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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. 

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.