Reproductive strategies reflect higher-order phenotypes that emerge through integration of developmental, morphological, physiological, and behavioural phenotypes. Understanding how these different phenotypes integrate and co-evolve to explain the diversification in reproductive strategies is a central goal of life history research (Flatt and Heyland, 2011). One such fundamental aspect of reproduction in internally fertilizing animals is the duration of intra-uterine embryonic development, which can be highly variable and is influenced by an interplay of genetic and environmental factors. While oviparity and viviparity reflect opposite extremes, many taxa display intermediate modes by laying eggs containing embryos at variably advanced stages of development (sometimes termed ovoviviparity). The degree of such maternal retention of fertilized eggs may vary significantly between closely related species or even between genotypes of the same species, for example in insects, snails, or reptiles, and is further influenced by diverse environmental factors, such as mating status or food availability (Meier et al., 1999; Markow et al., 2009; Bleu et al., 2012; Kalinka, 2015). Viviparity – and prolonged egg retention in general – are thought to promote maternal control over the offspring environment, providing an extended opportunity for offspring resource provisioning as well as improved offspring protection against environmental fluctuations, stressors, pathogens or predators (Blackburn, 1999; Avise, 2013; Kalinka, 2015; Ostrovsky et al., 2016). In addition, laying of advanced-stage embryos or larvae may generate an advantage during intra- and interspecific competition by reducing external egg-to-adult developmental time, for example, in insects (Bakker, 1961; Kalinka, 2015; Mueller and Bitner, 2015). Despite these apparent benefits, prolonged egg retention and viviparity are generally presumed to incur fitness costs, expressed as reduced maternal survival and fecundity, for example, due to higher metabolic costs as a result of prolonged gestation (Kalinka, 2015). How variation in ecological niche drives the evolution of different egg-laying modes given these apparent trade-offs has been a major focus of evolutionary ecological research (Blackburn, 1999; Avise, 2013; Kalinka, 2015; Ostrovsky et al., 2016).

The study of evolutionary transitions between ovi- and viviparity has concentrated on comparisons between species, so that evidence is mainly correlative and the genetic changes underlying such transitions can only rarely be determined (Horváth and Kalinka, 2018; Recknagel et al., 2021). Relatively few studies have examined quantitative intraspecific variation in egg retention although this approach may facilitate disentangling its relative costs and benefits. Intraspecific analysis may further allow for identification of genomic loci contributing to this variation and potentially provide insights into the molecular changes during incipient stages of evolutionary transitions towards obligate viviparity. One such study was performed for natural quantitative variation in egg retention of fertilized Drosophila females (Horváth and Kalinka, 2018): Genome-wide association (GWA) mapping yielded 15 potential candidate genes harbouring natural polymorphisms contributing to variation in egg retention. These variants have not yet been validated and it remains unclear which particular traits, such as fecundity or egg-laying behaviour, contribute to observed variation in egg retention (Horváth and Kalinka, 2018). In this study, prolonged Drosophila egg retention was correlated with a reduction in fecundity, in line with the prediction that evolutionary transitions towards viviparity impose fitness costs (Clutton-Brock, 1991; Blackburn, 1999; Avise, 2013; Kalinka, 2015; Ostrovsky et al., 2016). Analysis of intraspecific variation may thus be valuable to determine genetic causes and fitness consequences of divergent egg retention, providing an entry point into understanding evolutionary transitions between ovi- and viviparity.

In our study, to characterize intraspecific differences in egg retention, we focused on natural variation in egg laying of the male-hermaphrodite (androdioecious) Caenorhabditis elegans. In optimal conditions, this primarily self-fertilizing nematode completes its life cycle within 3–4 days, and hermaphrodites generate around 150–300 offspring over a period of 2–3 days. During the reproductive phase, animals of the reference strain (N2) accumulate up to~15 fertilized eggs in the uterus, caused by a delay between ovulation and egg laying (Schafer, 2006). Embryonic development takes around 15 hours and occurs independently of whether eggs are laid or retained in the uterus. On average, embryos spend two to three hours in utero, reaching the early gastrula (~30-cell) stage when they are being laid (Sulston et al., 1983). At any given time, the number of eggs retained in utero will therefore depend on rates of both egg production and egg laying. Reduced egg-laying rates lead to the accumulation of advanced stage embryos in utero. Egg laying is a rhythmic behaviour that alternates between inactive (~20min) and active (~2min) phases (Waggoner et al., 1998), regulated by a structurally simple neural circuit (White et al., 1986). During active egg-laying phases, the neurotransmitter serotonin and neuropeptides signal via the hermaphrodite-specific neurons (HSN) to increase excitability of vulva muscle cells, causing the rapid sequential release of four to six eggs (Waggoner et al., 1998; Shyn et al., 2003; Zhang et al., 2008; Collins et al., 2016; Brewer et al., 2019). Additional neuromodulatory signals and mechanosensory feedback regulate temporal patterns of egg-laying activity, which are further modulated by physiological and environmental inputs (Trent et al., 1983; Schafer, 2005; Ringstad and Horvitz, 2008; Koelle, 2018; Fernandez et al., 2020; Ravi et al., 2021; Aprison et al., 2022; Medrano and Collins, 2023). Food signals are required for sustained egg-laying activity (Horvitz et al., 1982; Trent, 1982; Waggoner et al., 1998; Daniels et al., 2000; Dong et al., 2000), whereas diverse stressors, such as starvation, hypoxia, thermal stress, osmotic stress, or pathogens, inhibit egg laying (Trent, 1982; Aballay et al., 2000; Waggoner et al., 2000; Chen and Caswell-Chen, 2003; Schafer, 2005; Zhang et al., 2008; McMullen et al., 2012; Fenk and de Bono, 2015). Prolonged stress exposure will lead to intra-uterine egg retention and internal (matricidal) hatching, so that larvae develop inside their mother, often leading to premature maternal death (Maupas, 1900; Trent, 1982; Chen and Caswell-Chen, 2003; Chen and Caswell-Chen, 2004). Environmentally induced egg retention and internal hatching in C. elegans can be considered a plastic switch from oviparity to viviparity, also termed facultative viviparity (Chen and Caswell-Chen, 2004). In C. elegans, while eggs can no longer be provisioned after fertilization, larvae in utero may feed on decaying maternal tissues allowing them to develop into advanced larval stages, even in nutrient-scarce environments (Chen and Caswell-Chen, 2004). Stress-induced internal hatching in C. elegans may thus reflect adaptive phenotypic plasticity allowing for offspring provisioning, in particular, by enabling larvae to develop into the diapausing, starvation-resistant dauer larval stage (Chen and Caswell-Chen, 2004), which also represents the key dispersal developmental stage, able to colonize novel favourable environments (Félix and Braendle, 2010).

