Macrosystem community assembly patterns are predicted by foundation tree species genetic connectivity and environment across the American Southwest

Bothwell, H. M.; Keith, A. R.; Hull, J. B.; Cooper, H. F.; Andrews, L. V.; Wehenkel, C.; Hultine, K. R.; Gehring, C. A.; Cushman, S. A.; Whitham, T. G.; Allan, G. J.

doi:10.1101/2021.06.24.449837

bioRxiv · 10.1101/2021.06.24.449837

Macrosystem community assembly patterns are predicted by foundation tree species genetic connectivity and environment across the American Southwest

Bothwell, H. M.·Keith, A. R.·Hull, J. B.·Cooper, H. F.·Andrews, L. V.·Wehenkel, C.·Hultine, K. R.·Gehring, C. A.·Cushman, S. A.·Whitham, T. G.·Allan, G. J.

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Abstract

Macrosystems ecology is an emerging science that aims to integrate traditionally distinct disciplines to predict how hierarchical interacting processes influence the emergence of complex patterns across local to regional and global scales. Despite increased focus on cross-scale relationships and cross-disciplinary integration, few macroecology studies incorporate genetic-based processes. Here we used a community genetics approach to investigate the pattern-process relationships underlying the emergence of macroscale biodiversity patterns. We tested the hypothesis that environmental variation, geography, and genetic connectivity in a foundation tree species differentially predict associated community assembly patterns from local to continental scales. Using genome-wide SNP data, we assessed genetic connectivity as a function of genetic similarity and structure in Fremont cottonwood (Populus fremontii) across its distribution throughout the southwestern US and Mexico. For the same trees, we measured community composition, diversity, and abundance of leaf modifying arthropods and sequenced targeted amplicons of twig fungal endophytes. Five key findings emerged. (1) We identified three primary and six secondary population genetic groups within P. fremontii, which occupy distinct climate niches. (2) Both the leaf modifying arthropod and fungal endophyte communities were significantly differentiated across host tree ecotypes, with genetic distance among sampling locations explaining 13-17% of respective macroscale community structure. (3) For arthropods, environmental distance was the strongest driver of community similarity. (4) Conversely, host genetic connectivity was the most important contributor to macroscale endophyte community structure, with no significant contribution of environmental distance. (5) Furthermore, we observed a shift in the strength of interspecific relationships, with host genetics most strongly influencing associated communities at the intermediate population scale. Our findings suggest that genetic connectivity and environmental variation play integrated roles in macroscale community assembly, and their relative importance changes with scale. Thus, conservation genetic management of the diversity harbored within foundation species is vital for sustaining associated regional biodiversity.

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Bothwell, H. M., Keith, A. R., Hull, J. B., Cooper, H. F., Andrews, L. V., Wehenkel, C., Hultine, K. R., Gehring, C. A., Cushman, S. A., Whitham, T. G., Allan, G. J.. 2021-06-25. Macrosystem community assembly patterns are predicted by foundation tree species genetic connectivity and environment across the American Southwest. https://doi.org/10.1101/2021.06.24.449837

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