Natural variation in the Caenorhabditis elegans egg-laying circuit modulates an intergenerational fitness trade-off

Evolutionary shifts from egg-laying (oviparity) to live birth (viviparity) are common across diverse taxa, and some species exhibit variability in egg-laying modes or an intermediate mode with eggs containing embryos at various stages of development. How such natural quantitative variation in egg retention arises through differences in genetics, behaviour, and physiology - and how this variation ultimately connects to variation in specific fitness components - remains poorly understood. Here, we investigate intraspecific variation in egg retention in the nematode Caenorhabditis elegans using a panel of 316 wild strains. We observe highly variable intra-uterine egg retention, with some strains exhibiting strongly reduced or increased retention with internal hatching. We identify multiple evolutionary origins of these phenotypic extremes and pinpoint candidate loci responsible for the observed variation. Analysis of a subset of strains confirms that natural variation in egg-laying behaviour contributes to differences in egg retention. Using neuromodulatory agents and CRISPR-Cas9-mediated genetic manipulation, we demonstrate that this behavioural variation arises from an evolutionarily divergent neuromodulatory architecture in the egg-laying circuitry. In addressing the question of why natural variation in C. elegans egg retention is maintained, we find that strong egg retention can reduce maternal fertility and survival due to detrimental hatching in utero. However, genotypes with strong egg retention may benefit from improved offspring protection against environmental insults and gain a competitive advantage with offspring exhibiting a shortened development time to reproductive maturity outside the uterus. The observed natural variation in egg-laying behaviour in C. elegans could therefore reflect modifications of a trade-off between alternative fitness components across generations. Our study reveals previously underappreciated diversity in the C. elegans egg-laying circuit and provides insights into the fitness consequences of this behavioural variation. We propose that intraspecific variation in nematode egg-laying behaviour offers an ideal system to identify molecular changes underlying evolutionary transitions between oviparity and viviparity in invertebrates.