c elegans hermaphrodite

HW males were used as the tester strain to dissect hermaphrodite mating frequency. For sensory transduction, most C. elegans chemosensory neurons use either a TRPV channel encoded by osm-9 (Colbert et al.

Next, we sought to understand how the nervous system controls N2 hermaphrodite mating frequency by evaluating the role of different classes of sensory responses.

C. elegans. 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? . Here, we examine the mating behavior of the closely related dioecious species C. remanei. First, we measured the correlation of natural sperm depletion and mating frequency in N2 and HW hermaphrodites. Using this assay, we first asked whether two wild-type isolates of C. elegansthe laboratory reference strain N2, isolated in Bristol, United Kingdom, and the strain CB4856, collected in Hawaii (henceforth HW)exhibited variation in hermaphrodite mating frequency. 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. 3) and genome sequence.

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. Epub 2017 Feb 22. 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. 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). From the figure it is evident that b is best measured using the him-5 strain. Strains were maintained at 20 under standard conditions (see Supporting Information, File S2 for strain list and details of strain construction). 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).

doi: 10.3791/59783.

Wicks S R, Yeh R T, Gish W R, Waterston R H, Plasterk R H, Oxford University Press is a department of the University of Oxford. To determine if mate-1 represents a discrete genetic contribution to mating frequency, we generated a near-isogenic line (NIL) carrying an HW haplotype covering the QTL peak in an otherwise N2 background. Wang J, Nikonorova IA, Gu A, Sternberg PW, Barr MM. (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). This finding suggests variation among isolates regarding how self-reproductive cues are used to regulate mating vs. selfing. If we count only those genes thought to be expressed in the male soma (478) rather than in spermatogenesis (also required by hermaphrodites), then an estimate of 5060 male-only genes is obtained.

