Sharing of chloroplast haplotypes among red oak species suggests interspecific gene flow between neighboring populations

Abstract

The North American red oak species Quercus rubra L., Quercus ellipsoidalis E. J. Hill, Quercus velutina Lam., and Quercus coccinea Münchh. are morphologically similar and showed very low interspecific differentiation at most nuclear genetic markers in our earlier analyses (<10%). However, a few genetic markers showed interspecific differentiation values (up to 84%) above neutral expectations, a pattern of genomic divergence consistent with models of ecological speciation in the face of gene flow and strong divergent selection. Accordingly, these interfertile species are predicted to maintain differential adaptations to drought, while neutral regions of the genome appear to be homogenized by interspecific gene flow. According to this model of maintenance of species integrity by divergent selection with gene flow, we expect a sharing of chloroplast haplotypes between interspecific population pairs. We analyzed maternally inherited chloroplast DNA markers for the first time in interspecific populations of the red oaks (section Lobatae) to provide additional evidence for contemporary gene flow between Q. rubra and Q. ellipsoidalis and between Q. velutina and Q. ellipsoidalis. Very low interspecific differentiation (GST= 0.023), but pronounced genetic differentiation among populations from different regions (GST= 0.277) across species, and sharing of regional chloroplast haplotypes between species in sympatric and neighboring populations provided strong evidence for contemporary interspecific gene flow. The pattern of divergence at chloroplast DNA markers in red oaks suggests interspecific gene flow that resulted in a sharing of chloroplast types while the ecological and morphological distinctness of species was maintained.