EDGE CMT: Origin and diversification of butterfly color patterns

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When we look across the diversity of life, we see many complex traits that are unique to certain groups of organisms. Feathers in birds, hair in mammals, and flowers in angiosperms, for example. It is a major question in biology how these kinds of novel traits first appear. What is the genetic basis of newness? Recent work across many species has shown that novel traits such as these are largely generated by old genes that have been repurposed for new roles. Novelty appears to emerge through a reshuffling of older genetic building blocks, which are proposed to be ancient subnetworks of interacting genes. But where do these gene networks come from in the first place? And how are they rewired to generate complex new traits? With this funding, Reed and colleagues are beginning to address these questions by looking at the origin of color in butterflies. They are characterizing the gene networks that underlie color pigmentation in butterflies, and they are determining how specific genetic changes caused these networks to be repurposed from ancestral roles in processes such as neural development, to make butterfly wing patterns. This work serves as a case study to help biologists understand the developmental genetic mechanisms that underlie the genesis and diversification of complex biological traits. The project also includes training in biology research skills of graduate and undergraduate students from diverse backgrounds, the development and dissemination of instructional videos for genomic methods, and the establishment of a web-based resource for functional genomics in butterflies.A core concept in modern biology is that novel morphological traits originate from gene regulatory networks that predate the traits themselves. Surprisingly, however, little is known about the specific genetic mechanisms that underlie the origin and repurposing of such gene networks. With this funding, Reed and colleagues develop the regulatory network encompassing the butterfly color pattern gene optix into a model for exploring the regulatory architecture of trait diversification. optix is a homeobox transcription factor that plays a deeply ancestral role in neural and retinal development in both invertebrates and vertebrates. In butterflies, however, this gene underwent a radical co-option event where it gained a novel function as a master regulator of wing pigmentation, including playing key roles in adaptation and mimicry. Thus, the researchers have a situation in Lepidoptera where they can pinpoint the phylogenetic timing of a major optix co-option and repurposing event, where this gene appeared as a de novo regulator of color patterns. Reed and colleagues are leveraging this opportunity to take a multi-species comparative approach to characterize the history of the optix regulatory network as it gained its novel adaptive function in color pattern regulation. Using optix as the focal point, they are characterizing the cis-, upstream, and downstream regulatory dynamics of regulatory co-option, and construct a comprehensive case study of how a new gene regulatory network can emerge from the genome to generate new morphological features – in this case, color itself.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.