Collaborative Research: cis-Regulatory architecture of color pattern convergence

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Understanding the origin and maintenance of biological diversity requires connecting patterns of genetic variation at the molecular level with morphological differences among individuals, populations, or species. Over the last decade, many examples of adaptive trait variation have been linked to developmental changes in gene expression. Regions of the genome that lie in between genes contain “regulatory elements” that regulate spatial and temporal patterns of gene expression. These regulatory regions are thought to play an essential role in trait adaptation. However, our understanding of the specific mechanisms through which regulatory elements have driven morphological diversification remains limited. Do changes involve a small number of elements with large effect, or many elements of minor effect? Do new gene expression patterns appear via origination of new elements, or changes in older ancestral elements? How do the functions of individual elements change? To what extent might some elements facilitate the convergence of traits across different linages? This project aims to address these questions. In doing so, it will decode some of the rules governing the structure, function, and evolution of regulatory elements. Specifically, the investigators will couple comparative biology with mechanistic studies of regulatory elements to understand the regulatory basis of repeated color pattern evolution in butterflies. The work will include public engagement at the Boston Science Museum. In addition, the work will develop strategies for increasing the recruitment of graduate students from historically underrepresented groups. Cis-regulatory elements (CREs) include promotors, enhancers, and silencers. These elements play an essential role in phenotypic evolution because they regulate patterns of gene expression during development. Despite recent progress in identifying and characterizing CREs responsible for adaptive trait variation, many questions remain. For example, what is the relationship between sequence divergence, the genomic architecture of transcription factor binding sites within CREs, and CRE function? Addressing these questions is complicated. CREs have been hypothesized to act as relatively independent modules controlling tissue-specific expression. However, growing evidence indicates that CRE mutations may have multiple downstream effects. Here, we propose to use the power of repeated evolution within a comparative framework to decode the rules governing CRE structure, function, and evolution. Our research addresses three primary questions. First, how is population-level sequence divergence responsible for wing pattern mimicry related to chromatin accessibility and patterns of gene expression in Limenitis butterflies? Second, to what extent does deep regulatory homology underlie repeated cases of convergent evolution across different phylogenetic timescales? Third, how do deeply ancestral vs. recently derived CREs contribute to color pattern evolution and convergence? We will answer these questions by identifying and functionally characterizing CREs controlling the expression of two genes, WntA and optix. These genes have been shown to underlie adaptive mimetic color pattern divergence within and between butterfly species. We will then leverage the widespread occurrence of convergent evolution across three butterfly genera to study broad-scale evolutionary patterns of CRE gain and loss. Ultimately, our results will shed light on how cis-regulatory elements arise, how they function to determine phenotype, and what rules govern their evolution.This project is co-funded by the Genetic Mechanisms program of the Molecular and Cellular Biosciences Division in the Biological Sciences Directorate.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.