A species-specific nuclear receptor was integrated into a developmental polyphenism pathway

Polyphenism, the ability of an organism to develop discrete, alternative forms of a trait in response to environmental signals, relies on molecular switches to guide developmental trajectories. In the nematode Pristionchus pacificus, such a switch produces a dimorphism in its adult feeding structures, enabling individuals to develop as either microbivores or predators based on the environments they experience before adulthood. Several regulators of this polyphenism are known, giving an opportunity to determine the ultimate molecular targets of a plastic transcriptional response and to reconstruct their evolutionary fates. Because nuclear receptors (NRs) are rapid molecular sensors of intrinsic and sometimes extrinsic signals, they provide likely candidates to link a switch mechanism to the alternative phenotypes produced. Here, we report the results of a reverse genetic screen of NRs, specifically those whose expression is influenced by the polyphenism, for their possible influence on polyphenism-related traits. Our screen identified a gene, pnhr-3, that influences the sensitivity of the polyphenism in P. pacificus. Phylogenetic analysis and microsynteny show that pnhr-3 is unique to this species. Additionally, its parent gene does not show polyphenism-biased expression, indicating that this new gene was recently recruited into an established molecular pathway. Along with 3 other NRs, which are also lineage-specific relative to outgroups that lack the polyphenism, pnhr-3 impacts other traits that also respond to resource conditions, influencing a polyphenism. Our findings highlight the short time scale in which a recently duplicated transcription factor with new putative regulatory sequences can be adopted into a regulatory pathway for plastic development.