Climatic adaptation and ecological divergence between two closely related pine species in Southeast China

Abstract

Climate is one of the most important drivers for adaptive evolution in forest trees. Climatic selection contributes greatly to local adaptation and intraspecific differentiation, but this kind of selection could also have promoted interspecific divergence through ecological speciation. To test this hypothesis, we examined intra- and interspecific genetic variation at 25 climate-related candidate genes and 12 reference loci in two closely related pine species, Pinus massoniana Lamb. and Pinus hwangshanensis Hisa, using population genetic and landscape genetic approaches. These two species occur in Southeast China but have contrasting ecological preferences in terms of several environmental variables, notably altitude, although hybrids form where their distributions overlap. One or more robust tests detected signals of recent and/or ancient selection at two-thirds (17) of the 25 candidate genes, at varying evolutionary timescales, but only three of the 12 reference loci. The signals of recent selection were species specific, but signals of ancient selection were mostly shared by the two species likely because of the shared evolutionary history. FST outlier analysis identified six SNPs in five climate-related candidate genes under divergent selection between the two species. In addition, a total of 24 candidate SNPs representing nine candidate genes showed significant correlation with altitudinal divergence in the two species based on the covariance matrix of population history derived from reference SNPs. Genetic differentiation between these two species was higher at the candidate genes than at the reference loci. Moreover, analysis using the isolation-with-migration model indicated that gene flow between the species has been more restricted for climate-related candidate genes than the reference loci, in both directions. Taken together, our results suggest that species-specific and divergent climatic selection at the candidate genes might have counteracted interspecific gene flow and played a key role in the ecological divergence of these two closely related pine species.

Effects of Geological and Environmental Events on the Diversity and Genetic Divergence of Four Closely Related Pines: Pinus koraiensis, P. armandii, P. griffithii, and P. pumila

“…Mountain uplift and past environmental oscillations may have been largely responsible for shaping the spatial patterns of diversity and genetic divergence among species (Coyne and Orr, 2004; Wachowiak et al, 2009). In general, the level and distribution of nucleotide diversity are historical products of the long-term evolution of a species, and they are largely associated with the evolutionary potential or future fate of a species (Wright and Gaut, 2005; Wachowiak et al, 2009; Zhou et al, 2014; Tsuda et al, 2017). In addition, ecological or proximal causes (e.g., mating systems) and various barriers (e.g., geographic and spatio-temporal isolation) due to geological history can cause fragmented of species distributions, which may lead to reduced gene flow between isolated populations and adaptability.…”

“…They are mainly characterized by long life cycles, large effective population sizes, incomplete lineage sorting, and extensive introgression/hybridization among populations, which makes their genetic structure and spatial patterns of diversity very different from those found in traditional model plants (Neale and Kremer, 2011; Gao et al, 2012; Li et al, 2012, 2013; Hao et al, 2015). For instance, conifers tend to share haplotypes/genotypes among species, with no distinct genetic divergence across species ranges, and most of the genetic variations are found within populations (Willyard et al, 2009; Chen et al, 2010; Ren et al, 2012; Liu et al, 2014; Zhou et al, 2014). In recent years, many studies have determined nucleotide polymorphisms and speciation history patterns using multiple nuclear loci (Ma et al, 2006; Li et al, 2010; Gao et al, 2012; Wachowiak et al, 2013; Zhou et al, 2014; Zou et al, 2016).…”

“…For instance, conifers tend to share haplotypes/genotypes among species, with no distinct genetic divergence across species ranges, and most of the genetic variations are found within populations (Willyard et al, 2009; Chen et al, 2010; Ren et al, 2012; Liu et al, 2014; Zhou et al, 2014). In recent years, many studies have determined nucleotide polymorphisms and speciation history patterns using multiple nuclear loci (Ma et al, 2006; Li et al, 2010; Gao et al, 2012; Wachowiak et al, 2013; Zhou et al, 2014; Zou et al, 2016). These biparentally inherited nuclear genes are functional genes that encode proteins and they are characterized by their orthology, moderate to high rates of evolution, and the presence of many phylogenetically informative sites (Zhou et al, 2014).…”

“…In recent years, many studies have determined nucleotide polymorphisms and speciation history patterns using multiple nuclear loci (Ma et al, 2006; Li et al, 2010; Gao et al, 2012; Wachowiak et al, 2013; Zhou et al, 2014; Zou et al, 2016). These biparentally inherited nuclear genes are functional genes that encode proteins and they are characterized by their orthology, moderate to high rates of evolution, and the presence of many phylogenetically informative sites (Zhou et al, 2014). Therefore, large numbers of nuclear markers can be used to detect the deep evolutionary relationships among closely related species, especially recently diverged taxa (Chen et al, 2010; Zou et al, 2016).…”

Analysis of Correlations Between Climate and Molecular Adaptive Evolution of Wild Barley with Geographical Information Systems (GIS)

“…Yongfeng Zhou et al used two closely related pine species growing in southeastern Chinese, Pinus massoniana Lamb and Pinus hwangshanensis Hisa as materials, to analyse 25 climate related genes.They found that variations in climate played an important role in the ecological divergence of the two species [2]. Not only on the woody perennial plants, climate also has a similar impact on the annual herbaceous plants such as Arabidopsis, barley and so on [3].…”