The detailed genetic understanding of C. elegans egg-laying behaviour has been obtained through the study of a single wild-type genotype, the laboratory strain N2, and its mutant derivatives (Schafer, 2006). It therefore remains unclear to what extent the egg-laying circuit harbours intraspecific variation. Although wild strains are highly isogenic due to a predominant self-fertilization (selfing) (Barrière and Félix, 2005; Lee et al., 2021), C. elegans retains considerable genetic (and phenotypic) diversity across the globe, with strains differing genetically, often in localized, highly divergent genomic regions (Andersen et al., 2012; Crombie et al., 2019; Lee et al., 2021; Gilbert et al., 2022). While egg-laying responses to diverse stimuli seem to be largely invariant across many C. elegans populations (Chen and Caswell-Chen, 2004; Chen et al., 2020; Vigne et al., 2021), wild strains may exhibit strongly divergent egg-laying behaviour (Vigne et al., 2021). These rare strains display constitutively strong egg retention (up to ~50 eggs in utero) and internal hatching irrespective of the environment (partial viviparity). A single, major-effect variant explains this derived phenotype: a single amino acid substitution (V530L) in KCNL-1, a small-conductance calcium-activated potassium channel subunit. This gain-of-function mutation causes vulval muscle hyperpolarization to reduce egg-laying activity, leading to constitutively strong egg retention and internal hatching (Vigne et al., 2021). The apparent evolutionary maintenance of the KCNL-1 V530L variant in natural C. elegans populations seems puzzling given its highly deleterious fitness effects caused by matricidal hatching. Competition experiments indicate, however, that this variant allele can be maintained in more natural conditions mimicking fluctuations in resource availability and/or if reproduction preferentially occurs during early adulthood (Vigne et al., 2021). Nevertheless, it remains unknown how constitutively strong egg retention may be beneficial in such conditions, and more generally, how different degrees of C. elegans egg retention affect alternative fitness components.

Here, extending our previous work (Vigne et al., 2021), we quantified the full spectrum of natural variation in C. elegans egg retention using a world-wide panel of strains covering much of the species’ genetic diversity (Lee et al., 2021). Our first aim was to characterize variation in egg laying, and to identify phylogenetic patterns and genomic regions (QTL) associated with observed phenotypic variation. We show that, while most strains differed only subtly in egg retention, a subset of strains exhibit deviant, strongly increased or reduced, egg retention. We provide evidence for repeated evolution of such extreme egg retention phenotypes through distinct genetic changes. We then characterized a subset of wild strains with divergent egg retention to determine how they differ in egg-laying behaviour and underlying neuromodulatory architecture. These results show that the C. elegans egg-laying system harbours surprisingly high natural diversity in the sensitivity to neuromodulators, such as serotonin, suggesting rapid evolution of the involved neural circuitry. In a second objective, we explored why variation in egg retention might be maintained in natural C. elegans populations. To address this question, we tested for the presence of fitness costs and benefits associated with variable egg retention of wild C. elegans strains. We experimentally demonstrate that strong egg retention usually reduces maternal fertility and survival, mostly due to frequent internal (matricidal) hatching. On the other hand, these genotypes with strong egg retention may be able to benefit from improved offspring protection against environmental insults and from a competitive advantage caused by a significantly reduced extra-uterine egg-to-adult developmental time. Observed natural variation in C. elegans egg-laying behaviour may therefore modify a trade-off between fitness components expressed in mothers versus offspring. Altogether, we present an integrative analysis of natural variation in C. elegans egg laying providing first insights into the genetic basis, fitness consequences and possible evolutionary ecological significance of this central reproductive behaviour.

Our study has quantified and characterized natural variation in C. elegans egg retention and egg-laying behaviour, resulting in the following main findings: (1) C. elegans exhibits quantitative variation in egg retention, with rare instances of extreme phenotypes at either end of the spectrum. (2) Both common and rare genetic variants underlie observed phenotypic variation. (3) Strain differences in egg retention can be largely explained by differences in egg-laying behaviour, such as the onset of egg laying activity and timing of the rhythm between active and inactive egg-laying phases. (4) These behavioural differences map, at least partly, to genetic differences in the sensitivity to various neuromodulators, indicative of natural variation in the C. elegans egg-laying circuitry. (5) Modified egg-laying behaviour causing strong egg retention – linked to frequent larval hatching in utero – negatively impacts maternal fitness, but (6) prolonged intra-uterine embryonic development may benefit offspring by improving their competitive ability and protection against environmental insults. (7) Hence, variation in C. elegans egg retention may reflect variation in a trade-off between antagonistic effects acting on maternal versus offspring fitness.

C. elegans egg retention is a quantitative (complex) trait: observed phenotypic distribution and GWA mapping indicate that this trait is likely influenced by multiple loci of small effect (Mackay et al., 2009). In addition, large-effect variants, such as KCNL-1 V530L (Vigne et al., 2021), occur but they seem to be relatively rare. Although variation in reproductive processes, such as self-sperm production and ovulation rates, contributes to observed variation in egg number in utero, we also present clear evidence for natural variation in egg-laying behaviour and involved neuromodulatory processes. How such behavioural differences arise through modification of specific cellular and physiological processes and how these, in turn, are mediated by specific molecular alterations of genes in the C. elegans egg-laying system remains to be elucidated. The genetics of the C. elegans egg-laying circuit has been studied for decades, and dozens of genes have been identified by mutations, which either reduce or increase egg-laying activity (Trent et al., 1983; Schafer, 2006). Some of the identified genes encode ion channels regulating cell and synaptic electrical excitability, others encode components of G-protein signalling pathways that act in specific cells of the circuit. Many more genes transmitting environmental and physiological signals via sensory processing are known to regulate C. elegans egg laying (Schafer, 2006; Ringstad and Horvitz, 2008; Fenk and de Bono, 2015; Banerjee et al., 2017). Recent research has further uncovered an important role of muscle-directed mechanisms regulating egg laying through sensation of internal stretch mediated by egg accumulation in utero (Collins et al., 2016; Ravi et al., 2018; Ravi et al., 2021; Medrano and Collins, 2023). This stretch-dependent homeostat directly targets vulval muscles and is sufficient to trigger egg laying when synaptic transmission is reduced or defective, for example, in the absence of HSN command neurons (Ravi et al., 2018; Ravi et al., 2021; Medrano and Collins, 2023). As indicated by our results (Figure 6B), changes in such muscle-directed signalling components in response to egg accumulation are likely key factors driving the evolution of C. elegans egg retention. Future experiments should therefore be aimed at understanding how such modifications in mechanosensory feedback interact with other potential changes in synaptic transmission to explain the natural diversity in the C. elegans egg-laying neural circuit. In addition, we cannot exclude that natural variation in egg-laying behaviour may arise through differential activity of developmental genes generating variation in the neuroanatomy of the egg-laying circuit itself, for example as observed between different Caenorhabditis species (Loer and Rivard, 2007).

Currently, the only known natural variant modulating C. elegans egg laying is the major-effect variant KCNL-1 V530L, which reduces egg laying through likely hyperpolarization of vulval muscles (Vigne et al., 2021), so that stimuli, such as mechanosensory inputs, are insufficient to trigger regular and successful egg-laying events. Our new results show that other unknown variants must cause the strong reduction of egg-laying activity in Class IIIA strains. Although our experimental results do not hint at any variants in specific candidate genes or processes, we detected strong differences in the serotonin response between Class IIIA strains (Figure 7B). Exogenous serotonin stimulated egg laying in all Class IIIA strains except in JU2829, where it inhibited egg laying as observed for Class IIIB strains (Figure 7B). This suggests that JU2829 might carry a variant with effects like KCNL-1 V530L, whereas variants with distinct functional effects would explain reduced egg-laying activity in other Class IIIA strains. The detection of both strong and subtle strain variation in egg-laying activity (also among strains within the same Class), as revealed by our pharmacological assays and when analysing the effects of mod-5(lf) in different strains (Figure 8), indicates the presence of many different natural variants that modulate egg-laying circuitry in C. elegans. Molecular identification of specific variants will thus be essential to explore how the nematode egg-laying circuit evolves at the intraspecific level.

