Opposing directions of stage-specific body shape change in a close relative of C. elegans

Abstract

Background Body size is a fundamental organismal trait. However, as body size and ecological contexts change across developmental time, evolutionary divergence may cause unexpected patterns of body size diversity among developmental stages. This may be particularly evident in polyphenic developmental stages specialized for dispersal. The dauer larva is such a stage in nematodes, and Caenorhabditis species disperse by traveling on invertebrate carriers. Here, we describe the morphology of a stress-resistant, dauer-like larval stage of the nematode Caenorhabditis inopinata, whose adults can grow to be nearly twice as long as its close relative, the model organism C. elegans. Results We find that a dauer-like, stress-resistant larval stage in two isolates of C. inopinata is on average 13% shorter and 30% wider than the dauer larvae of C. elegans, despite its much longer adult stage. Additionally, many C. inopinata dauer-like larvae were ensheathed, a possible novelty in this lineage reminiscent of the infective juveniles of parasitic nematodes. Variation in dauer-like larva formation frequency among twenty-four wild isolates of C. inopinata was also observed, although frequencies were low across all isolates (< 2%), with many isolates unable to produce dauer-like larvae under conventional laboratory conditions. Conclusion Most Caenorhabditis species thrive on rotting plants and disperse on snails, slugs, or isopods (among others) whereas C. inopinata is ecologically divergent and thrives in fresh Ficus septica figs and disperses on their pollinating wasps. While there is some unknown factor of the fig environment that promotes elongated body size in C. inopinata adults, the small size or unique life history of its fig wasp carrier may be driving the divergent morphology of its stress-resistant larval stages. Further characterization of the behavior, development, and morphology of this stage will refine connections to homologous developmental stages in other species and determine whether ecological divergence across multiple developmental stages can promote unexpected and opposing changes in body size dimensions within a single species.

Automated scoring of nematode nictation on a textured background

“…A characteristic of dauers that distinguishes them from other life stages is increased resistance to SDS [2]. Our liquid culture animals increase in SDS resistance over the course of the six days after feeding (Figure 5C) , while length changes little (Figure S8) , staying within the reported range for C. elegans dauers [50], suggesting that the increase in nictation coincides with the transition of these animals from L2d pre-dauers to dauer larvae. These findings demonstrate our ability to automate the scoring of nictation in C. elegans dauers.…”

Widespread changes in gene expression accompany body size evolution in nematodes

“…Thus, its behavioral and stress-response regimes are likely to be tuned to a radically different natural context, thus driving patterns of divergently developmentally dynamic expression in the genes underlying these biological functions. Consistent with this, the stress-resistant dauer stage has diverged in C. inopinata , exhibiting an apparent loss of radial constriction and a far lower prevalence in laboratory conditions than C. elegans (Hammerschmith et al . 2022).…”

Automated scoring of nematode nictation on a textured background

“…Our liquid culture animals increase in SDS resistance over the course of the six days after feeding ( Fig 5C ) , while length changes little ( S8 Fig ) , staying within the reported range for C . elegans dauers [ 44 ], suggesting that the increase in nictation coincides with the transition of these animals from L2d pre-dauers to dauer larvae. These findings demonstrate our ability to automate the scoring of nictation in C .…”