Experimental and theoretical support for costs of plasticity and phenotype in a nematode cannibalistic trait

Abstract

Developmental plasticity is the ability of a genotype to express multiple phenotypes under different environmental conditions and has been shown to facilitate the evolution of novel traits. However, while the associated cost of plasticity, i.e., the loss in fitness due to the ability to express plasticity in response to environmental change, and the cost of phenotype, i.e., the loss of fitness due to expressing a fixed phenotype across environments, have been theoretically predicted, empirically such costs remain poorly documented and little understood. Here, we use a plasticity model system, hermaphroditic nematode Pristionchus pacificus, to experimentally measure these costs in wild isolates under controlled laboratory conditions. P. pacificus can develop either a bacterial feeding or predatory mouth morph in response to different external stimuli, with natural variation of mouth-morph ratios between strains. We first demonstrated the cost of phenotype by analyzing fecundity and developmental speed in relation to mouth morphs across the P. pacificus phylogenetic tree. Then, we exposed P. pacificus strains to two distinct microbial diets that induce strain-specific mouth-form ratios. Our results indicate that the plastic strain does shoulder a cost of plasticity, i.e., the diet-induced predatory mouth morph is associated with reduced fecundity and slower developmental speed. In contrast, the non-plastic strain suffers from the cost of phenotype since its phenotype does not change to match the unfavorable bacterial diet but shows increased fitness and higher developmental speed on the favorable diet. Furthermore, using a stage-structured population model based on empirically derived life history parameters, we show how population structure can alleviate the cost of plasticity in P. pacificus. The results of the model illustrate the extent to which the costs associated with plasticity and its effect on competition depend on ecological factors. This study provides support for costs of plasticity and phenotype based on empirical and modeling approaches.

The role of plasticity and stochasticity in coexistence

“…The experimental measurements reported in Dardiry et al. (2023) reveal how the two bacterial diets drastically affect both the probability of developing the predatory mouth form and fecundity (Figure 2). With regards to the former, on E. coli OP50, strain A has the lowest probability of developing the predatory mouth form ($$$ \mu =\mathrm{0.11,0.01}\leqslant 95\%\mathrm{HDI}\leqslant 0.25 $$$), whereas strain B has an intermediate probability of developing the predatory mouth form ($$$ \mu =\mathrm{0.56,0.38}\leqslant 95\%\mathrm{HDI}\leqslant 0.75 $$$).…”

“…In order to construct an individual‐based model rooted in experimental observations, we took advantage of a dataset of laboratory measurements of three strains of P. pacificus previously published in Dardiry et al. (2023). This dataset includes measurements of fecundity and mouth‐from plasticity for each strain on E. coli OP50 and Novosphingobium sp.…”

“…The likelihood of assuming the Eu or St mouth form is determined by an interplay between the gene regulatory network and a wide range of environmental factors, e.g., culture conditions, temperature, and bacterial diet (Akduman et al, 2020;Lenuzzi et al, 2021;Werner et al, 2017Werner et al, , 2018. Natural isolates of P. pacificus display substantial variation in the likelihood of assuming one of the two mouth forms in identical environments (Dardiry et al, 2023;Ragsdale et al, 2013). In many ways, mouth-form plasticity in P. pacificus is more reminiscent of the switch between lytic and lysogenic cycles in bacteriophages (Ptashne, 2004) than cases of seasonal plasticity such as wing patterns in butterflies and other insects (Brakefield et al, 2003;Nijhout, 1994;van der Burg & Reed, 2021).…”

“…In order to construct an individual-based model rooted in experimental observations, we took advantage of a dataset of laboratory measurements of three strains of P. pacificus previously published in Dardiry et al (2023).…”

“…Here, we use P. pacificus to investigate the role of phenotypic plasticity in coexistence in animals. We take advantage of the fact that bacterial diet has the most profound influence on mouth‐form plasticity and fecundity in P. pacificus (Akduman et al., 2020; Dardiry et al., 2023). We use laboratory measurements on the effects of two bacterial diets—the standard laboratory food source Escherichia coli OP50 and environmentally derived bacterium Novospinghobium L76—on mouth‐form plasticity and the fecundity of three P. pacificus strains (henceforth, referred to as strains A, B, and C).…”