The East Asian Winter Monsoon Acts as a Major Selective Factor in the Intraspecific Differentiation of Drought-Tolerant Nitraria tangutorum in Northwest China

Abstract

The influence of Quaternary climate fluctuation on the geographical structure and genetic diversity of species distributed in the regions of the Qinghai–Tibet Plateau (QTP) has been well established. However, the underlying role of the East Asian monsoon system (EAMS) in shaping the genetic structure of the population and the demography of plants located in the arid northwest of China has not been explored. In the present study, Nitraria tangutorum, a drought-tolerant desert shrub that is distributed in the EAMS zone and has substantial ecological and economic value, was profiled to better understand the influence of EAMS evolution on its biogeographical patterns and demographic history. Thus, the phylogeographical structure and historical dynamics of this plant species were elucidated using its five chloroplast DNA (cpDNA) fragments. Hierarchical structure analysis revealed three distinct, divergent lineages: West, East-A, and East-B. The molecular dating was carried out using a Bayesian approach to estimate the time of intraspecies divergence. Notably, the eastern region, which included East-A and East-B lineages, was revealed to be the original center of distribution and was characterized by a high level of genetic diversity, with the intraspecific divergence time dated to be around 2.53 million years ago (Ma). These findings, combined with the data obtained by ecological niche modeling analysis, indicated that the East lineages have undergone population expansion and differentiation, which were closely correlated with the development of the EAMS, especially the East Asian winter monsoon (EAWM). The West lineage appears to have originated from the migration of N. tangutorum across the Hexi corridor at around 1.85 Ma, and subsequent colonization of the western region. These results suggest that the EAWM accelerated the population expansion of N. tangutorum and subsequent intraspecific differentiation. These findings collectively provide new information on the impact of the evolution of the EAMS on intraspecific diversification and population demography of drought-tolerant plant species in northwest China.

Evolutionary history of a desert perennial Arnebia szechenyi (Boraginaceae): Intraspecific divergence, regional expansion and asymmetric gene flow

“…It is likely that the northwestward movement of the East Asian monsoon intensified the spread from the eastern to western genetic groups. The important role of East Asian monsoon system in shaping population genetic structure has also been demonstrated in other plants in this region ( Yin et al., 2015 , 2020 ; Zhang et al., 2017b ).…”

“…The arid northwest region of China is one of the largest mid-latitude, temperate, continental interior dryland areas in the world. The disjunctive deserts of this region (i.e., the Taklamakan Desert, Badain Jaran Desert, and Tengger Desert) ( Yang and Scuderi, 2010 ), have attracted increasing interest from researchers (e.g., Meng et al., 2015 ; Yin et al., 2015 ; Zhang et al., 2017b ; Zeng et al., 2018 ; Li et al., 2019 ; Zhao et al., 2019 ; Yin et al., 2020 ). These studies have revealed that three factors have played a role in shaping the population genetic structure of plants occurring in this region: increased aridification, subsequent desert expansion, and changes in the East Asian monsoon system ( Yin et al., 2015 , 2020 ; Zhang et al., 2017b ).…”

“…The disjunctive deserts of this region (i.e., the Taklamakan Desert, Badain Jaran Desert, and Tengger Desert) ( Yang and Scuderi, 2010 ), have attracted increasing interest from researchers (e.g., Meng et al., 2015 ; Yin et al., 2015 ; Zhang et al., 2017b ; Zeng et al., 2018 ; Li et al., 2019 ; Zhao et al., 2019 ; Yin et al., 2020 ). These studies have revealed that three factors have played a role in shaping the population genetic structure of plants occurring in this region: increased aridification, subsequent desert expansion, and changes in the East Asian monsoon system ( Yin et al., 2015 , 2020 ; Zhang et al., 2017b ). Meanwhile, studies have shown that geographical barriers (e.g., mountains, sand dunes and continuous oases) may have led to intraspecific differentiation and even promoted speciation processes ( Zeng et al., 2018 ; Li et al., 2019 ; Zhao et al., 2019 ).…”

Will the artificial populations be sustainable? A genetic assessment on Caragana korshinskii afforestation in the semiarid regions of North China

“…In the present study, the level of cpDNA genetic diversity in the natural C. korshinskii populations is relatively higher (Hd = 0.29 ~ 1.00 and π = 0.00012 ~ 0.00085) compared to a sister species C. microphylla, in which the highest population genetic diversity is Hd = 0.771 and π = 0.0005 (Xu et al 2017). This is also higher than the other two constructive desert shrubs, with Reaumuria soongarica showing Hd = 0 ~ 0.600 and π = 0 ~ 0.00248 (Li et al 2012;Yin et al 2015) and Nitraria tangutorum showing Hd = 0.928 and π = 0.0007 (Yin et al 2020). In addition, the genetic diversity level of the afforested C. korshinskii populations in this study is also similar to or even higher (Hd = 0.64 ~ 1.00 and π = 0.00033 ~ 0.00073) than that of wild desert shrubs.…”

Genomic Adaptive Evolution of Sand Rice (Agriophyllum squarrosum) and Its Implications for Desert Ecosystem Restoration

“…Deserts in marginal monsoonal zones tend to experience frequent contractions and expansions during glacial and interglacial periods (Lu et al, 2013), during which times the dynamics (such as the distribution ranges and effective population size) of desert plants in this region are significantly sped up (Yin et al, 2015;Qian et al, 2016), which sheds an interesting light on the influence of climate change on the demographic history of desert plant species (Wang et al, 2013;Ignace et al, 2018;Shi et al, 2020;Yin et al, 2020). During long-term adaptation to monsoonal climate change and heterogeneous environments, those populations can be expected to harbor more valuable genetic resources.…”