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.

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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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