Consistent with previous reports on the apparent costs of transitioning from oviparity to obligate and facultative viviparity (Avise, 2013; Kalinka, 2015; Horváth and Kalinka, 2018), we found that increased C. elegans egg retention lowers maternal survival and fecundity. We then show that fitness costs associated with strong egg retention are potentially offset by improved offspring competitive ability and protection against environmental perturbations. To what extent our highly simplified experimental conditions recapitulate relevant ecological scenarios encountered by natural C. elegans populations remains to be explored. The likely ecological factors shaping natural variation in C. elegans egg retention are thus unknown and we have not found any obvious links between the degree of egg retention and habitat parameters, such as substrate type or climate. However, the likely ancestral (divergent) strains only very rarely exhibited a Class III phenotype, which could indicate that derived state of strong egg retention may have been favoured by the exploitation of novel microhabitats during the historically recent expansion of C. elegans reflected by globally distributed, swept haplotypes (Lee et al., 2019; Lee et al., 2021).

The typical C. elegans habitat is highly ephemeral in nature, exhibiting extreme fluctuations in nutrient availability and occurrence of diverse abiotic and biotic variables, including stressors and pathogens (Frézal and Félix, 2015; Schulenburg and Félix, 2017). A critical omission in our study is therefore the analysis of plasticity in egg retention and egg-laying behaviour in different or fluctuating environments. C. elegans egg laying is known to be highly plastic, strongly modulated by subtle and very diverse environmental factors, so that our analyses in standard laboratory conditions can only capture fractions of the complexity. Most prominently, diverse environmental stimuli (food quantity and quality, osmotic or hypoxic stress, pathogens, etc.) have inhibitory effects on egg laying and long-term exposure to these stimuli will lead to strong egg retention and matricidal hatching (Trent, 1982; Aballay et al., 2000; Waggoner et al., 2000; Chen and Caswell-Chen, 2003; Schafer, 2005; Zhang et al., 2008; McMullen et al., 2012; Fenk and de Bono, 2015; Vigne et al., 2021). Future research will therefore require to carefully examine how such environmental effects modulate egg laying and fitness consequences in strains with the here reported differences in constitutive egg retention. In particular, plastically induced egg retention and matricidal hatching by prolonged starvation may allow for nutrient provisioning of internally hatched larvae as they can consume debris stemming from the decaying mother, hence allowing for developmental growth in the absence of external food (Chen and Caswell-Chen, 2003; Chen and Caswell-Chen, 2004). Future experiments should therefore specifically test if internally hatched larvae in Class III strains (Figure 3E) may gain a further advantage through maternal provisioning while developing in utero, specifically when exposed to long-term conditions inhibiting egg laying, such as starvation.

The existence of pronounced natural variation in C. elegans egg retention and egg-laying behaviour generates novel opportunities to dissect the molecular genetic basis of intraspecific variation in egg retention, providing an entry point to understand the proximate mechanisms underlying evolutionary transitions between invertebrate ovi- and viviparity. In contrast to vertebrate taxa with intraspecific variation in egg-laying mode, such as certain lizards (Recknagel et al., 2021; Whittington et al., 2022), the C. elegans model allows for rapid and powerful genetic analysis, for example through linkage mapping of natural variants and subsequent functional validation of variants by CRISPR-Cas9 gene editing in multiple strains (Evans et al., 2021). Identifying the precise changes in C. elegans egg-laying circuitry that have led to variation in egg retention may also generate insights into the genetic basis of evolutionary diversification of egg-laying modes across species and genera. Nematodes display frequent transitions from oviparity to obligate viviparity in many distinct genera (Sudhaus, 1976; Ostrovsky et al., 2016), including in the genus Caenorhabditis, with at least one viviparous species, C. vivipara (Stevens et al., 2019). Although evidence exists for the evolution of egg-laying circuitry across oviparous Caenorhabditis species (Loer and Rivard, 2007), the specific cellular and genetic changes responsible for the transition to obligate viviparity in C. vivipara have yet to be examined. Resolving the genetic basis of intraspecific variation in C. elegans egg retention, including partial or facultative viviparity, may thus shed light on the molecular changes underlying the initial steps of evolutionary transitions from oviparity to obligate viviparity in invertebrates.

All data generated or analysed in this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

1. 1. Aballay A
   2. Yorgey P
   3. Ausubel FM

   (2000) Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans

   Current Biology 10:1539–1542.

   https://doi.org/10.1016/S0960-9822(00)00830-7

   • Google Scholar
2. 1. Andersen EC
   2. Gerke JP
   3. Shapiro JA
   4. Crissman JR
   5. Ghosh R
   6. Bloom JS
   7. Félix M-A
   8. Kruglyak L

   (2012) Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity

   Nature Genetics 44:285–290.

   https://doi.org/10.1038/ng.1050

   • Google Scholar
3. 1. Andersen EC
   2. Bloom JS
   3. Gerke JP
   4. Kruglyak L

   (2014) A variant in the neuropeptide receptor npr-1 is A major determinant of Caenorhabditis elegans growth and physiology

   PLOS Genetics 10:e1004156.

   https://doi.org/10.1371/journal.pgen.1004156

   • PubMed
   • Google Scholar
4. 1. Andersen EC
   2. Shimko TC
   3. Crissman JR
   4. Ghosh R

   (2015) A powerful new quantitative genetics platform, combining Caenorhabditis elegans high-throughput fitness assays with a large collection of recombinant strains

   G3: Genes, Genomes, Genetics 5:911–920.

   https://doi.org/10.1534/g3.115.017178

   • Google Scholar
5. 1. Aprison EZ
   2. Dzitoyeva S
   3. Ruvinsky I

   (2022) The serotonin circuit that coordinates germline proliferation and egg laying with other reproductive functions in Caenorhabditis elegans

   Proceedings. Biological Sciences 289:20220913.

   https://doi.org/10.1098/rspb.2022.0913

   • PubMed
   • Google Scholar
6. Book

   1. Avise J

   (2013) Evolutionary Perspectives on Pregnancy

   Columbia University Press.

   https://doi.org/10.7312/columbia/9780231160605.001.0001

   • Google Scholar
7. 1. Bakker K

   (1961) An analysis of factors which determine success in competition for food among larvae of Drosophila melanogaster

   Archives Néerlandaises de Zoologie 14:200–281.

   https://doi.org/10.1163/036551661X00061

   • Google Scholar
8. 1. Banerjee N
   2. Bhattacharya R
   3. Gorczyca M
   4. Collins KM
   5. Francis MM

   (2017) Local neuropeptide signaling modulates serotonergic transmission to shape the temporal organization of C. elegans egg-laying behavior

   PLOS Genetics 13:e1006697.

   https://doi.org/10.1371/journal.pgen.1006697

   • Google Scholar
9. 1. Barker DM

   (1992) Evolution of sperm shortage in a selfing hermaphrodite

   Evolution; International Journal of Organic Evolution 46:1951–1955.

   https://doi.org/10.1111/j.1558-5646.1992.tb01181.x

   • PubMed
   • Google Scholar
10. 1. Barrière A
    2. Félix MA

    (2005) High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations

    Current Biology 15:1176–1184.

