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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.

 

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. 

Resource polyphenism—the occurrence of environmentally induced, discrete, and intraspecific morphs showing differential niche use—is taxonomically widespread and fundamental to the evolution of ecological function where it has arisen. Despite longstanding appreciation for the ecological and evolutionary significance of resource polyphenism, only recently have its proximate mechanisms begun to be uncovered. Polyphenism switches, especially those influencing and influenced by trophic interactions, offer a route to integrating proximate and ultimate causation in studies of plasticity, and its potential influence on evolution more generally. Here, we use the major events in generalized polyphenic development as a scaffold for linking the molecular mechanisms of polyphenic switching with potential evolutionary outcomes of polyphenism and for discussing challenges and opportunities at each step in this process. Not only does the study of resource polyphenism uncover interesting details of discrete plasticity, it also illuminates and informs general principles at the intersection of development, ecology, and evolution. 

Pristionchus pacificusis a nematode model for the developmental genetics of morphological polyphenism, especially at the level of individual cells. Morphological polyphenism in this species includes an evolutionary novelty, moveable teeth, which have enabled predatory feeding in this species and others in its family (Diplogastridae). From transmission electron micrographs of serial thin sections through an adult hermaphrodite ofP. pacificus, we three‐dimensionally reconstructed all epithelial and myoepithelial cells and syncytia, corresponding to 74 nuclei, of its face, mouth, and pharynx. We found that the epithelia that produce the predatory morphology ofP. pacificusare identical toCaenorhabditis elegansin the number of cell classes and nuclei. However, differences in cell form, spatial relationships, and nucleus position correlate with gross morphological differences fromC. elegansand outgroups. Moreover, we identified fine‐structural features, especially in the anteriormost pharyngeal muscles, that underlie the conspicuous, left‐right asymmetry that characterizes theP. pacificusfeeding apparatus. Our reconstruction provides an anatomical map for studying the genetics of polyphenism, feeding behavior, and the development of novel form in a satellite model toC. elegans.

 

Abstract Developmental polyphenism, the ability to switch between phenotypes in response to environmental variation, involves the alternating activation of environmentally sensitive genes. Consequently, to understand how a polyphenic response evolves requires a comparative analysis of the components that make up environmentally sensitive networks. Here, we inferred coexpression networks for a morphological polyphenism, the feeding-structure dimorphism of the nematode Pristionchus pacificus. In this species, individuals produce alternative forms of a novel trait—moveable teeth, which in one morph enable predatory feeding—in response to environmental cues. To identify the origins of polyphenism network components, we independently inferred coexpression modules for more conserved transcriptional responses, including in an ancestrally nonpolyphenic nematode species. Further, through genome-wide analyses of these components across the nematode family (Diplogastridae) in which the polyphenism arose, we reconstructed how network components have changed. To achieve this, we assembled and resolved the phylogenetic context for five genomes of species representing the breadth of Diplogastridae and a hypothesized outgroup. We found that gene networks instructing alternative forms arose from ancestral plastic responses to environment, specifically starvation-induced metabolism and the formation of a conserved diapause (dauer) stage. Moreover, loci from rapidly evolving gene families were integrated into these networks with higher connectivity than throughout the rest of the P. pacificus transcriptome. In summary, we show that the modular regulatory outputs of a polyphenic response evolved through the integration of conserved plastic responses into networks with genes of high evolutionary turnover. 

Polyphenism, the extreme form of developmental plasticity, is the ability of a genotype to produce discrete morphologies matched to alternative environments. Because polyphenism is likely to be under switch-like molecular control, a comparative genetic approach could reveal the molecular targets of plasticity evolution. Here we report that the lineage-specific sulfotransferase SEUD-1, which responds to environmental cues, dosage-dependently regulates polyphenism of mouthparts in the nematodePristionchus pacificus. SEUD-1 is expressed in cells producing dimorphic morphologies, thereby integrating an intercellular signalling mechanism at its ultimate target. Additionally, multiple alterations ofseud-1support it as a potential target for plasticity evolution. First, a recent duplication ofseud-1in a sister species reveals a direct correlation between genomic dosage and polyphenism threshold. Second, inbreeding to produce divergent polyphenism thresholds resulted in changes in transcriptional dosage ofseud-1. Our study thus offers a genetic explanation for how plastic responses evolve.

 

A recent accumulation of studies has demonstrated that nongenetic, maternally transmitted factors are often critical to the health and development of offspring and can therefore play a role in ecological and evolutionary processes. In particular, microorganisms such as bacteria have been championed as heritable, symbiotic partners capable of conferring fitness benefits to their hosts. At the same time, parents may also pass various nonmicrobial organisms to their offspring, yet the roles of such organisms in shaping the developmental environment of their hosts remain largely unexplored. Here, we show that the nematodeDiplogastrellus monhysteroidesis transgenerationally inherited and sexually transmitted by the dung beetleOnthophagus taurus. By manipulating artificial chambers in which beetle offspring develop, we demonstrate that the presence ofD. monhysteroidesnematodes enhances the growth of beetle offspring, empirically challenging the paradigm that nematodes are merely commensal or even detrimental to their insect hosts. Finally, our research presents a compelling mechanism whereby the nematodes influence the health of beetle larvae:D. monhysteroidesnematodes engineer the bacterial and fungal communities that also inhabit the beetle developmental chambers, including specific taxa known to be involved in biomass degradation, possibly allowing larval beetles better access to their otherwise recalcitrant, plant-based diet. Thus, our findings illustrate that nongenetic inheritance can include intermediately sized organisms that live and proliferate in close association with, and in certain cases enhance, the development of their hosts’ offspring.

 

The ability to translate a single genome into multiple phenotypes, or developmental plasticity, defines how phenotype derives from more than just genes. However, to study the evolutionary targets of plasticity and their evolutionary fates, we need to understand how genetic regulators of plasticity control downstream gene expression. Here, we have identified a transcriptional response specific to polyphenism (i.e., discrete plasticity) in the nematode Pristionchus pacificus. This species produces alternative resource-use morphs—microbivorous and predatory forms, differing in the form of their teeth, a morphological novelty—as influenced by resource availability. Transcriptional profiles common to multiple polyphenism-controlling genes in P. pacificus reveal a suite of environmentally sensitive loci, or ultimate target genes, that make up an induced developmental response. Additionally, in vitro assays show that one polyphenism regulator, the nuclear receptor NHR-40, physically binds to promoters with putative HNF4α (the nuclear receptor class including NHR-40) binding sites, suggesting this receptor may directly regulate genes that describe alternative morphs. Among differentially expressed genes were morph-limited genes, highlighting factors with putative “on–off” function in plasticity regulation. Further, predatory morph-biased genes included candidates—namely, all four P. pacificus homologs of Hsp70, which have HNF4α motifs—whose natural variation in expression matches phenotypic differences among P. pacificus wild isolates. In summary, our study links polyphenism regulatory loci to the transcription producing alternative forms of a morphological novelty. Consequently, our findings establish a platform for determining how specific regulators of morph-biased genes may influence selection on plastic phenotypes.