Collaborative Proposal: Linking process to pattern through an experimental network approach to identify the behavioral mechanisms of reproductive isolation

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Animals frequently interact with members of their own and closely related species in non-random ways that have profound implications for evolution within and between populations, including the buildup or breakdown of genetic differences. Closely related subspecies often come into contact and interbreed, or, hybridize. This research will experimentally study how social interactions (networks), morphological traits, genomic ancestry, and migratory behavior explain the amount of interbreeding in two contact zones each consisting of two pairs of barn swallow subspecies that differ in degree of hybridization. The integration of observation and experiments in the wild with genomic analyses will allow for a direct test of how individual behaviors impact hybridization. The research uses miniaturized proximity loggers and network analytical methods to measure the frequency of interactions between individual swallows. Data collection will be accomplished through extensive student training and international collaboration. The use, visualization, and interpretation of social networks will be broadly disseminated through 1) conference presentations, workshops, and publications, 2) integrated into courses, 3) public release of code for new network analysis methods and 4) online dynamic interactive visualizations of research data with exercises and assessment tools. This work represents a highly novel and integrative approach to understanding how closely related populations evolve into different species, with important implications for biodiversity and conservation studies.Assortative behaviors (non-random social interactions) are thought to represent critical barriers to gene flow among recently diverged animal taxa. However, direct measurement of assortative behavior in nature is rarely possible. This research leverages the barn swallow (Hirundo rustica) subspecies complex to experimentally examine the contribution of assortative behavior to reproductive isolation in two hybrid zones between subspecies pairs that differ in evolutionary history. The following will be collected from each hybrid zone: 1) close-range social interactions from proximity tags to construct social networks, 2) fine-scale genomic information to measure individual ancestry, 3) wintering locations, migratory routes and timing of arrival data from geolocators and stable isotopes, 4) measures of morphological variation, and 5) data for molecular paternity analyses to construct fertilization networks based on within- and extra-pair matings as a direct measure of hybridization between subspecies. The construction of fertilization networks will enable analyses about the degree to which hybridization is mediated by social interactions, subspecific ancestry, migratory behavior, or morphology. These features are likely correlated with one another and their combined and relative importance in reproductive isolation will be analyzed using matrix regression methods. After collecting correlative data from each hybrid zone, experimental manipulations of phenotype and timing of breeding will be conducted to test for causal relationships between these traits and fertilizations, providing an extremely rare opportunity to experimentally test and manipulate predictors of hybridization. These comparisons offer the previously intractable opportunity to experimentally analyze how individual-level variation predicts reproductive decisions and the degree to which populations hybridize.This award was co-funded by Behavioral Systems in the Division of Integrative Organismal Systems and Evolutionary Processes in the Division of Environmental Biology.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.