    https://doi.org/10.1016/j.cub.2005.06.022

    • PubMed
    • Google Scholar
11. 1. Barrière A
    2. Félix MA

    (2007) Temporal dynamics and linkage disequilibrium in natural Caenorhabditis elegans populations

    Genetics 176:999–1011.

    https://doi.org/10.1534/genetics.106.067223

    • PubMed
    • Google Scholar
12. 1. Ben Soussia I
    2. El Mouridi S
    3. Kang D
    4. Leclercq-Blondel A
    5. Khoubza L
    6. Tardy P
    7. Zariohi N
    8. Gendrel M
    9. Lesage F
    10. Kim EJ
    11. Bichet D
    12. Andrini O
    13. Boulin T

    (2019) Mutation of a single residue promotes gating of vertebrate and invertebrate two-pore domain potassium channels

    Nature Communications 10:787.

    https://doi.org/10.1038/s41467-019-08710-3

    • PubMed
    • Google Scholar
13. 1. Billard B
    2. Vigne P
    3. Braendle C

    (2020) A natural mutational event uncovers a life history trade-off via hormonal pleiotropy

    Current Biology 30:4142–4154.

    https://doi.org/10.1016/j.cub.2020.08.004

    • PubMed
    • Google Scholar
14. Book

    1. Blackburn DG

    (1999)

    Viviparity and Oviparity: Evolution and Reproductive Strategies

    Academic Press.

    • Google Scholar
15. 1. Blackburn DG

    (2015) Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis

    Journal of Morphology 276:961–990.

    https://doi.org/10.1002/jmor.20272

    • PubMed
    • Google Scholar
16. 1. Bleu J
    2. Heulin B
    3. Haussy C
    4. Meylan S
    5. Massot M

    (2012) Experimental evidence of early costs of reproduction in conspecific viviparous and oviparous lizards

    Journal of Evolutionary Biology 25:1264–1274.

    https://doi.org/10.1111/j.1420-9101.2012.02518.x

    • PubMed
    • Google Scholar
17. 1. Branicky R
    2. Miyazaki H
    3. Strange K
    4. Schafer WR

    (2014) The voltage-gated anion channels encoded by clh-3 regulate egg laying in C. elegans by modulating motor neuron excitability

    The Journal of Neuroscience 34:764–775.

    https://doi.org/10.1523/JNEUROSCI.3112-13.2014

    • PubMed
    • Google Scholar
18. 1. Brewer JC
    2. Olson AC
    3. Collins KM
    4. Koelle MR

    (2019) Serotonin and neuropeptides are both released by the HSN command neuron to initiate Caenorhabditis elegans egg laying

    PLOS Genetics 15:e1007896.

    https://doi.org/10.1371/journal.pgen.1007896

    • PubMed
    • Google Scholar
19. 1. Burton NO
    2. Willis A
    3. Fisher K
    4. Braukmann F
    5. Price J
    6. Stevens L
    7. Baugh LR
    8. Reinke A
    9. Miska EA

    (2021) Intergenerational adaptations to stress are evolutionarily conserved, stress-specific, and have deleterious trade-offs

    eLife 10:e73425.

    https://doi.org/10.7554/eLife.73425

    • PubMed
    • Google Scholar
20. 1. Carnell L
    2. Illi J
    3. Hong SW
    4. McIntire SL

    (2005) The G-protein-coupled serotonin receptor SER-1 regulates egg laying and male mating behaviors in Caenorhabditis elegans

    The Journal of Neuroscience 25:10671–10681.

    https://doi.org/10.1523/JNEUROSCI.3399-05.2005

    • PubMed
    • Google Scholar
21. 1. Chen J
    2. Caswell-Chen EP

    (2003) Why Caenorhabditis elegans adults sacrifice their bodies to progeny

    Nematology 5:641–645.

    https://doi.org/10.1163/156854103322683355

    • Google Scholar
22. 1. Chen J
    2. Caswell-Chen EP

    (2004)

    Facultative vivipary is a life-history trait in Caenorhabditis elegans

    Journal of Nematology 36:107–113.

    • PubMed
    • Google Scholar
23. 1. Chen YC
    2. Seyedsayamdost MR
    3. Ringstad N

    (2020) A microbial metabolite synergizes with endogenous serotonin to trigger C. elegans reproductive behavior

    PNAS 117:30589–30598.

    https://doi.org/10.1073/pnas.2017918117

    • Google Scholar
24. Book

    1. Clutton-Brock TH

    (1991) The Evolution of Parental Care

    Princeton University Press.

    https://doi.org/10.1515/9780691206981

    • Google Scholar
25. 1. Collins KM
    2. Bode A
    3. Fernandez RW
    4. Tanis JE
    5. Brewer JC
    6. Creamer MS
    7. Koelle MR

    (2016) Activity of the C. elegans egg-laying behavior circuit is controlled by competing activation and feedback inhibition

    eLife 5:e21126.

    https://doi.org/10.7554/eLife.21126

    • PubMed
    • Google Scholar
26. 1. Cook DE
    2. Zdraljevic S
    3. Roberts JP
    4. Andersen EC

    (2017) CeNDR, the Caenorhabditis elegans natural diversity resource

    Nucleic Acids Research 45:D650–D657.

    https://doi.org/10.1093/nar/gkw893

    • PubMed
    • Google Scholar
27. 1. Crombie TA
    2. Zdraljevic S
    3. Cook DE
    4. Tanny RE
    5. Brady SC
    6. Wang Y
    7. Evans KS
    8. Hahnel S
    9. Lee D
    10. Rodriguez BC
    11. Zhang G
    12. van der Zwagg J
    13. Kiontke K
    14. Andersen EC

    (2019) Deep sampling of Hawaiian Caenorhabditis elegans reveals high genetic diversity and admixture with global populations

    eLife 8:e50465.

    https://doi.org/10.7554/eLife.50465

    • PubMed
    • Google Scholar
28. 1. Crombie TA
    2. McKeown R
    3. Moya ND
    4. Evans KS
    5. Widmayer SJ
    6. LaGrassa V
    7. Roman N
    8. Tursunova O
    9. Zhang G
    10. Gibson SB
    11. Buchanan CM
    12. Roberto NM
    13. Vieira R
    14. Tanny RE
    15. Andersen EC

    (2023) CaeNDR, the caenorhabditis natural diversity resource

    Nucleic Acids Res 45:D650–D657.

    https://doi.org/10.1093/nar/gkad887

    • Google Scholar
29. 1. Cutter AD

    (2004) Sperm-limited fecundity in nematodes: how many sperm are enough?

