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Abstract:
Supergenes are polymorphic multi-gene complexes that regulate the formation of alternative phenotypes, such as in the iconic examples of primrose heterostyly or butterfly mimicry. Despite recent progress, in the majority of examples to date the identities of the causal genes are unknown or their roles remain untested. Also, alternative morphs are traditionally linked to different haplotypes, but the supergene concept may also extend to phenotypic plasticity, i.e. to environmentally induced phenotypes formed in isogenic background. Here, we show the first example of a supergene regulating plasticity. The locus controlling developmental switching between predatory and microbivorous morphs in the nematode Pristionchus pacificus contains two sulfatases and two α-N-acetylglucosaminidases (nag) in an inverted tandem configuration. We provide functional characterization of all supergene constituents using CRISPR/Cas9-based reverse genetics and show that the nag genes and the previously identified eud-1/sulfatase have opposite phenotypic effects. These genes show non- overlapping neuronal expression and epistatic relationships. In contrast to other animal models and similar to the duplication that generated the supergene in Primula primroses, the synteny within the Pristionchus supergene is conserved in the entire genus, demonstrating that supergene organization can be retained over tens of millions years of evolution and multiple speciation events. However, the locus architecture is different in other dimorphic genera of the same family. Interestingly, divergence between paralogs in the supergene is counteracted by gene conversion as inferred from phylogenies and observed experimentally in the genotypes of CRISPR/Cas9-induced mutants. Thus, supergenes can control alternative phenotypes generated by plasticity or polymorphism.
