Collaborative Research: RoL: The evo-devo of male pregnancy and its effects on the brood pouch microbiome

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The evolution of novel traits can change the way that organisms interact with their environments to survive, grow and reproduce. Deep knowledge of the underlying genes and developmental changes that underly most evolutionary innovations is sparse, as is understanding of the ecological consequences for both the organisms in which novel traits emerged and the organisms with which they interact in communities. A particular gap in understanding is how the evolution of novel traits influences the biodiversity of their associated microbial communities. This project will help fill this gap in our knowledge by studying a remarkable innovation – male pregnancy in seahorses, pipefish and seadragons. This project will include the creation of new genome sequences and detailed studies of the developmental genetic underpinnings of the embryo brooding structures that make male pregnancy possible. The consequences of pouch evolution on the complexity and function of the community microbes in the pouch will also be studied, as well as how this unique host-associated microbiota can affect the fitness of embryos in the pouch. This project will provide research training to high school students, teachers, and undergraduates from underrepresented groups through immersive outreach and targeted support programs. The project will also support training of the next generation of scientists via education of Ph.D. students and postdoctoral scholars. Outreach to general public will be accomplished through public talks and through creation of a museum exhibit on syngnathid biology paired with web resources to support K-12 education.Male pregnancy, accompanied by morphologically diverse embryo brooding structures, is a defining evolutionary innovation in syngnathid fishes. The goal of this project is to build an integrative understanding of the developmental genetic origin of this remarkable syngnathid novelty and its role in mediating multi-level ecological interactions with host-associated microbiota. This project will include production of 19 new annotated reference genomes strategically sampled across the syngnathid lineage, morphogenetic analysis and transcriptional/epigenetic profiling of the developing pouch in a comparative framework that leverages the repeated, independent evolution of complex brooding structures in the family, and analysis of brood pouch biocomplexity as a determinant of pouch-associated microbiome assembly. When complete, this project will provide novel insights into genome structural evolution in syngnathids, identify protein sequence and gene regulation changes involved in brood pouch development, and address whether the evolution of the brooding tissues created specialization in host regulation of microbiota with consequences for brooded progeny. The work will attract new researchers to syngnathids for studies of evolutionary innovation and diversification. The project will provide research training to high school students, teachers, and undergraduates from underrepresented groups, and will support education of graduate students and postdoctoral scholars, including the opportunity to take intense short courses to learn next generation sequencing, bioinformatics, complex statistical analyses, and genome editing. Educational outreach to general public will be accomplished through public lectures by the PIs, and through creation of a museum exhibit on syngnathid biology, which will be paired with an associated web resource directed toward K-12 education.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.