    Evolution 58:651–655.

    https://doi.org/10.1111/j.0014-3820.2004.tb01687.x

    • Google Scholar
30. 1. Daniels SA
    2. Ailion M
    3. Thomas JH
    4. Sengupta P

    (2000) egl-4 acts through a transforming growth factor-beta/SMAD pathway in Caenorhabditis elegans to regulate multiple neuronal circuits in response to sensory cues

    Genetics 156:123–141.

    https://doi.org/10.1093/genetics/156.1.123

    • PubMed
    • Google Scholar
31. 1. Dempsey CM
    2. Mackenzie SM
    3. Gargus A
    4. Blanco G
    5. Sze JY

    (2005) Serotonin (5HT), fluoxetine, imipramine and dopamine target distinct 5HT receptor signaling to modulate Caenorhabditis elegans egg-laying behavior

    Genetics 169:1425–1436.

    https://doi.org/10.1534/genetics.104.032540

    • PubMed
    • Google Scholar
32. 1. Desai C
    2. Horvitz HR

    (1989) Caenorhabditis elegans mutants defective in the functioning of the motor neurons responsible for egg laying

    Genetics 121:703–721.

    https://doi.org/10.1093/genetics/121.4.703

    • PubMed
    • Google Scholar
33. 1. Dey S
    2. Proulx SR
    3. Teotónio H

    (2016) Adaptation to temporally fluctuating environments by the evolution of maternal effects

    PLOS Biology 14:e1002388.

    https://doi.org/10.1371/journal.pbio.1002388

    • PubMed
    • Google Scholar
34. 1. Dong MQ
    2. Chase D
    3. Patikoglou GA
    4. Koelle MR

    (2000) Multiple RGS proteins alter neural G protein signaling to allow C. elegans to rapidly change behavior when fed

    Genes & Development 14:2003–2014.

    https://doi.org/10.1101/gad.14.16.2003

    • Google Scholar
35. 1. Evans KS
    2. van MH
    3. Mcgrath PT
    4. Andersen EC
    5. Sterken MG

    (2021) From QTL to gene: C. elegans facilitates discoveries of the genetic mechanisms underlying natural variation

    Trends Genet 37:933–947.

    https://doi.org/10.1016/j.tig.2021.06.005

    • Google Scholar
36. 1. Fausett S
    2. Poullet N
    3. Gimond C
    4. Vielle A
    5. Bellone M
    6. Braendle C

    (2021) Germ cell apoptosis is critical to maintain Caenorhabditis elegans offspring viability in stressful environments

    PLOS ONE 16:e0260573.

    https://doi.org/10.1371/journal.pone.0260573

    • PubMed
    • Google Scholar
37. Preprint

    1. Fausett SR
    2. Sandjak A
    3. Billard B
    4. Braendle C

    (2022) Higher-order epistasis shapes natural variation in germ stem cell niche activity

    bioRxiv.

    https://doi.org/10.1101/2022.11.04.515229

    • Google Scholar
38. 1. Félix MA
    2. Braendle C

    (2010) The natural history of Caenorhabditis elegans

    Current Biology 20:R965–R969.

    https://doi.org/10.1016/j.cub.2010.09.050

    • PubMed
    • Google Scholar
39. 1. Fenk LA
    2. de Bono M

    (2015) Environmental CO2 inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

    PNAS 112:E3525–E3534.

    https://doi.org/10.1073/pnas.1423808112

    • PubMed
    • Google Scholar
40. 1. Fernandez RW
    2. Wei K
    3. Wang EY
    4. Mikalauskaite D
    5. Olson A
    6. Pepper J
    7. Christie N
    8. Kim S
    9. Weissenborn S
    10. Sarov M
    11. Koelle MR

    (2020) Cellular expression and functional roles of all 26 neurotransmitter GPCRs in the C. elegans egg-laying circuit

    The Journal of Neuroscience 40:7475–7488.

    https://doi.org/10.1523/JNEUROSCI.1357-20.2020

    • PubMed
    • Google Scholar
41. Book

    1. Flatt T
    2. Heyland A

    (2011)

    Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade-Offs

    Oxford University Press.

    • Google Scholar
42. 1. Frézal L
    2. Félix MA

    (2015) C. elegans outside the Petri dish

    eLife 4:e05849.

    https://doi.org/10.7554/eLife.05849

    • PubMed
    • Google Scholar
43. 1. Garsin DA
    2. Sifri CD
    3. Mylonakis E
    4. Qin X
    5. Singh KV
    6. Murray BE
    7. Calderwood SB
    8. Ausubel FM

    (2001) A simple model host for identifying Gram-positive virulence factors

    PNAS 98:10892–10897.

    https://doi.org/10.1073/pnas.191378698

    • PubMed
    • Google Scholar
44. 1. Gibson G
    2. Dworkin I

    (2004) Uncovering cryptic genetic variation

    Nature Reviews. Genetics 5:681–690.

    https://doi.org/10.1038/nrg1426

    • PubMed
    • Google Scholar
45. 1. Gilbert KJ
    2. Zdraljevic S
    3. Cook DE
    4. Cutter AD
    5. Andersen EC
    6. Baer CF

    (2022) The distribution of mutational effects on fitness in Caenorhabditis elegans inferred from standing genetic variation

    Genetics 220:iyab166.

    https://doi.org/10.1093/genetics/iyab166

    • PubMed
    • Google Scholar
46. 1. Gimond C
    2. Vielle A
    3. Silva-Soares N
    4. Zdraljevic S
    5. McGrath PT
    6. Andersen EC
    7. Braendle C

    (2019) Natural variation and genetic determinants of Caenorhabditis elegans sperm size

    Genetics 213:615–632.

    https://doi.org/10.1534/genetics.119.302462

    • PubMed
    • Google Scholar
47. Book

    1. Hall DH
    2. Altun ZF

    (2007)

    C. elegans Atlas

    Cold Spring Harbor Laboratory Press.

    • Google Scholar
48. 1. Hapiak VM
    2. Hobson RJ
    3. Hughes L
    4. Smith K
    5. Harris G
    6. Condon C
    7. Komuniecki P
    8. Komuniecki RW

    (2009) Dual excitatory and inhibitory serotonergic inputs modulate egg laying in Caenorhabditis elegans

    Genetics 181:153–163.

    https://doi.org/10.1534/genetics.108.096891

    • PubMed
    • Google Scholar
49. 1. Hobson RJ
    2. Hapiak VM
    3. Xiao H
    4. Buehrer KL
    5. Komuniecki PR
    6. Komuniecki RW

    (2006) SER-7, a Caenorhabditis elegans 5-HT7-like receptor, is essential for the 5-HT stimulation of pharyngeal pumping and egg laying

    Genetics 172:159–169.

    https://doi.org/10.1534/genetics.105.044495

    • PubMed
    • Google Scholar
50. 1. Hodgkin J
    2. Barnes TM

    (1991) More is not better: brood size and population growth in a self-fertilizing nematode

    Proceedings. Biological Sciences 246:19–24.

    https://doi.org/10.1098/rspb.1991.0119

    • PubMed
    • Google Scholar
51. 1. Horváth B
    2. Kalinka AT

    (2018) The genetics of egg retention and fertilization success in Drosophila: One step closer to understanding the transition from facultative to obligate viviparity

    Evolution; International Journal of Organic Evolution 72:318–336.

    https://doi.org/10.1111/evo.13411

    • PubMed
    • Google Scholar
52. 1. Horvitz HR
    2. Chalfie M
    3. Trent C
    4. Sulston JE
    5. Evans PD

    (1982) Serotonin and octopamine in the nematode Caenorhabditis elegans

    Science 216:1012–1014.

    https://doi.org/10.1126/science.6805073

    • PubMed
    • Google Scholar
53. 1. Jafari G
    2. Xie Y
    3. Kullyev A
    4. Liang B
    5. Sze JY

    (2011) Regulation of extrasynaptic 5-HT by serotonin reuptake transporter function in 5-HT-absorbing neurons underscores adaptation behavior in Caenorhabditis elegans

