Collaborative Research: Cognitive deficiency as a source of reproductive isolation between hybridizing species

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When different species breed with each other, or hybridize, the two original species can lose their distinctiveness unless hybrids become disadvantaged and less fit than their parents. Most research into hybrid disadvantage has focused on hybrid sterility or embryonic developmental problems. However, reductions in cognitive abilities such as learning and memory could also cause disadvantages for hybrids. Learning and memory are important for many species, but whether deficits in hybrids' learning and memory can function in keeping species separate is unknown. This collaborative project will evaluate the possibility that learning and memory deficiencies maintain the species boundary between hybridizing chickadee species. This work will fill an important void in our understanding of the development and maintenance of species, a fundamental evolutionary process. It will inspire new avenues of research in evolution, behavior, and neuroscience. The research also has important implications for the conservation of biodiversity. With this project, the researchers will train postdoctoral and graduate students. Additionally, underrepresented undergraduate students will gain integrative training in research and science communication. Students involved in mentored research at each institution during the academic year will work on a different aspect of the project at one of the other involved institutions during the summer. As a part of the summer experience, the students will collaborate with the Bird Academy at the Cornell Lab of Ornithology to develop a high-traffic online module on bird hybridization. They will therefore learn to employ diverse research approaches to address a common question, and to communicate science to the public. How learning and memory function in hybrids is relatively unexplored. These traits have been shaped by natural selection, but their role in the maintenance of species boundaries is unknown. The overall objective of the proposed research is to integrate behavior with neuroanatomy and genomics to evaluate the potential for hybrid deficiencies in cognitive ability to contribute to postzygotic reproductive isolation. Using naturally-hybridizing black-capped and Carolina chickadees, the proposed research will test the central hypothesis that selection acts against hybrids deficient in memory and learning, and that these deficiencies are reflected in neuroanatomic and genomic variation. This system is well suited for testing the role of cognition in postzygotic reproductive isolation because learning and memory are important for fitness in both species. Preliminary data suggest that hybrid chickadees have deficient memories and small hippocampal neurons, and that genes linked to learning and memory are involved in reproductive isolation. The research team will address the central hypothesis in an eastern Pennsylvania hybrid zone transect. With behavioral tests of learning and memory, comparative neuroanatomy, RNA sequencing, and whole-genome resequencing, the research will: 1) determine the relative learning and memory abilities of black-capped, Carolina, and hybrid chickadees; 2) quantify neuroanatomic differences between hybrid and parental-species chickadees; and 3) identify signatures of reproductive isolation and misexpression in genes underlying cognition. Through the completion and integration of these aims, this research will connect cognition with speciation in the first test of hybrid learning and memory deficiency as a postzygotic reproductive isolating barrier.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.