Evidence for selection on a CONSTANS-like gene between two red oak species

Abstract

Background and aims: Hybridizing species such as oaks may provide a model to study the role of selection in speciation with gene flow. Discrete species' identities and different adaptations are maintained among closely related oak species despite recurrent gene flow. This is probably due to ecologically mediated selection at a few key genes or genomic regions. Neutrality tests can be applied to identify so-called outlier loci, which demonstrate locus-specific signatures of divergent selection and are candidate genes for further study.

Methods: Thirty-six genic microsatellite markers, some with putative functions in flowering time and drought tolerance, and eight non-genic microsatellite markers were screened in two population pairs (n = 160) of the interfertile species Quercus rubra and Q. ellipsoidalis, which are characterized by contrasting adaptations to drought. Putative outliers were then tested in additional population pairs from two different geographic regions (n = 159) to support further their potential role in adaptive divergence.

Key results: A marker located in the coding sequence of a putative CONSTANS-like (COL) gene was repeatedly identified as under strong divergent selection across all three geographically disjunct population pairs. COL genes are involved in the photoperiodic control of growth and development and are implicated in the regulation of flowering time.

Conclusions: The location of the polymorphism in the Quercus COL gene and given the potential role of COL genes in adaptive divergence and reproductive isolation makes this a promising candidate speciation gene. Further investigation of the phenological characteristics of both species and flowering time pathway genes is suggested in order to elucidate the importance of phenology genes for the maintenance of species integrity. Next-generation sequencing in multiple population pairs in combination with high-density genetic linkage maps could reveal the genome-wide distribution of outlier genes and their potential role in reproductive isolation between these species.

Keywords: CONSTANS-like genes; Q. ellipsoidalis; Quercus rubra; divergent selection; ecological speciation; flowering time; red oak; speciation genes.

Fig. 1.

Sampling locations. Soil data are from Soil Survey Staff, Natural Resources Conservation Service, United States Department of Agriculture. Soil Survey Geographic (SSURGO) Database. Available online at http://soildatamart.nrcs.usda.gov. Accessed 6 January 2013. In the case of FC-A, the data were modified slightly to match field soil samples (data not shown).

Fig. 2.

Unrooted tree (UPGMA method) based on genetic distance (F_ST) at 20 markers; numbers at nodes are percentages over 1000 bootstrap replicates using Populations 2·0 (Langella, 1999).

Fig. 3.

Outlier loci analysis of 44 markers between species among all four FC/Baraga Plains populations as calculated by LOSITAN (Antao et al., 2008). Outliers are indicated by a star while all others are circles, and black lines represent the 5 % quantiles, with markers outside the lower 5 % quantile under balancing selection and the markers outside the upper 5 % quantile under divergent selection, while the grey line represents the median (50 %).

Fig. 4.

Allele frequency distribution of each species in the (A) FC/Baraga Plains populations, (B) CNF populations and (C) NNF populations for EST-SSR FIR013 (CONSTANS-like 1).