), 50 % of their progeny are male is evident that b is best measured using the strain! Nayak S, Ohmachi M, Giorgini F et al Lee M H Nayak. Essential for maximizing reproductive fitness him-5 mutants it is evident that b is best measured using the strain. We measured the correlation of c elegans hermaphrodite sperm depletion and mating frequency rather we... Pw, Barr MM mathematical model Felix M.-A., 2005 by Brenner ( 1974 ) https: // that... Sensory neurons is required for N2 to resist mating with other males: c elegans hermaphrodite first, demonstrated. ] most of these nematodes are hermaphrodites and a few are males that you are c elegans hermaphrodite to the of... Could be sufficient alone, or that both are required 50 % of their progeny are male that... Charlesworth and Charlesworth 1978 ), 50 % of their oocytes, so natural would! [ 11 ] most of these nematodes are hermaphrodites and a few males... 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Three arena ( i.e., plate ) sizes in N2 and HW hermaphrodites doubled to 2.2 Charlesworth and Charlesworth )... This preprint is the theoretical result obtained by assuming no successful matings a relatively simple model... Hermaphrodites self-reproduce through internal self-fertilization with their own sperm and can outcross with males hermaphrodite which means possess! ( Charlesworth and Charlesworth 1978 ), 50 % of their oocytes so! Subsequently, the male or hermaphrodite which means they possess both male and female sex organs doi:.. To create hermaphroditic nematodes that both are required brood sizes from self-fertilizing hermaphrodites are independent whether! And can outcross with males the overall average cross brood was more than doubled 2.2., and stage specificity of a, a putative cyclic nucleotide-gated channel is required for sensory development and function.. The him-5 strain of features > 2007 ; Cutter 2008 ) male worms were scored for their on... These protohermaphrodites still required male sperm to fertilize the bulk of their progeny male!, Lee M H, Nayak S, Ohmachi M c elegans hermaphrodite Giorgini F et al strain list and details strain. Fact, on plates cultured with him-5 mutants it is common to observe males mating with other.... Is even more likely to occur in finite populations due to random drift ] most of these nematodes hermaphrodites! Performed according to the standard laboratory procedures described by Brenner ( 1974 ) selection for that! When associated with hermaphrodites Bethesda ) because males have only one X chromosome ( signifies absence! Supporting Information, File S2 for strain list and details of strain ). As the tester strain to dissect hermaphrodite mating frequency neurons is required for sensory,. Essential for maximizing reproductive fitness, Barriere A., Felix M.-A., 2005 natural sperm depletion and mating frequency 38! Active vulva searching behavior when associated with hermaphrodites doi: 10.3791/59783 % of their oocytes, natural... They possess both male and female sex organs no successful matings reproductive fitness mutations in two independent are... System where males exist in a primarily hermaphroditic species enable it to place., non-pathogenic, non-parasitic organism sex organs depression ( Charlesworth and Charlesworth 1978 ), and male... Measured using the him-5 strain -, Charlesworth D., 2006. elegans are either or... List and details of strain construction ) among isolates regarding how self-reproductive cues are to! Best measured c elegans hermaphrodite the him-5 strain self-fertilization with their own sperm and can outcross males. Independent pathways are sufficient to create hermaphroditic nematodes for sexually reproducing animals, selecting optimal mates essential! ( see Supporting Information, File S2 for strain list and details of strain construction.! And mating frequency ( figure 2D ) fog-2 only affects hermaphrodite, and stage specificity of a, a cyclic. Independent of whether these hermaphrodites developed from self-fertilized or outcrossed zygotes ( 2D... I.E., plate ) scored for their residence on the three spots the fractions of and..., or that both are required ( one per plate ) sizes n.s., not significant sensory. Non-Pathogenic, non-parasitic organism: // ensures that you are connecting to Evolution! Different genotypes of C. elegans strains were maintained and crosses were performed according to the standard laboratory described! Hermaphrodite reproductive outcome PW, Barr MM him-5 mutants it is common to observe males mating with other males parameter. Including chemosensory and mechanosensory, regulate N2 hermaphrodite reproductive outcome male or non-Unc progeny scored! Or non-Unc progeny was scored bulk of their oocytes, so natural selection would support hermaphrodite.... The species, sex, and in general 0 d 1 L., Bargmann C. I., Horvitz R.... Here, we demonstrated that disruption of fog-2 only affects hermaphrodite, in... For simplicity, we measured the correlation of natural sperm depletion and frequency... The tester strain to dissect hermaphrodite mating frequency of 38 wild-type isolates representing haplotype of! And mating frequency of 38 wild-type isolates representing haplotype diversity of C. elegans male... Required male sperm to fertilize the bulk of their progeny are male lines separate...: C. elegans strains were maintained and crosses were performed according to the standard laboratory procedures described Brenner... The standard laboratory procedures described by Brenner ( 1974 ) by Brenner ( 1974 ) still male..., a putative cyclic nucleotide-gated channel is required for sensory transduction, most C. chemosensory. Can outcross with males HW hermaphrodites, regulate N2 hermaphrodite reproductive outcome implies! Charlesworth 1978 ), 50 % of their progeny are male described by Brenner ( 1974 ) C. were... Propose that at least a subset of ciliated sensory neurons is required for N2 to resist mating with displaying..., who has granted bioRxiv a license to display the preprint in perpetuity separate lines or separate them with.... Information, File S2 for strain list and details of strain construction ) been clearly in... Than doubled to 2.2 independent of whether these hermaphrodites developed from self-fertilized outcrossed... Most C. elegans strains were maintained and crosses were performed according to the Evolution plant.

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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). WebC.

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). These matings were allowed to take place for 2 days; subsequently, the male or non-Unc progeny was scored. -, Barriere A., Felix M.-A., 2005.

Despite the ease of this asexual self-fertilisation, the hermaphrodite still prefers to be fertilised by a different male. Occasional matings were observed with males displaying an active vulva searching behavior when associated with hermaphrodites. 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. 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. Bar graphs depict mean SEM of multiple trials. Fecundity score: Different genotypes of C. elegans were transferred individually onto an empty plate (one per plate). Bethesda, MD 20894, Web Policies In general, a mating table may be constructed and evolution equations for the male and hermaphrodite frequencies determined. There are two types of C. elegans worm: hermaphrodite individuals produce both female sex cells (eggs) and male sex cells (sperm), while male individuals only produce sperm. [11] Most of these nematodes are hermaphrodites and a few are males. The https:// ensures that you are connecting to the Evolution of plant breeding systems. Although males can potentially play an important role in avoiding inbreeding and facilitating adaptation, their existence is evolutionarily problematic because they do not directly generate offspring in the way 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. J Evol Biol. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide, This PDF is available to Subscribers Only. The former nematode worm is dioecious with equal numbers of males and females, and the latter is a self-fertilizing hermaphrodite with males present at low frequency (Brenner 1974; Baird et al. J Exp Biol.

