attractant. Egg-laying behavior has served as an important phenotypic assay for the genetic dissection of 4) These advantages make . 1998). Would you like email updates of new search results? official website and that any information you provide is encrypted C. elegans males optimize mate-choice decisions via sex-specific responses to multimodal sensory cues. Weber K P, De S, Kozarewa I, Turner D J, Babu M M et al. (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. Clifford R, Lee M H, Nayak S, Ohmachi M, Giorgini F et al. doi: 10.1371/journal.pgen.1010560. R/qtl: QTL mapping in experimental crosses. When the number of males and hermaphrodites was sampled, we found 9.1% (N = 1315) and 4.0% (N = 2798) of males and hermaphrodites, respectively, engaged in mating. (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). C. elegans; behavior; cilia; male; nervous system; polycystin; sexual dimorphism. Phylogenetic evidence suggests that C. elegans evolved from a true male/female ancestor (Kiontke et al. eCollection 2022 Apr 15. Striking in our natural isolate data is the observation that strains carrying very similar haplotypes exhibited the full range of mating frequency (Figure 4A). Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves. Out of these 40 matings, copulation was observed in only 2, both of which had. This NIL B exhibited low mating frequency, similar to N2 (Figure 3D), suggesting that the right half of the fragment is not sufficient to augment mating. We made additional tests by crossing two isolates of C. elegans: the AB1 strain from Australia and N2 from Bristol, England. Clipboard, Search History, and several other advanced features are temporarily unavailable. Results of a competition experiment between N2 wild type and him-5 mutant. Genomic structure of him-5 and. Caenorhabditis elegans provides a unique experimental system where males exist in a primarily hermaphroditic species. 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. 2003) (see File S2 for additional details). (B) QTL analysis of hermaphrodite mating frequency of RILs in (A). 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. Further, the observation that females of C. remanei, a closely related obligate outcrossing species, are much more attractive to heterospecific C. elegans males than are conspecific C. elegans hermaphrodites (Chasnov et al. (DH) Hermaphrodite mating frequency of N2-derived mutants defective in (D) neurotransmission (unc-13) or neurosecretion (unc-31), (E) mechanosensation to gentle touch (mec-3 and mec-4), (F) ciliated sensory neuron function (osm-6), (G) TRPV channel (osm-9) or cGMP-gated (tax-2 and tax-4) channelmediated sensory transduction in chemosensory neurons, and (H) cGMP-gated channel (tax-2) sensory transduction in only four sensory neurons. McGrath P T, Xu Y, Ailion M, Garrison J L, Butcher R A et al. 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. 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? National Library of Medicine The life-history transition from obligate to facultative outcrossing allows C. elegans hermaphrodites two reproductive options, but it is not clear to what extent they make a strategic choice between them, how that choice is regulated, or whether there is genetic variation in reproductive decision segregating in natural populations. It is observed that the him-5 mutation was essentially eliminated from the populations in ~70 days (~23 generations). Search for other works by this author on: Corresponding author: Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, 52 Oxford St, Cambridge, Massachusetts 02138. (A) The dorsal nerve cord (DNC) and ventral nerve cord (VNC) run along the entire length of the animal from the nerve ring. Stegeman GW, Baird SE, Ryu WS, Cutter AD. See this image and copyright information in PMC. Here, as a step in this direction, we consider the evolutionary status of C. elegans. Natural selection acts more strongly on earlier than later produced progeny. Rather, we propose that at least a subset of ciliated sensory neurons is required for N2 to resist mating with males. 2005; Sivasundar and Hey 2005), suggesting that hermaphrodite reproduction could be a naturally variable, regulated decision. We found that the difference between N2 and HW hermaphrodite mating frequency remained at three arena sizes tested (Figure 1C). 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. In fact, C. elegans males are significantly more attracted to C. remanei females than they are to hermaphrodites of their own species. government site. 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. While several sensory cues have been implicated in males' ability to recognize hermaphrodites, achieving an 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. The increase in mating frequency of NIL A relative to N2 is similar to the mean effect size estimated from the RIL population (Figure 3C), but it cannot fully explain the difference between N2 and HW or RIL A. In the context of generating NIL A, which contains the entire 5-MB HW fragment covering mate-1 from RIL A, we also obtained a recombinant that lost the left half of the HW fragment in the region, leaving a 3-MB introgression. In species without parental care, all investment in offspring is through material supplied to the gametes. (A) The dorsal nerve cord (DNC) and ventral nerve cord (VNC) run along Of note, Morsci et al. 