1. Introduction

Humans have, either accidentally or intentionally, transported tens of thousands of vascular plant species within and among continents across the world, of which over 13,000 have naturalized beyond their native ranges (van Kleunen et al., 2015). Naturalized species may pose significant threats to biodiversity and ecosystem structure and functioning in the recipient regions, particularly when they become invasive (Rejmánek et al., 2013). Investigating naturalized species composition in a particular region and phylogenetic relationships among naturalized plant species and between native and naturalized plant species in the region is a key research field in ecology and biogeography (van Kleunen et al., 2015; Park et al., 2020; Zhang et al., 2021a; Omer et al., 2022; Qian et al., 2022).

The Qinghai-Tibet Plateau, known as “the roof of the world” (Mao et al., 2013; Feijó et al., 2020), covers an area of ca. 2.5 million km² with an average height of more than 4500 m and many peaks exceeding 7000 m (Renner, 2016). The Qinghai-Tibet Plateau is the highest and one of the most extensive plateaus in the world (Zhang et al., 2002; Wen et al., 2014). The uplift of the plateau was driven by the collision of the Indian plate with the Eurasian plate, beginning at ca. 50 million years ago (Royden et al., 2008). A number of studies have investigated taxonomic diversity, genetic diversity, and phylogenetic structure of native vascular plants on the plateau (e.g., Wu, 2008; Mao et al., 2013; Yan et al., 2013; Mao et al., 2021; Li et al., 2022), but to the best of our knowledge there are few studies investigating taxonomic diversity and phylogenetic structure for introduced vascular plants on the plateau.

The extensive variation in the topography and climate of the Qinghai-Tibet Plateau generates a great diversity of habitats, which support abundant species diversity. However, biodiversity in the Qinghai-Tibet Plateau is threatened by biological invasions (Li et al., 2016). Tu et al. (2018) found over 136 invasive plants in the region, some of which, including Ageratina adenophora and Galinsoga parviflora, are cosmopolitan invasive species. Over a hundred of invasive plant species have been found in Nyingchi, a small city of Xizang (Yang et al., 2018). Recent development of the transportation network, such as railway and expressway, has not only stimulated connection between the Qinghai-Tibet Plateau and other regions in China but also among regions within the plateau, which have caused an increased risk of biological invasions. For example, in the selected 43 representative sites along the section from Ya'an to Changdu in the new Sichuan–Xizang Railway, Deng et al. (2020) found 58 invasive alien plant species in the sites.

In this study, we determine species richness of naturalized non-native species of vascular plants and investigate phylogenetic relatedness of native and naturalized non-native species of angiosperms on the Qinghai-Tibet Plateau. We do so for the plateau as a whole and for its constituent regions separately. Our key finding is that naturalized plant species are a phylogenetically clustered subset of all plant species on the plateau.

2. Materials and methods

The study area included all of Xizang Autonomous Region, commonly known as Tibet, and about one third of Qinghai Province, as shown in Fig. 1. This area, which included 1,448,815 km², is the core part of the Qinghai-Tibet Plateau. To facilitate discussion, we called our study area the Qinghai-Tibet Plateau (QTP), although our study area does not cover all of the Qinghai-Tibet Plateau (see Mao et al., 2021 for more information about various definitions of the QTP). Following Qian et al. (2019a), we divided the QTP into eight regions, of which seven were located in Xizang Autonomous Region and one was located in Qinghai Province (Fig. 1). These regions were coded as XZ1 through XZ7 for the seven regions in Xizang Autonomous Region and QH3 for the region in Qinghai Province in Qian et al. (2019a); we used these codes to name the regions in this study.

Distributions of vascular plants in the eight regions were documented based on numerous sources, including, but not being limited to, Wu et al. (1994–2013), Wu (1983–1987), Liu (1996–1999), Wu (2008), and herbarium specimen records with the Global Biodiversity Information Facility (GBIF; http://www.gbif.org) and the National Specimen Information Infrastructure (NSII; http://www.nsii.org.cn). Botanical nomenclature was standardized according to the World Flora Online (WFO, http://www.worldfloraonline.org), using the package U.Taxonstand (Zhang and Qian, 2023). Infraspecific taxa were combined with their parental species. The status of nativity of each species (i.e., native versus non-native) and the status of establishment of each non-native species (i.e., naturalized versus non-naturalized) were determined based on Wu et al. (1994–2013), Wu (1983–1987), Liu (1996–1999), Wu (2008), Lin et al. (2022), and Ma and Li (2018). Because information on plant species that were native to Chinese provinces outside of the QTP and were introduced to the QTP is generally lacking, non-native species considered here were those that were introduced to and naturalized in China and present on the QTP.

