The genomics of adaptive colouration in Hypolimnas butterflies and the wood tiger moth, Arctia plantaginis

Wing phenotypes in butterflies and moths are a striking example of adaptive evolution and are a tractable trait to dissect the genetic mechanisms underlying adaptations. Studies of Lepidoptera, mainly mimetic species from the tropics, have led to two general patterns. First, a limited set of genes have been re-used multiple times in controlling the evolution of wing phenotypes, and second, structural variation often underlies such traits. Clarifying the generality of these two patterns requires the dissection of the genetic architecture of wing phenotypes in a wider variety of species. In this thesis, I explore the genetic basis of wing mimicry in Hypolimnas butterflies and of aposematism in the wood tiger moth using a range of genomics and transcriptomics methods. First, I produce genome assemblies of two Hypolimnas species and investigate the evolution of W chromosomes in Lepidoptera. By comparing the H. misippus genome assembly to multiple Lepidoptera species, I provide evidence that suggests that the W chromosome has a shared origin across the Lepidoptera. Second, I identify the genetic basis of forewing mimicry in H. misippus using a dataset of 335 individuals sequenced using haplotagging, a linked read sequencing technique. To analyse these data, I develop a method called Wrath for the visualisation and exploration of candidate structural variants. I find that transposable element insertions are associated with forewing phenotype and present evidence for the usefulness of Wrath to explore haplotagging data. Third, I examine the evolution of mimicry in the Hypolimnas genus by identifying and comparing the genetic basis of wing phenotypes in H. misippus and H. bolina. Using a dataset of 214 whole genome sequences of H. bolina individuals together with my H. misippus data, I show that cortex, a gene involved in wing colour in many Lepidoptera, is the most likely candidate for the control of white colour elements in the two species. Furthermore, I present evidence that the regulatory elements controlling the presence of hindwing white are likely not homologous between the two species. Additionally, I show that a region close to optix, another well-known colour gene, is associated with orange elements in H. bolina. Finally, I explore the genetic basis of a complex phenotype involving aposematism and behavioural and physiological traits in the wood tiger moth, Arctia plantaginis, and show that this trait is associated with the duplication of a yellow family gene. This work contributes to our understanding of the evolution of wing phenotypes in the Lepidoptera. Overall, my results highlight the importance of structural variation in the evolution of wing colouration while also emphasising the repeatability of the genetic basis of adaptive traits.

NERC; St John's College; The Cambridge Trust