Collaborative Research: RoL: The intersection between cell fate decisions and phenotypic diversification in a rapidly radiating butterfly lineage

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Animal structures are made of combinations and arrangements of distinct cell types, the product of complex cell decision-making during development. But how do cells, which contain identical genetic information, decide their fate? This research addresses this fundamental biological question in a simple, yet spectacularly diverse animal structure–the color patterns on the wings of Heliconius butterflies. Although Heliconius wing patterns are highly diverse, they are created by altering the distribution of just three cell types (red, black and yellow wing scales) across the wing surface. Unlike in a complex organ, the cell decisions that create these patterns unfold on a flat canvas of non-migrating cells. This attribute greatly simplifies the process of understanding the interactions among genes and how these interactions change throughout development to create a specific pattern. This research capitalizes on this fact and emerging genomic tools to characterize the molecular decisions that determine how a developing wing cell becomes specified into one of the three different scale cell types. The project is strengthened by a 6-month internship program that targets traditionally underrepresented groups and offers an in-depth research experience and hands-on professional development. Moreover, through partnerships with science museums, this project will create bilingual (English and Spanish) experiential learning resources that harness the potential of butterflies to educate a variety of audiences (school children, teachers, and life-long learners) about genes, development, natural selection, and the role that interactions among them play in generating Earth’s biodiversity.Evolutionary processes constantly generate and rearrange specialized cell types, forging the morphological dimension of biodiversity. Research is starting to connect changes in gene expression and open chromatin to cell fate decisions. However, this research has mostly focused on early embryonic development or on the developmental trajectories of complex organs in a few species. Although powerful, these studies do not have an explicit goal of linking changes in cell fate decisions to phenotypic change. This research fills this important knowledge gap by characterizing the rules governing cell specification– from signals, to reception, transduction, transcriptional activation, and fate determination during the critical developmental period when the wing patterns of Heliconius butterflies are established. Here, extensive knowledge of the ecological and evolutionary significance of wing color patterns, experimental tractability, and fantastic diversity make Heliconius a powerful experimental system for understanding how the processes of cell specification are modified by natural selection to produce diversity. By casting single-cell transcriptomics, open chromatin profiling and CRISPR loss-of-function experiments within an evolutionary framework that includes replicated cases of the independent evolution of identical wing patterns, this project will determine the rules that govern how cells communicate and acquire a specialized fate during development, and how those rules are applied to generate diversity.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.