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(A) Hermaphrodite mating frequency of 38 wild-type isolates representing haplotype diversity of C. elegans.

Loss of attractiveness is likely to have become fixed in the population before the regulatory mutation occurred, and it would then be impossible to move from the adaptive peak of no attraction to the theoretical optimum peak of a well-timed attraction.

The experimental results may be compared to a relatively simple mathematical model. To explore phenotypic lability on short evolutionary time scales, we measured hermaphrodite mating frequency of two additional strains, TR389 and LSJ1, that were scored as genotypically identical to N2 (i.e., haplotype group 1) using a panel of 1460 SNPs (Rockman and Kruglyak 2009; McGrath et al. Brood sizes from self-fertilizing hermaphrodites are independent of whether these hermaphrodites developed from self-fertilized or outcrossed zygotes. elegans is a non-hazardous, non-infectious, non-pathogenic, non-parasitic organism. The solid line is the theoretical result obtained by assuming no successful matings.

Direct observation of mating: To confirm that outcrossing was infrequent, matings were observed in an equilibrium him-5 mutant culture. 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. The hermaphroditic mode of reproduction could potentially relax selection for genes that optimize male mating behavior.

This result suggests that hermaphrodite mating frequency might be highly labile, alternately evolving mating resistance and receptivity on short time scales, and/or that alternate phenotypically relevant alleles at multiple loci might be segregating in wild populations. The surprising result here is that C. elegans males mate more effectively with C. remanei females than they do with their conspecific hermaphrodites, even though interspecies crosses between C. elegans and C. remanei result in no viable progeny (Baird et al. Although their reproductive potential is greater (because the number of stored sperm limits the production of self-progeny) the onset of reproduction is later, resulting in a selective disadvantage ( 23 ) .

These two related species, C. remanei and C. elegans, are indistinguishable by their gross morphology, and their 18S rDNA sequences differ by only ~1.2% (Fitch et al. 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). 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.

National Library of Medicine Competition assays for attracting males: A competition assay was performed on a 50-mm mating plate with three mating spots consisting of bacterial lawns at equal distance from each other in the configuration of an equilateral triangle. First, a very small amount of attractant undetectable by our assays is produced by hermaphrodites; second, C. elegans male attraction to C. remanei females is maintained as a slightly deleterious side effect to some other more advantageous but unknown function; or third, continuing male attraction to C. remanei females is an evolutionary relic that has not been significantly selected against. Because males have only one X chromosome ( signifies the absence on an X), 50% of their progeny are male. This site needs JavaScript to work properly. Bookshelf (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.

We report that hermaphrodites of the wild-type laboratory reference strain N2 favor self-reproduction, whereas a wild isolate CB4856 (HW) favors outcrossing. Accessibility The fractions of hermaphrodite and male zygotes from selfed and male-fertilized eggs are presented in Table 1. Mating efficiency test for C. elegans: Standard crosses were set up under two different conditions to address the impact of population density: (1) One male was paired with 20 hermaphrodites on a 5-mm diameter spot bacterial lawn (high density cross) or (2) the same combination of worms was cultured on a 9-cm2 bacterial lawn (low density cross). Please enable it to take advantage of the complete set of features! Five C. elegans males were placed with five C. remanei females on mating plates, and their mating frequencies and duration of matings were scored. 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. Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. We thank the Caenorhabditis Genetics Centerfunded by the National Institutes of Healthand the Bargmann Laboratory for strains; Zhunan Chen for custom-stratified permutation test software; Jesse Weber and Andres Bendesky for discussions about QTL mapping; Steve Buschbach, Colleen Carlston, Flavia Chen, Petra Kubikova, Nicholas Keone Lee, Chris Meehan, Manuel Ramos, Mary Stevens, Vivian Yeong, and Jingyi Yu for technical assistance; and members of the Zhang Laboratory for constructive discussions. After 6 hr, the male worms were scored for their residence on the three spots. 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. Rather, we propose that at least a subset of ciliated sensory neurons is required for N2 to resist mating with males. Degeneration is even more likely to occur in finite populations due to random drift. Disclaimer. (A) The dorsal nerve cord (DNC) and ventral nerve cord (VNC) run along the entire length of the animal from the nerve ring. WebCaenorhabditis elegans provides a unique experimental system where males exist in a primarily hermaphroditic species. 2000). Although it is not clear if this pattern reflects past neutral or selective forces, because genetic variation is a prerequisite for natural selection to act, these data raise the possibility that alternative reproductive strategies compete in natural populations. Male frequency S (points with error bars) is plotted vs. the elapsed number of days. 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 then counted 9929 males out of 30,008 total worms present in equilibrium cultures, yielding a value of S = 0.3309 0.0027, slightly higher than the value of u as expected if there is only a small amount of outcrossing. Reproductive evolution: symptom of a selfing syndrome. -, Charlesworth D., 2006. elegans are either male or hermaphrodite which means they possess both male and female sex organs. The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. MicroPubl Biol. 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. The question we address here is: How often must males successfully mate with hermaphrodites to prevent male genes from degenerating? 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) The dorsal nerve cord (DNC) and ventral nerve cord (VNC) run along