    The Journal of Neuroscience 31:8948–8957.

    https://doi.org/10.1523/JNEUROSCI.1692-11.2011

    • PubMed
    • Google Scholar
54. 1. Johnston WL
    2. Dennis JW

    (2012) The eggshell in the C. elegans oocyte-to-embryo transition

    Genesis 50:333–349.

    https://doi.org/10.1002/dvg.20823

    • PubMed
    • Google Scholar
55. 1. Kalinka AT

    (2015) How did viviparity originate and evolve? Of conflict, co-option, and cryptic choice

    BioEssays 37:721–731.

    https://doi.org/10.1002/bies.201400200

    • PubMed
    • Google Scholar
56. 1. Koelle MR

    (2018) Neurotransmitter signaling through heterotrimeric G proteins: insights from studies in C. elegans

    WormBook 2018:1–52.

    https://doi.org/10.1895/wormbook.1.75.2

    • PubMed
    • Google Scholar
57. 1. Kopchock RJ
    2. Ravi B
    3. Bode A
    4. Collins KM

    (2021) The sex-specific vc neurons are mechanically activated motor neurons that facilitate serotonin-induced egg laying in C. elegans

    The Journal of Neuroscience 41:3635–3650.

    https://doi.org/10.1523/JNEUROSCI.2150-20.2021

    • PubMed
    • Google Scholar
58. 1. Kosinski M
    2. McDonald K
    3. Schwartz J
    4. Yamamoto I
    5. Greenstein D

    (2005) C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes

    Development 132:3357–3369.

    https://doi.org/10.1242/dev.01916

    • Google Scholar
59. 1. Kullyev A
    2. Dempsey CM
    3. Miller S
    4. Kuan CJ
    5. Hapiak VM
    6. Komuniecki RW
    7. Griffin CT
    8. Sze JY

    (2010) A genetic survey of fluoxetine action on synaptic transmission in Caenorhabditis elegans

    Genetics 186:929–941.

    https://doi.org/10.1534/genetics.110.118877

    • Google Scholar
60. 1. Large EE
    2. Padmanabhan R
    3. Watkins KL
    4. Campbell RF
    5. Xu W
    6. McGrath PT

    (2017) Modeling of a negative feedback mechanism explains antagonistic pleiotropy in reproduction in domesticated Caenorhabditis elegans strains

    PLOS Genetics 13:e1006769.

    https://doi.org/10.1371/journal.pgen.1006769

    • PubMed
    • Google Scholar
61. 1. Lee D
    2. Zdraljevic S
    3. Cook DE
    4. Frézal L
    5. Hsu JC
    6. Sterken MG
    7. Riksen JAG
    8. Wang J
    9. Kammenga JE
    10. Braendle C
    11. Félix MA
    12. Schroeder FC
    13. Andersen EC

    (2019) Selection and gene flow shape niche-associated variation in pheromone response

    Nature Ecology & Evolution 3:1455–1463.

    https://doi.org/10.1038/s41559-019-0982-3

    • Google Scholar
62. 1. Lee D
    2. Zdraljevic S
    3. Stevens L
    4. Wang Y
    5. Tanny RE
    6. Crombie TA
    7. Cook DE
    8. Webster AK
    9. Chirakar R
    10. Baugh LR
    11. Sterken MG
    12. Braendle C
    13. Félix MA
    14. Rockman MV
    15. Andersen EC

    (2021) Balancing selection maintains hyper-divergent haplotypes in Caenorhabditis elegans

    Nature Ecology & Evolution 5:794–807.

    https://doi.org/10.1038/s41559-021-01435-x

    • Google Scholar
63. 1. Letunic I
    2. Bork P

    (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments

    Nucleic Acids Research 47:W256–W259.

    https://doi.org/10.1093/nar/gkz239

    • Google Scholar
64. 1. Loer CM
    2. Rivard L

    (2007) Evolution of neuronal patterning in free-living rhabditid nematodes I: Sex-specific serotonin-containing neurons

    The Journal of Comparative Neurology 502:736–767.

    https://doi.org/10.1002/cne.21288

    • PubMed
    • Google Scholar
65. 1. Mackay TFC
    2. Stone EA
    3. Ayroles JF

    (2009) The genetics of quantitative traits: challenges and prospects

    Nature Reviews Genetics 10:565–577.

    https://doi.org/10.1038/nrg2612

    • Google Scholar
66. 1. Markow TA
    2. Beall S
    3. Matzkin LM

    (2009) Egg size, embryonic development time and ovoviviparity in Drosophila species

    Journal of Evolutionary Biology 22:430–434.

    https://doi.org/10.1111/j.1420-9101.2008.01649.x

    • PubMed
    • Google Scholar
67. Book

    1. Maupas E

    (1900)

    Modes et Formes de Reproduction Des Nématodes

    Worldcat.

    • Google Scholar
68. 1. McCarter J
    2. Bartlett B
    3. Dang T
    4. Schedl T

    (1997) Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages

    Developmental Biology 181:121–143.

    https://doi.org/10.1006/dbio.1996.8429

    • PubMed
    • Google Scholar
69. 1. McMullen PD
    2. Aprison EZ
    3. Winter PB
    4. Amaral LAN
    5. Morimoto RI
    6. Ruvinsky I

    (2012) Macro-level modeling of the response of C. elegans reproduction to chronic heat stress

    PLOS Computational Biology 8:e1002338.

    https://doi.org/10.1371/journal.pcbi.1002338

    • PubMed
    • Google Scholar
70. 1. Medrano E
    2. Collins KM

    (2023) Muscle-directed mechanosensory feedback activates egg-laying circuit activity and behavior in Caenorhabditis elegans

    Current Biology 33:2330–2339.

    https://doi.org/10.1016/j.cub.2023.05.008

    • PubMed
    • Google Scholar
71. 1. Meier R
    2. Kotrba M
    3. Ferrar P

    (1999) Ovoviviparity and viviparity in the Diptera

    Biological Reviews 74:199–258.

    https://doi.org/10.1111/j.1469-185X.1999.tb00186.x

    • Google Scholar
72. 1. Mok DZL
    2. Sternberg PW
    3. Inoue T

    (2015) Morphologically defined sub-stages of C. elegans vulval development in the fourth larval stage

    BMC Developmental Biology 15:26.

    https://doi.org/10.1186/s12861-015-0076-7

    • PubMed
    • Google Scholar
73. 1. Mueller LD
    2. Bitner K

    (2015) The evolution of ovoviviparity in a temporally varying environment

    The American Naturalist 186:708–715.

    https://doi.org/10.1086/683661

    • PubMed
    • Google Scholar
74. 1. Ostrovsky AN
    2. Lidgard S
    3. Gordon DP
    4. Schwaha T
    5. Genikhovich G
    6. Ereskovsky AV

    (2016) Matrotrophy and placentation in invertebrates: a new paradigm

    Biological Reviews of the Cambridge Philosophical Society 91:673–711.

    https://doi.org/10.1111/brv.12189

    • PubMed
    • Google Scholar
75. 1. Padilla PA
    2. Nystul TG
    3. Zager RA
    4. Johnson ACM
    5. Roth MB

    (2002) Dephosphorylation of cell cycle-regulated proteins correlates with anoxia-induced suspended animation in Caenorhabditis elegans

    Molecular Biology of the Cell 13:1473–1483.

