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Abstract Polyphenism, the ability of an organism to develop discrete, alternative forms of a trait in response to environmental signals, relies on molecular switches to guide developmental trajectories. In the nematode Pristionchus pacificus, such a switch produces a dimorphism in its adult feeding structures, enabling individuals to develop as either microbivores or predators based on the environments they experience before adulthood. Several regulators of this polyphenism are known, giving an opportunity to determine the ultimate molecular targets of a plastic transcriptional response and to reconstruct their evolutionary fates. Because nuclear receptors (NRs) are rapid molecular sensors of intrinsic and sometimes extrinsic signals, they provide likely candidates to link a switch mechanism to the alternative phenotypes produced. Here, we report the results of a reverse genetic screen of NRs, specifically those whose expression is influenced by the polyphenism, for their possible influence on polyphenism-related traits. Our screen identified a gene, pnhr-3, that influences the sensitivity of the polyphenism in P. pacificus. Phylogenetic analysis and microsynteny show that pnhr-3 is unique to this species. Additionally, its parent gene does not show polyphenism-biased expression, indicating that this new gene was recently recruited into an established molecular pathway. Along with 3 other NRs, which are also lineage-specific relative to outgroups that lack the polyphenism, pnhr-3 impacts other traits that also respond to resource conditions, influencing a polyphenism. Our findings highlight the short time scale in which a recently duplicated transcription factor with new putative regulatory sequences can be adopted into a regulatory pathway for plastic development. 

Abstract Plasticity is a widespread feature of development, enabling phenotypic change based on the environment. Although the evolutionary loss of plasticity has been linked both theoretically and empirically to increased rates of phenotypic diversification, molecular insights into how this process might unfold are generally lacking. Here, we show that a regulator of nongenetic inheritance links evolutionary loss of plasticity in nature to changes in plasticity and morphology as selected in the laboratory. Across nematodes of Diplogastridae, which ancestrally had a polyphenism, or discrete plasticity, in their feeding morphology, we use molecular evolutionary analyses to screen for change associated with independent losses of plasticity. Having inferred a set of ancestrally polyphenism-biased genes from phylogenetically informed gene-knockouts and gene-expression comparisons, selection signatures associated with plasticity’s loss identify the histone H3K4 di/monodemethylase genespr-5/LSD1/KDM1A. Manipulations of this gene affect both sensitivity and variation in plastic morphologies, and artificial selection of manipulated lines drive multigenerational shifts in these phenotypes. Our findings thus give mechanistic insight into how traits are modified as they traverse the continuum of greater to lesser environmental sensitivity. 

Integration and modularity can have a profound impact on the function and evolution of environmentally responsive traits, especially when they result in discrete, alternative forms—that is, developmental polyphenism. An unresolved issue for understanding this impact is the degree to which the genetic architectures of the individual components of a plastic trait permit independent versus coordinated evolution. The association of trait variation with genomic variation can provide a test of whether the same loci influence different components of the same integrated phenotype. An example of a coordinated, plastic trait is in the shark-tooth nematode Pristionchus pacificus, which develops into either a bacterial-feeding or a predatory adult morph, depending on its perception of local food availability. Moreover, this polyphenism, when measured as morph induction in response to a common set of cues, differs across natural isolates of the species. By creating recombinant inbred lines (RILs) from natural isolates that have diverged in their morph-induction bias, followed by quantitative trait locus analysis, we tested whether and the extent to which component traits of this resource polyphenism are linked. We found that RILs with more frequent induction of the predatory morph also produced Eu individuals that were more effective predators. We also found that these two traits are associated with the same major-effect locus, suggesting that their causal genes are physically linked, if not the same, and are therefore likely to experience coordinated selection. In contrast, we found that morphological variation was not linked to these two traits and that such variation within each morph was even independent of variation in the other. Our findings show that the same coordinated plastic trait exhibits a blend of genetic correlation and independence, whose balance shapes the trait’s evolutionary potential. 