We used the package U.PhyloMaker (Jin and Qian, 2023) to generate a phylogenetic tree for the angiosperm species on the QTP. Specifically, we used the megatree GBOTB.extended.TPL.tre (Jin and Qian, 2022), which was derived from the megatrees reported in Smith and Brown (2018) and Zanne et al. (2014), as a phylogenetic backbone, the functions build.nodes.1, and Scenario 3 (Jin and Qian, 2022, 2023) to generate the phylogenetic tree. The vast majority of the genera in our data set were included in the megaphylogeny. We added the genera and species in our data set that were absent from the megatree to their respective families and genera using the U.PhyloMaker software (Scenario 3; Jin and Qian, 2022). Qian and Jin (2021) showed that, for the phylogenetic metrics used in this study, values derived from a fully resolved species-level tree are nearly identical to those from a tree resolved only at the genus level. Smaller phylogenetic trees were extracted from the phylogenetic tree for various analyses (see below for details). Phylogenetic trees generated by U.PhyloMaker or its sister packages (Qian and Jin, 2016; Jin and Qian, 2019, 2022) have been commonly used in studies on phylogenetic diversity and structure in regional and global floras (e.g., Qian et al., 2019a; Yue and Li, 2021; Zhang et al., 2021b; Qian, 2023; Zhou et al., 2023). Because introduced gymnosperm and pteridophyte species were few on the QTP and because the evolutionary history of gymnosperms and pteridophytes differs substantially from that of angiosperms, our phylogeny-based analyses included only angiosperms, as in many previous studies on plants (e.g., Qian et al., 2022). For non-native angiosperm species, our phylogeny-based analyses included only naturalized species.

We used net relatedness index (NRI) and nearest taxon index (NTI) (Webb, 2000; Webb et al., 2002) to measure phylogenetic relatedness among species. They were calculated using the package PhyloMeasures (Tsirogiannis and Sandel, 2016). NRI represents phylogenetic relatedness based on the average phylogenetic distance of all species in an assemblage whereas NTI quantifies phylogenetic relatedness by incorporating only the distances of the closest relative (Webb et al., 2002; Cadotte et al., 2018). Therefore, using NRI and NTI simultaneously in this study allows exploring patterns of species assembly at both deep and shallow evolutionary histories. Positive values of NRI and NTI indicate that species within assemblages are more closely related than expected for a random draw from the species pool; negative values of NRI and NTI indicate that species within assemblages are more distantly related than expected for a random draw from the species pool.

We calculated several sets of NRI and NTI for the QTP as a whole and for each of the eight regions, using tailor-made species pools. First, we calculated NRI and NTI for naturalized species for the QTP as a whole and for each region, using their respective species pools (e.g., for a particular region, the species pool included all native and naturalized angiosperm species in the region). An observed value of NRI or NTI was compared to a null expectation generated from 999 random draws of equal species richness from the species pool. For a normal distribution, significance at p-value < 0.05 is equivalent to NRI or NTI > 1.96 (i.e., significantly more phylogenetic clustering), or < −1.96 (i.e., significantly more phylogenetic over-dispersion) (Hortal et al., 2011). Second, to compare phylogenetic relatedness of angiosperms among the eight regions for both native and naturalized species, we calculated NRI and NTI for native and naturalized species in each region separately, using the species pool including all native and naturalized angiosperm species on the QTP. Because this set of values for NRI and NTI were derived from the same species pool, they can be compared.

3. Results

A total of 9580 species of vascular plants were found on the QTP delineated in this study (Fig. 1), of which 9086 were native species, 8335 of which in turn were angiosperms. Of the 494 non-native species, 314 were naturalized species, all of which were angiosperms. Each of the eight regions on the QTP had, on average, 2595 and 59 species of native and naturalized vascular plants, respectively (2446 and 59 species of native and naturalized angiosperms, respectively). Species richness of naturalized plants tended to decrease from the south to the north of the QTP, with the hotspot of naturalized plants being the region XZ4, which included the capital of Xizang Autonomous Region (Lhasa) and thus had more human-induced transportations of non-native plant species than other regions on the QTP.

When all naturalized angiosperm species on the QTP were considered, they were phylogenetically significantly (P < 0.05) clustered with respect to the species pool including all native and naturalized angiosperm species on the QTP, regardless of whether basal-weighted or tip-weighted metric of phylogenetic relatedness was used (i.e., NRI = 6.967, NTI = 2.692; Fig. 2). For the eight regions on the QTP, NRI and NTI were positive in seven regions (i.e., all but QH3; Fig. 3), 64% of which were significant (i.e., NRI and NTI > 1.96).