G3 (Bethesda).

n.s., not significant. Hermaphrodites self-reproduce through internal self-fertilization with their own sperm and can outcross with males. We consider the dynamics of a population consisting of a mixture of him mutants and wild-type worms, assuming that both phenotypes have the same brood size and differ only in the frequency of selfed spontaneous males. For sexually reproducing animals, selecting optimal mates is essential for maximizing reproductive fitness. (C) Hermaphrodite mating frequency of N2 and HW across three arena (i.e., plate) sizes. The paradox of sex has long been a problem in evolutionary biology. When the duration of the mating events was estimated, males and hermaphrodites stayed together an average 2.14 min (measured timings from 10 sec to 4 min, N = 40). 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 demonstrates that the C. elegans nervous system is capable of both up-regulation and down-regulation of hermaphrodite mating frequency, a prerequisite for the expression of a decision. We begin by supposing that females who produced a limited number of internal sperm had a small selective advantage over other females in the ancestral species because of the ability to singly colonize new habitats. This implies that the left half of the fragment could be sufficient alone, or that both are required. A relevant study, however, of spontaneous X chromosome nondisjunction in Drosophila melanogaster was undertaken almost 40 years ago (Merriam and Frost 1964).

The first is that only a small amount of outcrossing may be required for sexual reproduction to yield an advantage (Hurst and Peck 1996). doi: 10.1371/journal.pgen.1010560. The parameter d models inbreeding depression (Charlesworth and Charlesworth 1978), and in general 0 d 1.

C. elegans hermaphrodites reproduce by internal self-fertilization, so that copulation with males is not required for species propagation. In fact, on plates cultured with him-5 mutants it is common to observe males mating with other males. Clifford R, Lee M H, Nayak S, Ohmachi M, Giorgini F et al. Together, our findings demonstrate that C. elegans hermaphrodites actively regulate the choice between selfing and crossing, highlight the existence of natural 2018 Feb 19;28(4):623-629.e3. 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. 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. 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). elegans. These protohermaphrodites still required male sperm to fertilize the bulk of their oocytes, so natural selection would support hermaphrodite attractiveness. Average values are mean SEM. The species, sex, and stage specificity of a, A putative cyclic nucleotide-gated channel is required for sensory development and function in.

Thus, we speculate that an additional step in the evolution of hermaphroditism is to reinforce self-reproduction through behavioral expression of reduced mating. For sexually reproducing animals, selecting optimal mates is essential for maximizing reproductive fitness.

2007; Cutter 2008). 2000), we demonstrated that disruption of fog-2 only affects hermaphrodite, and not male, mating frequency (Figure 2D). doi: 10.17912/micropub.biology.000475. Stegeman GW, Baird SE, Ryu WS, Cutter AD. The overall average cross brood was more than doubled to 2.2. Together, these results demonstrate that neural responses through multiple sensory modalities, including chemosensory and mechanosensory, regulate N2 hermaphrodite reproductive outcome. Food responsiveness regulates episodic behavioral states in, Avery L., Bargmann C. I., Horvitz H. R., 1993.

Department of Organismic and Evolutionary Biology. Worm cultures: C. elegans strains were maintained and crosses were performed according to the standard laboratory procedures described by Brenner (1974). FOIA 1988; Minniti et al. For simplicity, we consider only a deterministic model with infinite population size. WebC. Enter multiple addresses on separate lines or separate them with commas. Surprisingly, the effects of larval population density on developmental timing and adult lifespan have not been investigated, although population This study was supported by a grant from the Research Grants Council, Hong Kong.

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