Abstract
The mountains of southern China are an excellent system for
investigating the processes driving the geographic distribution of
biodiversity and radiation of plant populations in response to
Pleistocene climate fluctuations. How the key mountain ranges in
southern China have affected the evolution of narrowly distributed
species is less studied than more widespread species. Here we focused onCercis chuniana, a woody species endemic to the southern mountain
ranges in subtropical China, to elucidate its population dynamics. We
used genotyping by sequencing (GBS) to investigate the spatial pattern
of genetic variation among 11 populations. Bayesian time estimation
revealed that population divergence occurred in the middle Pleistocene,
when populations in the Nanling Mts. separated from those to the east.
Geographical isolation was detected between the populations located in
adjacent mountain ranges, thought to function as geographical barriers
due to their complex physiography. As inferred by ecological niche
modeling and coalescent simulations, secondary contact occurred during
the warm Lushan-Tali interglacial period in China, with intensified East
Asia summer monsoon and continuous habitat available for occupation.
Complex physiography plus long-term stable ecological conditions across
glacial cycles facilitated the demographic expansion in the Nanling
Mts., from which contemporary migration began. Our work shows that
population genomic approaches are effective in detecting the population
dynamics of narrowly distributed species. This study advances our
understanding how glacial cycles have affected the evolutionary history
of plant species in southern China montane ecosystems.
KEYWORDS: Cercis chuniana , demographic modeling,
geographic isolation, Pleistocene glacial cycles, secondary contact,
Southern China mountainous ranges
INTRODUCTION
High physiographical heterogeneity is suggested to prompt rapid
diversification in montane habitats because of the increased ecological
opportunities afforded by frequent episodes of geographic isolation
(Colin & Ruth, 2006; Muellner-Riehl, 2019; Simpson, 1964). The high
biodiversity of southern China is due in large part to the extreme
physiographical heterogeneity of its mountain ranges (Fan et al. ,
2018; Xu et al., 2017; Yang, Dick, Yao, & Huang, 2016). Often oriented
in either north-south or northeast-southwest directions (Hou, 1983;
Wang, 1992a; Wang, 1992b; Ying, 2001), these topographically diverse
ranges have been suggested to serve as either geographical barriers or
colonization corridors for various plant species (Gong et al., 2016;
Tian et al., 2018; Xiong, Wu, & Zhang, 2019). Their local habitat
uniqueness has been attributed to complex topography correlated with
longitudinal or steep elevational gradients (Qiu, Zeng, Chen, Zhang, &
Zhong, 2013; Wang, Fang, Tang, & Shi, 2012). The primary vegetation
type of these mountains is subtropical evergreen broadleaved forest
(STEBF), one of the largest continuous such forests in the world and
well known for harbouring ancient relictual elements of the
north-temperate biota (Qiu, Fu, & Comes, 2011; Wang, Fang, Tang, &
Shi, 2012). Many of their plant species, predominantly endemics, exhibit
high rates of local and rapid radiation (Hou et al., 2017; López-Pujol,
Zhang, Sun, Ying, & Ge, 2011) presumably arising within the last 5
million years, in line with both orogenic events and Pleistocene glacial
cycles (Li et al. , 1979; Liu et al. , 2013; Shi, Li, & Li,
1998; Wang et al. , 2010). These characteristics make southern
China an excellent system for investigating the processes driving the
geographic distribution of biodiversity and radiation of plant
populations in response to Pleistocene climate fluctuations.
Climatic oscillations associated with glacial cycles during the
Pleistocene are also considered as an important factor driving the
distribution pattern of biodiversity and shaping the demographic history
of populations, particularly in montane regions (Hewitt, 2004; Li et
al., 2019; Mesquita, Tillmann, Bernad, Rosemond, & Suding, 2018;
Svenningm, Normand, & Skov, 2009). Although still under debate,
considerable data are now available to support four glacial periods in
eastern China (east to 105ºE) during the Pleistocene, i.e. the Poyang,
Dagu, Lushan and Tali Glacials (Duan, Pu, & Wu, 1980). In southern
China, the degree of habitat connectivity is thought to have decreased
during glacial periods, with vegetation belts lowering in elevation and
contracting in geographic range, providing the opportunity for both
geographical isolation and genetic divergence to occur (Shi, Cui, & Su,
2006). Multiple glacial refugia correlated with centres of genetic
diversity have been identified in southern China, out of which
subsequent localized or rapid range expansions have been inferred (Chen
et al., 2012; Gong, Chen, Dobes, Fu, & Koch, 2008; Li, Shao, Lu,
Zhang, & Qiu, 2012; Qiu, Fu, & Comes, 2011; Tian et al., 2015).
Previous research has elucidated the scenarios involved with glacial and
postglacial evolutionary history of plant species in southern China
(Gong et al., 2016; Liu et al., 2012; Tian, Ye, Wang, Bao, & Wang,
2020). However, most of this research has focused on widespread species
and ignored how key mountain ranges might affect the evolution of
narrowly distributed species.
Cercis chuniana F. P. Metcalf (Fabaceae: Cercidoideae; Azani et
al., 2017) is a small tree or shrub endemic to the STEBF of southern
China. It has a narrow geographical distribution, extending from the
Wuyi and Eastern China Mountains westwards to the Nanling Mountains with
increasingly larger population sizes and densities. Unique amongCercis species, it has an asymmetrical leaf blade (Chen, Zhang,
Larsen, & Vincent, 2010; Metcalf, 1940), which makes it easily
identifiable morphologically. The species is resolved near the base of
the Cercis phylogenetic tree, with an estimated age of 2.40 Ma
(Fritsch et al. , 2018; Liu et al., unpublished data, 2020). As
with its congeners in China, it exhibits an adaptation to mesic
environments through its acuminate leaf blade apex (Fritsch et
al. , 2018; Isely, 1975; Wunderlin Larsen, & Larsen, 1981).
Genotyping by sequencing (GBS) has been widely used as a genomic
approach for investigating genetic diversity and population structure
(Chen, Hou, Zhang, Pang, & Li, 2017; Metzker, 2010; Niu et al. ,
2019). Because it is based on genomic reduction with restriction
enzymes, GBS does not require a reference genome to detect single
nucleotide polymorphisms (SNPs). In combination with marker discovery
and genotyping, GBS provides a rapid, high-throughput, and
cost-effective tool for a genome-wide analysis for nonmodel species
(Andrews, Good, Miller, Luikart, & Hohenlohe, 2016; Davey et
al. , 2011; Scheben, Batley, & Edwards, 2017). Here, we used GBS
and collected genome-wide SNPs for population genetic analyses ofC. chuniana . We aimed to 1) investigate genetic diversity and
population structure of the species, 2) elucidate its demographic
history, and 3) use the data to infer the roles of mountain ranges in
southern China and Pleistocene climatic fluctuations in driving its
diversification and geographic distribution. We thereby hoped to gain a
better understanding of the impact of this environment on the
evolutionary history of narrowly distributed species.