Cis-regulation and conditional chromatin remodeling in development and evolution of ontogenies in horned beetles

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Organisms across the tree of life adjust the way they grow in response to diverse internal and external influences. The same traits may manifest differently in males compared to females, or look different depending on whether the developing organism had access to sufficient food or not. Such “conditional” or “context-responsive” development is wide-spread, and has diversified rapidly and greatly across traits and species. Past work identified many important mechanisms that regulate condition-responsive development, yet, how such differences arise in the first place, and how subsequent development interprets these differences and adjusts itself accordingly, remains very poorly understood. This research uses horned beetles as a study system to fill this void. Horned beetles possess highly diverse forms of context-responsive development that are amenable to comparative and experimental study. Through the lens of this study system this work aims to (a) characterize the genetic networks that allows the development of complex traits such as horns, wings, and legs to be both initiated and completed in response to varying conditions; as well as (b) investigate how this regulation changes from trait to trait, and from species to species, and thereby contributes to organismal diversity. This research is further integrated within multifaceted science outreach activities aimed at developing resources in support of K12 Indiana Science Teaching Standards, training K-12 teachers, and increasing the participation of historically underrepresented demographics in science. Organismal form and function emerge through the integration of genotype and environment via the agency of developmental processes. The proposed work will address the developmental mechanisms by which the horned beetle species Onthophagus integrates genotype and environment in the genesis of organismal form and function during ontogeny, and how changes in this integration shape organismal diversity both within and among this species. This research will break new ground by integrating the genome-wide analysis of chromatin accessibility and gene expression with the functional analysis of candidate genes and pathways. Further, this work will be executed in a comparative manner across traits that differ in the degree or nature of their context-responsive development, and across species that have diverged in trait-specific conditional development. The proposed work has three major objectives: first, it will identify the role of cis-regulatory architecture in environment- and male/female-specific development. Second, it will characterize how this role has diversified across taxa and traits representing varying degrees of evolutionary diversification and innovation. Finally, this research will assess the nature of interactions – as well as evolutionary changes therein – between several known master-regulators of condition-dependent development and their context-responsive gene regulatory networks in producing intraspecific morphological variation. Collectively, the proposed work aims to transform our understanding of the developmental mechanisms that integrate genotype and environment in the genesis of organismal form and function during ontogeny, and how changes in this integration shape organismal diversity both within and among species.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.