Introduction
The Quaternary period, comprising the Holocene and Pleistocene Epochs,
spanned the last ~2.6 million years (Myr) and
has
been characterized by distinct climatic oscillations, especially
alternating glacial and interglacial cycles in the Northern Hemisphere
(Shackleton & Opdyke, 1973; Pillans & Gibbard, 2012; Elias, 2013).
The
glacial cycles co-varied with, and probably profoundly affected, other
aspects of the climate, including the intensity of the Asian monsoon,
even in unglaciated regions (An, Kutzbach, Prell, & Porter, 2001; Jiang
, Lang, Tian, & Guo, 2011; Liu et al.,
2018).
Climate
fluctuations during the Quaternary glaciations led to dramatic changes
in
the
geographical distribution, genetic structure, and population
demography
of plant species (Hewitt, 2000; Wang et al., 2009; Jia et al., 2012; Liu
et al., 2018).
Quaternary climate change is known to have strongly affected
the
distributions of plants in Northern China (Tian et al., 2009; Qiu, Fu,
& Comes, 2011; Liu, Sun, Ge, Gao, & Qiu,
2012).
Northern China is dominated by deserts, which developed in the
Quaternary to due to sustained orogenesis of the Qinghai-Tibetan Plateau
and surrounding areas that ultimately enhanced aridity within the region
(Wu, 1992, 2002; Meng & Zhang, 2011). The climatic processes that gave
rise to the deserts also shaped regional plant diversity and yielded
highly complex demographic histories of native species (Ge, Yu, Yuan,
Huang, & Yan, 2005; Ge et al., 2011; Yang, Fang, Dong, Peng, & Li,
2006).
In
particular, many plants within the deserts of Northern China underwent
adaptive and demographic change in response to cold, arid conditions,
which occurred during the intermittent glacial periods and which may be
primary mechanisms explaining modern distributions (e.g., Comes &
Kadereit, 1998; Hewitt, 2000; Ge et al., 2011; Zhang & Zhang, 2012; Su
& Zhang, 2013; Zhang, Zhang, & Williams, 2014; Xu & Zhang, 2015;
Shuyskaya, Toderich, Gismatullina, Rajabov, & Khohlov, 2017; Merklinger
et al., 2019; El-Tayeh, Galal, Soliman, & Zaki, 2020). For example, Su
& Zhang (2013) proposed that the onset of aridity during Quaternary
glacial periods was a primary driver of population processes and
structures in Nitraria sphaerocarpa Maxim. (Nitrariaceae,
Sapindales), and Xu & Zhang (2015) revealed that periods of cold, arid
conditions during the Pleistocene glaciations resulted in the genetic
differentiation and demographic structuring in Atraphaxis
frutescens (L.) K.Koch (Polygonaceae).
Nevertheless, these prior studies on population histories of desert
plants of Northern China have focused primarily on
woody
species. Studies on herbs of the region are largely lacking, and to our
knowledge, the only such study is on Delphinium naviculare W. T.
Wang (Ranunculaceae) (Zhang & Zhang, 2012), which is endemic at
mid-elevations within the Tianshan Mountains of Xinjiang Province of
China (Wang & Warnock, 2001). Herbaceous plants of the deserts of
Northern China merit further study because they comprise a vital
component of desert plant communities, and studies focusing on dominant
grass species are especially warranted (Meng & Zhang, 2011). Herbaceous
plants may have been more sensitive to Quaternary climatic oscillations
because they differ markedly from woody species in their response to
cold, often via death of aboveground biomass as either part of an
annulment or perennial life cycle. Moreover, dominant species likely
achieved their abundance due to their responses to the glacial cycles.
In modern times, deserts and semi-deserts, such as in Northern China,
are extremely fragile ecosystems, the stability of which impacts global
environmental conditions and influences climate change (Su, 2013).
