Long-distance dispersal drives the genetic variation and historical demography of Quercus magnoliifolia and Quercus resinosa (Fagaceae) in the Mexican highlands

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Abstract While hybridization and introgression can have a strong adaptive importance, it can impede divergence of species. Quercus magnoliifolia and Q. resinosa are two endemic oak species distributed across the Mexican highlands. These species diverged ecological and morphologically; however, no nuclear genetic differentiation is evident. In this study, we determined the mechanisms that shape patterns of genetic variation and establish the role of migration and hybridization in the evolutionary history of these two oak species. To do this, Bayesian approaches were used for inference on migration rates and directionality and timing of divergence between species using chloroplast microsatellites. We then integrated species distribution models to infer the geographic distribution of Q. magnoliifolia and Q. resinosa during Last Interglacial, Last Glacial Maximum, and Mid-Holocene time frames. We failed in distinguishing a unique genetic composition for each species. Chloroplast differentiation was more congruent with geography than the taxonomic status of each species. Our study revealed that after the divergence (c. 10 Mya) of these two oak species, high rates of introgression took place at the end of the Pleistocene. Furthermore, past distribution models predicted that Q. magnoliifolia and Q. resinosa have likely been in sympatry presumable since Last Glacial Maximum and Q. resinosa probably expanded geographically towards its current distribution around Mid-Holocene. This expansion was supported by testing migration models, suggesting recent establishment of Q. resinosa to the north of Trans-Mexican Volcanic Belt. We hypothesized that after Q. magnoliifolia and Q. resinosa diverged, colonization events followed by hybridization between oaks and long-distance seed dispersal occurred, explaining the present-day patterns of distribution of chloroplast diversity. We propose that divergence of species remains mainly on loci under natural selection, providing evidence on the “porous” nature of species boundaries among oaks.

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