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. 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. 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. Fecundity score: Different genotypes of C. elegans were transferred individually onto an empty plate (one per plate). Mainstream theories divide possible forces into two broad categories: Either sexual outcrossing produces recombinant types that are better able to adapt to a changing environment, or sex more efficiently eliminates deleterious mutations (Crow 1994; Hurst and Peck 1996). To determine the role of males in C. elegans, we develop a mathematical model for the genetic system of hermaphrodites that can either self-fertilize or be fertilized by males and we perform laboratory observations and experiments on both C. elegans and a related dioecious species C. remanei. This implies that the left half of the fragment could be sufficient alone, or that both are required. 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. The site is secure. 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. A lack of mating vigor comparable to C. elegans would likely drive a dioecious species extinct. 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. 1996). 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. Elegans ; behavior ; cilia ; male ; nervous system ; polycystin sexual! 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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. Black points denote phenotypes of RILs with genotype data at this marker; gray points denote phenotypes of remaining RILs with imputed genotypes at this marker. 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). However, it is unlikely that the mate-1 locus is solely responsible for the observed continuous, quantitative phenotypic variation in the mating frequency among other wild-type isolates (Figure 4A), because the middle of chromosome V that spans the mate-1 locus exhibits almost no variation among these strains and nearly all strains carry an N2 allele (Rockman and Kruglyak 2009). Attractive hermaphrodites, however, may be mated quickly with the disadvantage that early progeny are 50% males, whereas early progeny of unattractive hermaphrodites are likely to be selfed and are thus 100% hermaphrodites. We observed that NIL A exhibited mating frequency significantly higher than N2 (Figure 3D), confirming that mate-1(HW) is sufficient to increase hermaphrodite mating. Early works of John Sulston, Robert Horvitz, and 2009). C. elegans are microscopic nematodes used extensively as a model organism due to their simplicity, allowing researchers to study basic molecular processes in biology. Hermaphrodites self-reproduce through internal self-fertilization with their own sperm and can outcross with males. J Exp Biol. 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). 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). The reproductive outcome of the interaction (i.e., outcrossing or only selfing) was quantified by scoring the presence or absence of males among the F1 progeny; presence of male progeny (typically 20100 among hundreds) was scored as "mating success," and absence of male progeny (2 males, but usually zero) was scored as "mating failure" (Figure S1). Please enable it to take advantage of the complete set of features! (E) Two-way competition between 10 C. elegans hermaphrodites and 10 C. elegans males. 2005) with additional markers (Wicks et al. Furthermore, as shown in Table 2C, when the C. remanei female was killed by a hot worm pick the carcass did not elicit the same attraction, suggesting that the attractant was emitted only by live females. (B) Reproductive tempo (i.e., self-progeny and self-sperm depletion) of isolated hermaphrodites in the period after the same treatment in (A). 2009). WebC. , Oxford University Press is a department of the University of Oxford. Plates where the female or hermaphrodite migrated from her home spot were discarded. In similar assays, two-way competitions were performed to compare directly the preference between sources of attractant. Egg-laying behavior has served as an important phenotypic assay for the genetic dissection of 4) These advantages make . 1998). Would you like email updates of new search results? official website and that any information you provide is encrypted C. elegans males optimize mate-choice decisions via sex-specific responses to multimodal sensory cues. Weber K P, De S, Kozarewa I, Turner D J, Babu M M et al. (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. Clifford R, Lee M H, Nayak S, Ohmachi M, Giorgini F et al. doi: 10.1371/journal.pgen.1010560. R/qtl: QTL mapping in experimental crosses. When the number of males and hermaphrodites was sampled, we found 9.1% (N = 1315) and 4.0% (N = 2798) of males and hermaphrodites, respectively, engaged in mating. (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). C. elegans; behavior; cilia; male; nervous system; polycystin; sexual dimorphism. Phylogenetic evidence suggests that C. elegans evolved from a true male/female ancestor (Kiontke et al. eCollection 2022 Apr 15. Striking in our natural isolate data is the observation that strains carrying very similar haplotypes exhibited the full range of mating frequency (Figure 4A). Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves. Out of these 40 matings, copulation was observed in only 2, both of which had. This NIL B exhibited low mating frequency, similar to N2 (Figure 3D), suggesting that the right half of the fragment is not sufficient to augment mating. We made additional tests by crossing two isolates of C. elegans: the AB1 strain from Australia and N2 from Bristol, England. Clipboard, Search History, and several other advanced features are temporarily unavailable. Results of a competition experiment between N2 wild type and him-5 mutant. Genomic structure of him-5 and. Caenorhabditis elegans provides a unique experimental system where males exist in a primarily hermaphroditic species. 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. 2003) (see File S2 for additional details). (B) QTL analysis of hermaphrodite mating frequency of RILs in (A). 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. Further, the observation that females of C. remanei, a closely related obligate outcrossing species, are much more attractive to heterospecific C. elegans males than are conspecific C. elegans hermaphrodites (Chasnov et al. (DH) Hermaphrodite mating frequency of N2-derived mutants defective in (D) neurotransmission (unc-13) or neurosecretion (unc-31), (E) mechanosensation to gentle touch (mec-3 and mec-4), (F) ciliated sensory neuron function (osm-6), (G) TRPV channel (osm-9) or cGMP-gated (tax-2 and tax-4) channelmediated sensory transduction in chemosensory neurons, and (H) cGMP-gated channel (tax-2) sensory transduction in only four sensory neurons. McGrath P T, Xu Y, Ailion M, Garrison J L, Butcher R A et al. 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. 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? National Library of Medicine The life-history transition from obligate to facultative outcrossing allows C. elegans hermaphrodites two reproductive options, but it is not clear to what extent they make a strategic choice between them, how that choice is regulated, or whether there is genetic variation in reproductive decision segregating in natural populations. It is observed that the him-5 mutation was essentially eliminated from the populations in ~70 days (~23 generations). Search for other works by this author on: Corresponding author: Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, 52 Oxford St, Cambridge, Massachusetts 02138. (A) The dorsal nerve cord (DNC) and ventral nerve cord (VNC) run along the entire length of the animal from the nerve ring. Stegeman GW, Baird SE, Ryu WS, Cutter AD. See this image and copyright information in PMC. Here, as a step in this direction, we consider the evolutionary status of C. elegans. Natural selection acts more strongly on earlier than later produced progeny. Rather, we propose that at least a subset of ciliated sensory neurons is required for N2 to resist mating with males. 2005; Sivasundar and Hey 2005), suggesting that hermaphrodite reproduction could be a naturally variable, regulated decision. We found that the difference between N2 and HW hermaphrodite mating frequency remained at three arena sizes tested (Figure 1C). 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. In fact, C. elegans males are significantly more attracted to C. remanei females than they are to hermaphrodites of their own species. government site. 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. While several sensory cues have been implicated in males' ability to recognize hermaphrodites, achieving an 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. The increase in mating frequency of NIL A relative to N2 is similar to the mean effect size estimated from the RIL population (Figure 3C), but it cannot fully explain the difference between N2 and HW or RIL A. In the context of generating NIL A, which contains the entire 5-MB HW fragment covering mate-1 from RIL A, we also obtained a recombinant that lost the left half of the HW fragment in the region, leaving a 3-MB introgression. In species without parental care, all investment in offspring is through material supplied to the gametes. (A) The dorsal nerve cord (DNC) and ventral nerve cord (VNC) run along Of note, Morsci et al. 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. 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. 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. Fecundity score: Different genotypes of C. elegans were transferred individually onto an empty plate (one per plate). Mainstream theories divide possible forces into two broad categories: Either sexual outcrossing produces recombinant types that are better able to adapt to a changing environment, or sex more efficiently eliminates deleterious mutations (Crow 1994; Hurst and Peck 1996). To determine the role of males in C. elegans, we develop a mathematical model for the genetic system of hermaphrodites that can either self-fertilize or be fertilized by males and we perform laboratory observations and experiments on both C. elegans and a related dioecious species C. remanei. This implies that the left half of the fragment could be sufficient alone, or that both are required. 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. The site is secure. 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. A lack of mating vigor comparable to C. elegans would likely drive a dioecious species extinct. 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. 1996). 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. Elegans ; behavior ; cilia ; male ; nervous system ; polycystin sexual! 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