Developmental Plasticity and Robustness of a Nematode Mouth-Form Polyphenism

Abstract

In the last decade, case studies in plants and animals provided increasing insight into the molecular mechanisms of developmental plasticity. When complemented with evolutionary and ecological analyses, these studies suggest that plasticity represents a mechanism facilitating adaptive change, increasing diversity and fostering the evolution of novelty. Here, we summarize genetic, molecular and evolutionary studies on developmental plasticity of feeding structures in nematodes, focusing on the model organism Pristionchus pacificus and its relatives. Like its famous cousin Caenorhabditis elegans, P. pacificus reproduces as a self-fertilizing hermaphrodite and can be cultured in the laboratory on E. coli indefinitely with a four-day generation time. However, in contrast to C. elegans, Pristionchus worms show more complex feeding structures in adaptation to their life history. Pristionchus nematodes live in the soil and are reliably found in association with scarab beetles, but only reproduce after the insects' death. Insect carcasses usually exist only for a short time period and their turnover is partially unpredictable. Strikingly, Pristionchus worms can have two alternative mouth-forms; animals are either stenostomatous (St) with a single tooth resulting in strict bacterial feeding, or alternatively, they are eurystomatous (Eu) with two teeth allowing facultative predation. Laboratory-based studies revealed a regulatory network that controls the irreversible decision of individual worms to adopt the St or Eu form. These studies revealed that a developmental switch controls the mouth-form decision, confirming long-standing theory about the role of switch genes in developmental plasticity. Here, we describe the current understanding of P. pacificus mouth-form regulation. In contrast to plasticity, robustness describes the property of organisms to produce unchanged phenotypes despite environmental perturbations. While largely opposite in principle, the relationship between developmental plasticity and robustness has only rarely been tested in particular study systems. Based on a study of the Hsp90 chaperones in nematodes, we suggest that robustness and plasticity are indeed complementary concepts. Genetic switch networks regulating plasticity require robustness to produce reproducible responses to the multitude of environmental inputs and the phenotypic output requires robustness because the range of possible phenotypic outcomes is constrained. Thus, plasticity and robustness are actually not mutually exclusive, but rather complementary concepts.

Keywords: Caenorhabditis elegans; Hsp chaperones; Pristionchus pacificus; developmental plasticity; robustness; switch genes.

FIGURE 1

(A) Conceptual mechanism of the genetic regulation of plastic development. Environmental inputs are processed and integrated by a network of genes, referred to as switch genes. The switch network takes a decision to activate one of the alternative developmental programs and passes the signal down to a genetic network that executes the selected phenotype. (B,C) Hypothetical scenarios of change in the reaction norm of a continuously (B) or discontinuously (C) plastic trait in the conditions when the switch network or the phenotype execution network is impaired. The original distribution of phenotypes is shown in black in the foreground or gray in the background, altered distribution resulting from impairment of the switch network is shown in red and altered distribution resulting from incorrect execution of the phenotype is shown in blue.

FIGURE 2

(A) The eurystomatous morph of P. pacificus devouring a larva of C. elegans. (B,C) The mouth of the eurystomatous (B) and of the stenostomatous (C) morph. On the left, differential interference contrast (DIC) image. On the right, overlay of the DIC image and an image of fluorescein-stained cuticle at the base of the buccal cavity, which includes teeth. Arrows point at the tips of teeth. (D) Current model of the regulation of mouth-form plasticity in P. pacificus. The genes shown are part of the switch network, i.e., mutations in these genes only change the frequencies of alternative phenotypes in the population. (E,F) Phenotypic effects caused by impairment of Hsp90 heat shock proteins, which are known to provide robustness to phenotype execution networks. In these conditions, both morphs are still produced but the morphologies are abnormal. (E) PCA ordination of sets of landmarks representing control individuals and individuals exposed to heat stress and treatment by radicicol, a pharmacological inhibitor of Hsp90. (F) Morphological disparity within different groups shown in the PCA ordination in panel E. Error bars show SD. n.s., not significant (P-value > 0.05); ^∗∗P-value < 0.01; ^∗∗∗P-value < 0.001. Panels E and F reproduced from Sieriebriennikov et al. (2017).