A common developmental response to resource competition is an inducible offense, the facultative predation of competitors. At its extreme, this response involves the development of alternative phenotypic morphs, or polyphenism. However, how polyphenism evolves to meet ecological challenges, such as competitor species, is unknown. Using replicated experimental evolution, during which starved nematodes could consume heterospecific competitors, we investigated whether induction of a predatory morph could evolve and how generalizable this change’s genetic basis is. Fifty generations of evolution across multiple populations resulted in parallel changes in higher morph-induction and parallel genomic responses, including repeated selection for a specific transcription-factor binding-site variant. In tandem, we artificially selected directly for tooth morphology and drove the predatory morph near to fixation. That trait-specific selection promoted greater changes in predatory morph induction than experimental evolution indicates that polyphenism evolution is balanced by selection for whole-organism performance. Our results thus describe the predictability by which a resource polyphenism evolves amid scarce resources. 

competitors. At its extreme, this response involves the development of alternative phenotypic morphs, or polyphenism. However, how polyphenism evolves to meet ecological challenges, such as competitor species, is unknown. Using replicated experimental evolution, during which starved nematodes could consume heterospecific competitors, we investigated whether induction of a predatory morph could evolve and how generalizable this change’s genetic basis is. Fifty generations of evolution across multiple populations resulted in parallel changes in higher morph-induction and parallel genomic responses, including repeated selection for a specific transcription-factor binding-site variant. In tandem, we artificially selected directly for tooth morphology and drove the predatory morph near to fixation. That trait-specific selection promoted greater changes in predatory morph induction than experimental evolution indicates that polyphenism evolution is balanced by selection for whole-organism performance. Our results thus describe the predictability by which a resource polyphenism evolves amid scarce resources. 

Phenotypic plasticity often requires the coordinated response of multiple traits observed individually as morphological, physiological or behavioural. The integration, and hence functionality, of this response may be influenced by whether and how these component traits share a genetic basis. In the case of polyphenism, or discrete plasticity, at least part of the environmental response is categorical, offering a simple readout for determining whether and to what degree individual components of a plastic response can be decoupled. Here, we use the nematodePristionchus pacificus, which has a resource polyphenism allowing it to be a facultative predator of other nematodes, to understand the genetic integration of polyphenism. The behavioural and morphological consequences of perturbations to the polyphenism’s genetic regulatory network show that both predatory activity and ability are strongly influenced by morphology, different axes of morphological variation are associated with different aspects of predatory behaviour, and rearing environment can decouple predatory morphology from behaviour. Further, we found that interactions between some polyphenism-modifying genes synergistically affect predatory behaviour. Our results show that the component traits of an integrated polyphenic response can be decoupled and, in principle, selected upon individually, and they suggest that multiple routes to functionally comparable phenotypes are possible. 

Polyphenism is a type of developmental plasticity that translates continuous environmental variability into discontinuous phenotypes. Such discontinuity likely requires a switch between alternative gene-regulatory networks, a principle that has been borne out by mechanisms found to promote morph-specific gene expression. However, whether robustness is required to execute a polyphenism decision has awaited testing at the molecular level. Here, we used a nematode model for polyphenism,Pristionchus pacificus, to identify the molecular regulatory factors that ensure the development of alternative forms. This species has a dimorphism in its adult feeding structures, specifically teeth, which are a morphological novelty that allows predation on other nematodes. Through a forward genetic screen, we determined that a duplicate homolog of the Mediator subunit MDT-15/MED15,P. pacificusMDT-15.1, is necessary for the polyphenism and the robustness of the resulting phenotypes. This transcriptional coregulator, which has a conserved role in metabolic responses to nutritional stress, coordinates these processes with its effects on this diet-induced polyphenism. Moreover, this MED15 homolog genetically interacts with two nuclear receptors, NHR-1 and NHR-40, to achieve dimorphism: Single and double mutants for these three factors result in morphologies that together produce a continuum of forms between the extremes of the polyphenism. In summary, we have identified a molecular regulator that confers discontinuity to a morphological polyphenism, while also identifying a role for MED15 as a plasticity effector.