Ebony underpins Batesian mimicry in an insect melanic polymorphism

The evolution of Batesian mimicry - whereby harmless species avoid predation through their resemblance to harmful species - has long intrigued biologists. In rare cases, such mimicry systems can be highly dynamic, being maintained via frequency-dependent selection on intraspecific polymorphisms, in which only some individuals within a population resemble a noxious model. Here, we use genomic approaches to identify the genetic basis of a striking mimicry polymorphism within a widespread New Zealand stonefly complex. Specifically, highly melanised specimens of Zelandoperla closely resemble an aposematic stonefly (Austroperla cyrene) well-known for its production of hydrogen cyanide. We assess convergence in the colour pattern of these two species, compare their relative palatability to predators, and use genome-wide association mapping to elucidate the genetic basis of this mimicry polymorphism. Our analysis reveals that melanised Zelandoperla overlap significantly with Austroperla in colour space, but are significantly more palatable to predators, indicating that they are indeed Batesian mimics. Analysis of 194,773 genome-wide SNPs reveals a strong outlier locus (ebony) differentiating melanic (mimic) versus non-melanic phenotypes. As ebony has a well-documented role in insect melanin biosynthesis, our findings highlight its conserved function across deeply divergent hexapod lineages. Distributional records suggest a link between the occurrence of Zelandoperla mimics and forested ecosystems where the model Austroperla is abundant, suggesting the potential for adaptive shifts in this system underpinned by environmental change.