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Mosaic genetic differentiation along environmental and geographic gradients indicate divergent selection in a white pine species complex

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Abstract

We explored the role of isolation by environment in a white pine species complex: Pinus flexilis, Pinus strobiformis and Pinus ayacahuite distributed from Canada to Central America. We predict that species differentiation would match genetic structure of candidate genes associated with significant differences in climatic niche in the species complex. To test this prediction, we sequenced five candidate genes for drought tolerance and three housekeeping genes, in individuals from across the entire range of each species. We performed neutrality tests, estimated genetic differentiation and performed partial mantel correlations, to test for isolation by environment in the species complex. Our results show that different loci vary in degrees of genetic differentiation within species and contrast in patterns of differentiation among species. This is considered to be a mosaic pattern of genetic differentiation. There was also significant isolation by environment in candidate genes. P. flexilis was genetically differentiated for candidate genes and P. ayacahuite for housekeeping genes. There was also an overall pattern of shared ancestral polymorphism followed by independent evolution. Nonetheless, all loci together recovered groups that correspond to the recognized taxonomy. In conclusion, the pattern of isolation by environment in candidate genes support the idea of ecologically driven differentiation of this species complex, especially in the case of P. flexilis. The observed difference in housekeeping genes between P. strobiformis and P. ayacahuite can be due to limited gene flow. The mosaic pattern of differentiation suggests that speciation is recent and ecological differences could be a factor in the diversification of pines in North America.

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Acknowledgments

We thank D. Piñero, A. Vázquez-Lobo, R. Salas-Lizana, D. Gernandt, L. Jardón-Barbolla, A. Ortíz-Medrano, J.P. Jaramillo-Correa, A. Mastretta-Yanes, I. Eyres and A.M. Humphreys, for their insights on conifer evolution and speciation. Thanks to S. González-Martínez, D. Grivet for sharing their knowledge on drought tolerance genes, and to M. Powell and V. Savolainen for laboratory facilities. Thanks to A. Aswad, I. Eyres, and C.Q. Tang for their help in the molecular work. Thanks to G. Bradburd for his assistance with BEDASSLE, J.A. Endler and the anonymous reviewers for the comments that helped improve the manuscript. This research was funded by a CONACYT’s Mexican Postdoctoral Fellowship (No. 149841) awarded to A.M.-L. A.M.-L. conceived the ideas, collected and analysed the data. A.M.-L. and T.G.B. wrote the manuscript.

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  1. Alejandra Moreno-Letelier

    Present address: Jardín Botánico, Instituto de Biología, Universidad Nacional Autónoma de México, Circuito exterior s/n, Ciudad Universitaria, 04510, Mexico, DF, Mexico

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  1. Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire, SL5 7PY, UK

    Alejandra Moreno-Letelier & Timothy G. Barraclough

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Moreno-Letelier, A., Barraclough, T.G. Mosaic genetic differentiation along environmental and geographic gradients indicate divergent selection in a white pine species complex. Evol Ecol 29, 733–748 (2015). https://doi.org/10.1007/s10682-015-9785-4

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