    https://doi.org/10.1091/mbc.01-12-0594

    • PubMed
    • Google Scholar
76. 1. Pickett CL
    2. Kornfeld K

    (2013) Age-related degeneration of the egg-laying system promotes matricidal hatching in Caenorhabditis elegans

    Aging Cell 12:544–553.

    https://doi.org/10.1111/acel.12079

    • PubMed
    • Google Scholar
77. 1. Poullet N
    2. Vielle A
    3. Gimond C
    4. Carvalho S
    5. Teotónio H
    6. Braendle C

    (2016) Complex heterochrony underlies the evolution of Caenorhabditis elegans hermaphrodite sex allocation

    Evolution; International Journal of Organic Evolution 70:2357–2369.

    https://doi.org/10.1111/evo.13032

    • PubMed
    • Google Scholar
78. 1. Ranganathan R
    2. Sawin ER
    3. Trent C
    4. Horvitz HR

    (2001) Mutations in the Caenorhabditis elegans serotonin reuptake transporter MOD-5 reveal serotonin-dependent and -independent activities of fluoxetine

    The Journal of Neuroscience 21:5871–5884.

    https://doi.org/10.1523/JNEUROSCI.21-16-05871.2001

    • PubMed
    • Google Scholar
79. 1. Ravi B
    2. Garcia J
    3. Collins KM

    (2018) Homeostatic feedback modulates the development of two-state patterned activity in a model serotonin motor circuit in Caenorhabditis elegans

    The Journal of Neuroscience 38:6283–6298.

    https://doi.org/10.1523/JNEUROSCI.3658-17.2018

    • PubMed
    • Google Scholar
80. 1. Ravi B
    2. Zhao J
    3. Chaudhry SI
    4. Signorelli R
    5. Bartole M
    6. Kopchock RJ
    7. Guijarro C
    8. Kaplan JM
    9. Kang L
    10. Collins KM

    (2021) Presynaptic Gαo (GOA-1) signals to depress command neuron excitability and allow stretch-dependent modulation of egg laying in Caenorhabditis elegans

    Genetics 218:iyab080.

    https://doi.org/10.1093/genetics/iyab080

    • PubMed
    • Google Scholar
81. Software

    1. R Development Core Team

    (2018) R: A language and environment for statistical computing

    R Foundation for Statistical Computing, Vienna, Austria.

    https://www.r-project.org/
82. 1. Recknagel H
    2. Carruthers M
    3. Yurchenko AA
    4. Nokhbatolfoghahai M
    5. Kamenos NA
    6. Bain MM
    7. Elmer KR

    (2021) The functional genetic architecture of egg-laying and live-bearing reproduction in common lizards

    Nature Ecology & Evolution 5:1546–1556.

    https://doi.org/10.1038/s41559-021-01555-4

    • PubMed
    • Google Scholar
83. 1. Reiner DJ
    2. Weinshenker D
    3. Thomas JH

    (1995) Analysis of dominant mutations affecting muscle excitation in Caenorhabditis elegans

    Genetics 141:961–976.

    https://doi.org/10.1093/genetics/141.3.961

    • Google Scholar
84. 1. Ringstad N
    2. Horvitz HR

    (2008) FMRFamide neuropeptides and acetylcholine synergistically inhibit egg-laying by C. elegans

    Nature Neuroscience 11:1168–1176.

    https://doi.org/10.1038/nn.2186

    • PubMed
    • Google Scholar
85. 1. Sandhu A
    2. Badal D
    3. Sheokand R
    4. Tyagi S
    5. Singh V

    (2021) Specific collagens maintain the cuticle permeability barrier in Caenorhabditis elegans

    Genetics 217:iyaa047.

    https://doi.org/10.1093/genetics/iyaa047

    • PubMed
    • Google Scholar
86. 1. Schafer WR
    2. Kenyon CJ

    (1995) A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans

    Nature 375:73–78.

    https://doi.org/10.1038/375073a0

    • PubMed
    • Google Scholar
87. 1. Schafer WR
    2. Sanchez BM
    3. Kenyon CJ

    (1996) Genes affecting sensitivity to serotonin in Caenorhabditis elegans

    Genetics 143:1219–1230.

    https://doi.org/10.1093/genetics/143.3.1219

    • Google Scholar
88. 1. Schafer WR

    (2005) Egg-laying

    WormBook 1:7.

    https://doi.org/10.1895/wormbook.1.38.1

    • PubMed
    • Google Scholar
89. 1. Schafer WR

    (2006) Genetics of egg-laying in worms

    Annual Review of Genetics 40:487–509.

    https://doi.org/10.1146/annurev.genet.40.110405.090527

    • Google Scholar
90. 1. Schierenberg E
    2. Junkersdorf B

    (1992) The role of eggshell and underlying vitelline membrane for normal pattern formation in the early C. elegans embryo

    Roux’s Archives of Developmental Biology 202:10–16.

    https://doi.org/10.1007/BF00364592

    • PubMed
    • Google Scholar
91. 1. Schindelin J
    2. Arganda-Carreras I
    3. Frise E
    4. Kaynig V
    5. Longair M
    6. Pietzsch T
    7. Preibisch S
    8. Rueden C
    9. Saalfeld S
    10. Schmid B
    11. Tinevez JY
    12. White DJ
    13. Hartenstein V
    14. Eliceiri K
    15. Tomancak P
    16. Cardona A

    (2012) Fiji: an open-source platform for biological-image analysis

    Nature Methods 9:676–682.

    https://doi.org/10.1038/nmeth.2019

    • PubMed
    • Google Scholar
92. 1. Schulenburg H
    2. Félix MA

    (2017) The natural biotic environment of Caenorhabditis elegans

    Genetics 206:55–86.

    https://doi.org/10.1534/genetics.116.195511

    • PubMed
    • Google Scholar
93. 1. Shyn SI
    2. Kerr R
    3. Schafer WR

    (2003) Serotonin and Go modulate functional states of neurons and muscles controlling C. elegans egg-laying behavior

    Current Biology 13:1910–1915.

    https://doi.org/10.1016/j.cub.2003.10.025

    • PubMed
    • Google Scholar
94. 1. Stein KK
    2. Golden A

    (2018) The C. elegans eggshell

    WormBook 2018:1–36.

    https://doi.org/10.1895/wormbook.1.179.1

    • PubMed
    • Google Scholar
95. 1. Stevens L
    2. Félix MA
    3. Beltran T
    4. Braendle C
    5. Caurcel C
    6. Fausett S
    7. Fitch D
    8. Frézal L
    9. Gosse C
    10. Kaur T
    11. Kiontke K
    12. Newton MD
    13. Noble LM
    14. Richaud A
    15. Rockman MV
    16. Sudhaus W
    17. Blaxter M

    (2019) Comparative genomics of 10 new Caenorhabditis species

    Evolution Letters 3:217–236.

    https://doi.org/10.1002/evl3.110

    • Google Scholar
96. 1. Stiernagle T

    (2006) Maintenance of C. elegans

    WormBook 1:11.

    https://doi.org/10.1895/wormbook.1.101.1

    • PubMed
    • Google Scholar
97. Book

    1. Sudhaus W

    (1976)

    Vergleichende Untersuchungen Zur Phylogenie, Systematik, Ökologie, Biologie Und Ethologie Der Rhabditidae (Nematoda)

    Zoologica.

