Adaptive Variation and Introgression of a CONSTANS-Like Gene in North American Red Oaks

Abstract

Oaks provide a model system to study maintenance of species identity by divergent selection since they maintain morphological differences and ecological adaptations despite interspecific hybridization. The genome of closely related interfertile oak species was shown to be largely homogeneous, with a few genomic areas exhibiting high interspecific differentiation possibly as result of strong divergent selection. Previously, a genic microsatellite was identified as under strong divergent selection, being nearly fixed on alternative alleles in the two interfertile North American red oak species: Quercus rubra L. and Quercus ellipsoidalis E.J. Hill. Further genotyping in two other red oak species-Quercus velutina Lam. and Quercus coccinea Münchh.-revealed a similar bias for the Q. ellipsoidalis-specific allele. To further elucidate the basis of this differentiation, we sequenced the microsatellite in individuals from all four red oak species. Sequence variability was observed in the microsatellite motif which encodes a poly-Q repeat in a COL gene involved in phenology and growth. Furthermore, in neighboring (parapatric) Q. rubra/Q. ellipsoidalis populations, introgression of the Q. ellipsoidalis-specific allele into Q. rubra occurred at a lower rate than introgression of the Q. rubra-specific allele into Q. ellipsoidalis despite symmetric interspecific gene flow, indicating potential adaptive introgression. Introgression of adaptive alleles can be an important mechanism for rapid adaptation to new environmental conditions (e.g., climate change).

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

“…Characterization of the outlier locus COL in neighboring (parapatric) populations of Q. rubra and Q. ellipsoidalis from three regions (Lind‐Riehl et al, 2014; Lind‐Riehl and Gailing, 2017) showed signatures of asymmetric introgression of outlier alleles; introgression of allele 141 ( Q. rubra allele) into Q. ellipsoidalis was consistently higher than introgression of allele 138 into Q. rubra (Lind‐Riehl and Gailing, 2017). In the only sympatric population of Q. rubra , Q. ellipsoidalis , and Q. velutina , an opposite pattern was observed, introgression of allele 138 into Q. rubra was higher than introgression of allele 141 into Q. ellipsoidalis .…”

“…Despite recurrent and symmetric interspecific gene flow in contact zones between both species (Lind and Gailing, 2013; Owusu et al, 2015; Lind‐Riehl and Gailing, 2017), they remain morphologically and ecologically distinct, and hybrids and introgressive forms in adult trees are relatively rare in neighboring (parapatric) populations (Lind and Gailing, 2013; Collins et al, 2015). For example, genetic assignment analyses in populations of Q. rubra and Q. ellipsoidalis in the northern range of both species, where they co‐occur as the only interfertile oak species, revealed no F 1 hybrids, 6.5% introgressive forms with Q. ellipsoidalis in Q. rubra populations, and 9.0% introgressive forms with Q. rubra in Q. ellipsoidalis populations (Lind‐Riehl and Gailing, 2017). Interspecific gene flow was also reflected in low interspecific genetic differentiation at most nuclear and genic microsatellites and sharing of regional chloroplast haplotypes between species in sympatric and parapatric populations (Lind and Gailing, 2013; Zhang et al, 2015).…”

“…The microsatellite was nearly fixed on two different alleles in both species, allele 138 in Q. ellipsoidalis and allele 141 in Q. rubra . This outlier locus with very high interspecific differentiation can be used as diagnostic marker to follow introgression of outlier alleles between species (Arnold, 2006; Lind‐Riehl and Gailing, 2017). The EST, in which FIR013 is located, was annotated as CONSTANS ‐like ( COL ) (Lind‐Riehl et al, 2014; Lind‐Riehl and Gailing, 2017), a circadian clock gene with putative function in the photoperiodic control of flowering and growth cessation (Putterill et al, 1995; Yano et al, 2000; Holefors et al, 2009; Amasino and Michaels, 2010; Lind‐Riehl et al, 2014).…”

“…This outlier locus with very high interspecific differentiation can be used as diagnostic marker to follow introgression of outlier alleles between species (Arnold, 2006; Lind‐Riehl and Gailing, 2017). The EST, in which FIR013 is located, was annotated as CONSTANS ‐like ( COL ) (Lind‐Riehl et al, 2014; Lind‐Riehl and Gailing, 2017), a circadian clock gene with putative function in the photoperiodic control of flowering and growth cessation (Putterill et al, 1995; Yano et al, 2000; Holefors et al, 2009; Amasino and Michaels, 2010; Lind‐Riehl et al, 2014). A Blast search against the NCBI Arabidopsis nucleotide database (Zhang et al, 2000) revealed the highest similarity to the Arabidopsis thaliana mRNA for the CONSTANS gene (Putterill et al, 1995) (E = 1E‐95; 67% identity, accession X94937.1), a circadian clock gene of the flowering pathway whose expression accelerates flowering in response to long days by activation of the FLOWERING LOCUS T (Suárez‐López et al, 2001; Amasino and Michaels, 2010).…”

“…Sequencing of both alleles in Q. rubra and in the drought‐tolerant clade comprising Q. ellipsoidalis , Quercus velutina Lam., and Quercus coccinea Münchh. revealed that the trinucleotide SSR in COL encodes a poly (Q) repeat (poly glutamine repeat) and that Q. ellipsoidalis and the other more drought‐tolerant species, Q. velutina and Q. coccinea , are missing one repeat unit (Lind‐Riehl and Gailing, 2017). In the European white oak species Q. petraea , a single nucleotide polymorphism (SNP) located in the same COL gene was associated with vegetative bud burst (Alberto et al, 2013), a trait directly correlated with flowering time in oaks (Chesnoiu et al, 2009; Collins et al, 2015).…”