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Regulators of an ancient polyphenism evolved through episodic protein divergence and parallel gene radiations.

ABSTRACT: Polyphenism is a form of developmental plasticity that transduces environmental cues into discontinuous, often disparate phenotypes. In some cases, polyphenism has been attributed to facilitating morphological diversification and even the evolution of novel traits. However, this process is predicated on the origins and evolutionary maintenance of genetic mechanisms that specify alternate developmental networks. When and how regulatory loci arise and change, specifically before and throughout the history of a polyphenism, is little understood. Here, we establish a phylogenetic and comparative molecular context for two dynamically evolving genes, eud-1 and seud-1, which regulate polyphenism in the nematode Pristionchus pacificus. This species is dimorphic in its adult feeding-structures, allowing individuals to become microbivores or facultative predators depending on the environment. Although polyphenism regulation is increasingly well understood in P. pacificus, the polyphenism is far older than this species and has diversified morphologically to enable an array of ecological functions across polyphenic lineages. To bring this taxonomic diversity into a comparative context, we reconstructed the histories of eud-1 and seud-1 relative to the origin and diversification of polyphenism, finding that homologues of both genes have undergone lineage-specific radiations across polyphenic taxa. Further, we detected signatures of episodic diversifying selection on eud-1, particularly in early diplogastrid lineages. Lastly, transgenic rescue experiments suggest that the gene's product has functionally diverged from its orthologue's in a non-polyphenic outgroup. In summary, we provide a comparative framework for the molecular components of a plasticity switch, enabling studies of how polyphenism, its regulation, and ultimately its targets evolve.

SUBMITTER: Biddle JF

PROVIDER: S-EPMC7062019 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Regulators of an ancient polyphenism evolved through episodic protein divergence and parallel gene radiations.

Biddle Joseph F JF Ragsdale Erik J EJ

Proceedings. Biological sciences 20200226 1921

Polyphenism is a form of developmental plasticity that transduces environmental cues into discontinuous, often disparate phenotypes. In some cases, polyphenism has been attributed to facilitating morphological diversification and even the evolution of novel traits. However, this process is predicated on the origins and evolutionary maintenance of genetic mechanisms that specify alternate developmental networks. When and how regulatory loci arise and change, specifically before and throughout the ...[more]

PMID: 32098612

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Project description:Background and aimsZingiberales comprise a clade of eight tropical monocot families including approx. 2500 species and are hypothesized to have undergone an ancient, rapid radiation during the Cretaceous. Zingiberales display substantial variation in floral morphology, and several members are ecologically and economically important. Deep phylogenetic relationships among primary lineages of Zingiberales have proved difficult to resolve in previous studies, representing a key region of uncertainty in the monocot tree of life.MethodsNext-generation sequencing was used to construct complete plastid gene sets for nine taxa of Zingiberales, which were added to five previously sequenced sets in an attempt to resolve deep relationships among families in the order. Variation in taxon sampling, process partition inclusion and partition model parameters were examined to assess their effects on topology and support.Key resultsCodon-based likelihood analysis identified a strongly supported clade of ((Cannaceae, Marantaceae), (Costaceae, Zingiberaceae)), sister to (Musaceae, (Lowiaceae, Strelitziaceae)), collectively sister to Heliconiaceae. However, the deepest divergences in this phylogenetic analysis comprised short branches with weak support. Additionally, manipulation of matrices resulted in differing deep topologies in an unpredictable fashion. Alternative topology testing allowed statistical rejection of some of the topologies. Saturation fails to explain observed topological uncertainty and low support at the base of Zingiberales. Evidence for conflict among the plastid data was based on a support metric that accounts for conflicting resampled topologies.ConclusionsMany relationships were resolved with robust support, but the paucity of character information supporting the deepest nodes and the existence of conflict suggest that plastid coding regions are insufficient to resolve and support the earliest divergences among families of Zingiberales. Whole plastomes will continue to be highly useful in plant phylogenetics, but the current study adds to a growing body of literature suggesting that they may not provide enough character information for resolving ancient, rapid radiations.

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Regulators of an ancient polyphenism evolved through episodic protein divergence and parallel gene radiations.

Publications

Regulators of an ancient polyphenism evolved through episodic protein divergence and parallel gene radiations.

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