    • Google Scholar
98. 1. Sulston JE
    2. Schierenberg E
    3. White JG
    4. Thomson JN

    (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans

    Developmental Biology 100:64–119.

    https://doi.org/10.1016/0012-1606(83)90201-4

    • Google Scholar
99. Book

    1. Trent C

    (1982)

    Genetic and Behavioral Studies of the Egg-Laying System of Caenorhabditis elegans

    Massachusetts Institute of Technology.

    • Google Scholar
100. 1. Trent C
     2. Tsuing N
     3. Horvitz HR

     (1983) Egg-laying defective mutants of the nematode Caenorhabditis elegans

     Genetics 104:619–647.

     https://doi.org/10.1093/genetics/104.4.619

     • PubMed
     • Google Scholar
101. 1. Trexler JC
     2. DeAngelis DL

     (2003) Resource allocation in offspring provisioning: an evaluation of the conditions favoring the evolution of matrotrophy

     The American Naturalist 162:574–585.

     https://doi.org/10.1086/378822

     • Google Scholar
102. 1. Trivers RL

     (1974) Parent-Offspring Conflict

     American Zoologist 14:249–264.

     https://doi.org/10.1093/icb/14.1.249

     • Google Scholar
103. 1. Van Voorhies WA
     2. Ward S

     (2000) Broad oxygen tolerance in the nematode Caenorhabditis elegans

     The Journal of Experimental Biology 203:2467–2478.

     https://doi.org/10.1242/jeb.203.16.2467

     • PubMed
     • Google Scholar
104. 1. Vielle A
     2. Callemeyn-Torre N
     3. Gimond C
     4. Poullet N
     5. Gray JC
     6. Cutter AD
     7. Braendle C

     (2016) Convergent evolution of sperm gigantism and the developmental origins of sperm size variability in Caenorhabditis nematodes

     Evolution 70:2485–2503.

     https://doi.org/10.1111/evo.13043

     • Google Scholar
105. 1. Vigne P
     2. Gimond C
     3. Ferrari C
     4. Vielle A
     5. Hallin J
     6. Pino-Querido A
     7. El Mouridi S
     8. Mignerot L
     9. Frøkjær-Jensen C
     10. Boulin T
     11. Teotónio H
     12. Braendle C

     (2021) A single-nucleotide change underlies the genetic assimilation of A plastic trait

     Science Advances 7:eabd9941.

     https://doi.org/10.1126/sciadv.abd9941

     • PubMed
     • Google Scholar
106. 1. Waggoner LE
     2. Zhou GT
     3. Schafer RW
     4. Schafer WR

     (1998) Control of alternative behavioral states by serotonin in Caenorhabditis elegans

     Neuron 21:203–214.

     https://doi.org/10.1016/s0896-6273(00)80527-9

     • PubMed
     • Google Scholar
107. 1. Waggoner LE
     2. Hardaker LA
     3. Golik S
     4. Schafer WR

     (2000) Effect of a neuropeptide gene on behavioral states in Caenorhabditis elegans egg-laying

     Genetics 154:1181–1192.

     https://doi.org/10.1093/genetics/154.3.1181

     • PubMed
     • Google Scholar
108. 1. Ward S
     2. Carrel JS

     (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans

     Developmental Biology 73:304–321.

     https://doi.org/10.1016/0012-1606(79)90069-1

     • PubMed
     • Google Scholar
109. 1. Weinshenker D
     2. Garriga G
     3. Thomas JH

     (1995) Genetic and pharmacological analysis of neurotransmitters controlling egg laying in C. elegans

     The Journal of Neuroscience 15:6975–6985.

     https://doi.org/10.1523/JNEUROSCI.15-10-06975.1995

     • PubMed
     • Google Scholar
110. 1. Weinshenker D
     2. Wei A
     3. Salkoff L
     4. Thomas JH

     (1999) Block of an ether-a-go-go-like K(+) channel by imipramine rescues egl-2 excitation defects in Caenorhabditis elegans

     The Journal of Neuroscience 19:9831–9840.

     https://doi.org/10.1523/JNEUROSCI.19-22-09831.1999

     • PubMed
     • Google Scholar
111. 1. White JG
     2. Southgate E
     3. Thomson JN
     4. Brenner S

     (1986) The structure of the nervous system of the nematode Caenorhabditis elegans

     Philosophical Transactions of the Royal Society of London. B, Biological Sciences 314:1–340.

     https://doi.org/10.1098/rstb.1986.0056

     • Google Scholar
112. 1. Whittington CM
     2. Van Dyke JU
     3. Liang SQT
     4. Edwards SV
     5. Shine R
     6. Thompson MB
     7. Grueber CE

     (2022) Understanding the evolution of viviparity using intraspecific variation in reproductive mode and transitional forms of pregnancy

     Biological Reviews of the Cambridge Philosophical Society 97:1179–1192.

     https://doi.org/10.1111/brv.12836

     • PubMed
     • Google Scholar
113. 1. Widmayer SJ
     2. Evans KS
     3. Zdraljevic S
     4. Andersen EC

     (2022) Evaluating the power and limitations of genome-wide association studies in Caenorhabditis elegans

     G3 12:jkac114.

     https://doi.org/10.1093/g3journal/jkac114

     • PubMed
     • Google Scholar
114. 1. Yue X
     2. Zhao J
     3. Li X
     4. Fan Y
     5. Duan D
     6. Zhang X
     7. Zou W
     8. Sheng Y
     9. Zhang T
     10. Yang Q
     11. Luo J
     12. Duan S
     13. Xiao R
     14. Kang L

     (2018) TMC proteins modulate egg laying and membrane excitability through a background leak conductance in C. elegans

     Neuron 97:571–585.

     https://doi.org/10.1016/j.neuron.2017.12.041

     • Google Scholar
115. 1. Zhang M
     2. Chung SH
     3. Fang-Yen C
     4. Craig C
     5. Kerr RA
     6. Suzuki H
     7. Samuel ADT
     8. Mazur E
     9. Schafer WR

     (2008) A self-regulating feed-forward circuit controlling C. elegans egg-laying behavior

     Current Biology 18:1445.

     https://doi.org/10.1016/j.cub.2008.08.047

     • PubMed
     • Google Scholar
116. 1. Zhao Y
     2. Long L
     3. Xu W
     4. Campbell RF
     5. Large EE
     6. Greene JS
     7. McGrath PT

     (2018) Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain

     eLife 7:e38675.

     https://doi.org/10.7554/eLife.38675

     • PubMed
     • Google Scholar

Author details

1. Laure Mignerot

   Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   Contributed equally with

   Clotilde Gimond

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3306-6244

2. Clotilde Gimond

   Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France

   Contribution

   Conceptualization, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   Contributed equally with

   Laure Mignerot

   Competing interests

   No competing interests declared

3. Lucie Bolelli

   Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

4. Charlotte Bouleau

   Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

5. Asma Sandjak

   Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

6. Thomas Boulin

   Institut NeuroMyoGène, CNRS, Inserm, Université de Lyon, Lyon, France

   Contribution

   Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1734-1915

7. Christian Braendle

   Université Côte d’Azur, CNRS, Inserm, IBV, Nice, France

   Contribution

   Conceptualization, Resources, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Methodology, Writing – original draft, Project administration

   For correspondence

   braendle@unice.fr

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0203-4581

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