Although deserts typically have sparse vegetation, plants are critical
for maintaining their integrity. In Northern China, the desert grassland
ecosystems in particular are becoming rapidly degraded due to long-term
overgrazing and desertification and, simultaneously, desert is
encroaching on arable land within the region (Li, Liu, & Wang, 2004;
Hanafi & Jauffret, 2008; Wang, 2009; Peters, Yao, Sala, & Anderson,
2012; Deng, Zhang, & Shangguan, 2014; State Forestry Administration,
2015; Wang & Zhou, 2015; Wei, Wang, & Niu, 2020). These desert
grasslands represent a large area within China and adjacent countries
and occur at both low and high elevations. Dominant plant species within
the grasslands are often psammophytes, which have special adaptations to
resist being buried by sand and to tolerate having periodically exposed
roots. Simultaneously, these plants help to anchor sands in place and
prevented wind erosion, and are thus critical for promoting
environmental stability within their ecosystems (Ma, 1991; Pan, 2006;
Zhou, Yuan, & Jing, 2011).
In this study, we focus on one psammophyte, Psammochloa villosa(Trin.) Bor, which comprises a monotypic genus in tribe Stipeae of
Poaceae. This species, commonly called sand whip, is a perennial
rhizomatous herb that is primarily distributed in the desert grasslands
of northwestern China, especially the Inner Mongolian Plateau, the Hexi
Corridor of Gansu, central and Northern Ningxia, and Northern Shanxi
(Liu, 1985; Ma, 1994; Huang, 2003). It also occurs in Mongolia. The
flowering and fruiting period of P. villosa is from September to
November, and the seeds are 5 - 7 mm long with an average weight of
5.507 ± 0.053 mg (Huang, 2003). Such light seeds are likely dispersed by
high winds that occur throughout much of its natural desert habitat.
Nevertheless, seedlings are rarely observed (Zhu, 2005).Psammochloa
villosa is known to have high resistance to drought, cold, alkaline
soils, disease, wind, and burial by sand, all of which likely represent
evolutionary adaptations and facilitate its survival in grassland and
dune areas (Lu, 1987; Huang, 1995, 1997; Wu & Phillips, 2006).
Previous
research on P. villosa has been mainly focused on studying its
anatomy, embryology and microbiology (e.g., Dong & Alaten, 1999; Huang,
Dong, & Gutterman, 2004; Wang et al., 2011; Zhang et al., 2017; Lv et
al., 2018), with few studies so far focused on molecular markers (e.g.,
Li & Ge, 2001). The species is ecologically widespread at low and high
elevations (900-2900 m) (Kuo, 1987; Wu & Phillips, 2006).
In our present study, we
investigated the influence of climate aridification and oscillations on
the genetic structure and evolutionary processes of P. villosaduring the Quaternary in north-western China using amplified fragment
length polymorphism (AFLP) markers and ENM. We used AFLPs because they
remain extremely efficient for investigating genetic diversity, genetic
structure, and population demography due to their high levels of
polymorphism (Wang, Wang, Liu, Yang, & Chen, 2008), their reproducible,
reliable results that are unaffected by the developmental stage of plant
materials, and their universality among plant species. In addition, they
have been used to resolve genetic structures and population demography
in many diverse grass species such as Oryza sativa , Leymus
racemosus , Orinus thoroldii and O. kokonoricus (Zhang &
Jia, 2002; Sim, 2005; Li, 2015; Cai, 2017; Liu, Harris, Gao, Su, & Ren,
2019). Our main objectives were to (1) analyze the genetic structure
from 43 populations of P. villosa from Inner Mongolian Plateau
using an AFLP dataset, (2) test whether historical genetic divergence
occurred among populations in response to Quaternary climate
oscillations, and (3) evaluate the abiotic factors that are most
influential in driving the distributions of P. villosa . Moreover,
because no assessment of the conservation needs of P. villosa had
previously been accomplished, we also performed a preliminary assessment
based on Extent of Occurrence (EOO) with interpretation according to
guidelines of the International Union for the Conservation of Nature
(IUCN). We believe that, taken together, our results can provide a
scientific basis for improved protection and sustainable utilization
(e.g., as forage) of P. villosa within the fragile desert
grassland ecosystems of Northern China.