Evidence for environment-dependent introgression of adaptive genes between two red oak species with different drought adaptations.

Abstract

Introgression of adaptive alleles between hybridizing species is likely an important mechanism to generate new genetic variation for adaptation to rapidly changing environmental conditions. Oaks provide a model for the study of adaptive gene introgression because environmental selection maintains high interspecific differentiation at a few outlier loci and species-specific adaptations despite recurrent interspecific gene flow. Previously, we identified a CONSTANS-like gene under strong divergent selection between drought-tolerant Quercus ellipsoidalis and drought-averse Quercus rubra. Neighboring (parapatric) populations of both species were fixed for alternate alleles, Q. ellipsoidalis for allele 138 and Q. rubra for allele 141. In this study, we analyzed introgression of these outlier alleles in sympatric and in parapatric Q. rubra/Q. ellipsoidalis populations. We found evidence that environmental selection affected the level and direction of outlier allele introgression. Thus, in the face of symmetric interspecific gene flow, outlier allele introgression was asymmetric and introgression of allele 138 into Q. rubra was consistently higher than introgression of allele 141 into Q. ellipsoidalis in sympatric populations, but the opposite pattern was found in parapatric populations. Furthermore, the rate of introgression of outlier alleles between species in sympatric stands was related to soil quality (i.e., soil water holding capacity, nutrient availability). This pattern suggests that introgression of adaptive genes between these two red oak species is strongly affected by environmental selection and is an important mechanism for species' adaptation to changing environmental conditions in a changing climate.