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.
- Award ID(s):
- 1911688
- PAR ID:
- 10250483
- Editor(s):
- Ruvinsky, Ilya
- Date Published:
- Journal Name:
- Molecular Biology and Evolution
- Volume:
- 38
- Issue:
- 2
- ISSN:
- 1537-1719
- Page Range / eLocation ID:
- 331 to 343
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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,more » « less
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. pacificus MDT-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. -
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. -
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
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