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Connecting genetic incompatibilities with natural selection on additive genetic variation during adaptive radiation

By Gregory Matthew Walter, J. David Aguirre, Melanie J Wilkinson, Thomas J Richards, Mark W Blows, Daniel Ortiz-Barrientos

Posted 16 Jan 2019
bioRxiv DOI: 10.1101/520809

Evolutionary biologists have long sought to identify the links between micro and macroevolution to better understand how biodiversity is created. Despite this pursuit, it remains a challenge to understand how allele frequency changes correlate with the evolution of morphological diversity, and the build-up of reproductive isolation amongst taxa. To connect mechanisms of microevolution with patterns of diversification, we tested the adaptive importance of alleles underlying genetic incompatibilities, and the consequences for predicting evolutionary trajectories of multiple ecotypes of an Australian wildflower. Using a quantitative genetics crossing design, we produced an F4 generation Advanced Recombinant Form (ARF) between four contrasting ecotypes, which we phenotyped in the glasshouse (N=770) and transplanted into the four natural habitats (N=14,265 seeds), alongside the parental ecotypes. F2 hybrid breakdown was associated with the loss of extreme phenotypes and habitat-specific genetic variation in field performance. Genetic trade-offs existed among habitats, but only in axes describing smaller amounts of genetic variance for fitness. Habitats that showed stronger patterns of adaptive divergence for native versus foreign ecotypes, also showed lower genetic variance in fitness of the ARF. Integrating data from the field and glasshouse predicted patterns of selection on morphological traits in a similar direction to the parental ecotypes. Overall, our results provide strong empirical evidence linking ecotype specific alleles with phenotypic divergence, fitness trade-offs, rapid adaptation and the accumulation of genetic incompatibilities among recently derived ecotypes. Our data connects microevolutionary change with macroevolution through adaptive radiation, where selection for environment specific alleles creates rapid adaptive divergence leading to speciation.

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