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.
- PAR ID:
- 10475889
- Publisher / Repository:
- Proceedings of the National Academy of Sciences of the United States of America
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 120
- Issue:
- 32
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- e2308816120
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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.more » « less
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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 nematode
Pristionchus 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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Abstract 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 nematode
Pristionchus pacificus . SEUD-1 is expressed in cells producing dimorphic morphologies, thereby integrating an intercellular signalling mechanism at its ultimate target. Additionally, multiple alterations ofseud-1 support it as a potential target for plasticity evolution. First, a recent duplication ofseud-1 in 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. -
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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 gene
spr-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.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2308816120
