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1. Data from: Genomic parallelism defines repeated evolution of an inducible offense

   https://doi.org/10.5061/dryad.1zcrjdg33  

   Levis, Nicholas; Ragsdale, Erik (January 2025, Dryad)

   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. 

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2. Natural variation reveals functional and genetic integration of a polyphenism

   https://doi.org/10.1093/icb/icag005  

   Nicholson, Rose M; Levis, Nicholas A; Allison, Marc R; Geis, Elizabeth A; Ragsdale, Erik J (February 2026, Integrative And Comparative Biology)

   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. 

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3. Multiple Plasticity Regulators Reveal Targets Specifying an Induced Predatory Form in Nematodes

   https://doi.org/10.1093/molbev/msz171  

   Bui, Linh T; Ragsdale, Erik J (July 2019, Molecular Biology and Evolution)

   Abstract 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. 

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4. Polyphenism of a Novel Trait Integrated Rapidly Evolving Genes into Ancestrally Plastic Networks

   https://doi.org/10.1093/molbev/msaa235  

   Casasa, Sofia; Biddle, Joseph F; Koutsovoulos, Georgios D; Ragsdale, Erik J (September 2020, Molecular Biology and Evolution)

   Ruvinsky, Ilya (Ed.)

   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. 

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5. Genetic regulators of a resource polyphenism interact to couple predatory morphology and behaviour

   https://doi.org/10.1098/rspb.2024.0153  

   Nicholson, Rose M; Levis, Nicholas A; Ragsdale, Erik J (June 2024, Proceedings of the Royal Society B: Biological Sciences)

   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. 

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