When native and naturalized angiosperm species in each of the eight regions were compared to the species pool of all (native and naturalized) angiosperm species on the QTP, NRI was positive for seven of the eight regions when native species were considered and for all the eight regions when naturalized species were considered (Fig. 4); 87.5% of the 16 values of NRI (i.e., 2 plant groups by 8 regions) were significant (P < 0.05) (Fig. 4). NRI for native species was greater than that of naturalized species in four of the eight regions (Fig. 4). NTI was positive in all the 16 cases, 87.5% of which were significant, and NTI for native species was greater than that for naturalized species in all the eight regions (Fig. 4).

4. Discussion

This study conducted the first investigation of introduced plants on the Qinghai-Tibet Plateau (QTP) at two spatial scales (i.e., the QTP as a whole and regions within it) focusing on both taxonomic diversity and phylogenetic relatedness. Although the QTP accounts for only about 15% of the total land area of China, the number of naturalized non-native species of vascular plants accounts for 25% of the total naturalized non-native species of vascular plants in China (314 versus 1271; this study; Qian and Qian, 2022). However, the QTP has much lower species richness of naturalized vascular plants than does a region east of it with similar latitudes. For example, a region including six contiguous provinces (Anhui, Henan, Hubei, Jiangsu, Shandong, and Zhejiang) in eastern China, which covers a total of 855,503 km², has 756 naturalized non-native species of vascular plants according to the data set compiled by Qian et al. (2022). Each of the six provinces has, on average, less area than the average area of the eight regions on the QTP (i.e., ~142,600 km² versus ~181,000 km²), but has much higher species richness of naturalized non-native vascular plants than does the QTP (i.e., 507 versus 59). Qian and Qian (2022) found that species richness of naturalized plants is positively correlated with mean annual temperature and annual precipitation. Within the QTP, we also found that species richness of naturalized plants tended to decrease with increasing latitude and thus decreasing temperature. Thus, that the QTP has a lower species richness of naturalized plants than a region of similar latitude in eastern China is likely duo to the fact that the former has lower temperature and precipitation than does the latter.

Our study showed that naturalized non-native angiosperms on the QTP are a phylogenetically clustered subset of the total (native plus naturalized non-native) angiosperm flora of the QTP (Fig. 2). This is the case regardless of whether NRI or NTI was used as a measure of phylogenetic relatedness. We observed the same pattern for the vast majority of the regional angiosperm floras on the QTP (Fig. 3). Previous studies (e.g., Lu et al., 2018; Qian et al., 2019a) showed that angiosperm species in western China, including the QTP, are phylogenetically more closely related (i.e., more strongly clustered) than those in eastern China. Across China, Qian et al. (2022) showed that the introduction of alien species generally increased phylogenetic clustering of angiosperms in the recipient areas. The findings of previous and present studies on the Chinese angiosperm flora together suggest that adding naturalized non-native species to a recipient region would likely increase phylogenetic relatedness among species in the region. Previous studies for angiosperm floras in other continents (e.g., Africa, Omer et al., 2022; North America, Qian and Sandel, 2022) also showed that naturalized non-native angiosperms increase phylogenetic relatedness in recipient regions. This consistent pattern among different continents suggests that the pattern is robust, even in regions with cold and arid environments such as the QTP, whose native plant species have already been a phylogenetically clustered subset of the species pool including all species in China (Lu et al., 2018; Qian et al., 2019a), although exceptions may occur (e.g., region QH3 in this study; Fig. 3).

We found that when deep evolutionary history is considered, naturalized species in an angiosperm assemblage are phylogenetically more closely related than native species in the assemblage in four of the eight regions on the QTP (i.e., NRI for naturalized species > NRI for native species; Fig. 4a), and are more distantly related than native species in the other four regions (i.e., NRI for naturalized species < NRI for native species; Fig. 4a). In addition, NRI for native species in the former four regions are higher than NRI for native species in the latter four regions (Fig. 4a). Of the four regions with NRI for naturalized species < NRI for native species, three are located in the southernmost part of the QTP (i.e., regions XZ2, XZ3 and XZ6), and have areas in relatively low elevations (e.g., < 500 m in regions XZ2 and XZ3). Areas in low elevations in these three regions lave relatively warm and moist subtropical or tropical climates, which favors species in many lineages, particularly those in ancient, tropical lineages. Tropical niche conservatism hypothesis predicts that species in warm and humid climates are more distantly related than those in cold and dry climates (Wiens and Donoghue, 2004; Qian et al., 2019a), leading to lower NRI and NTI in these regions than other regions. Furthermore, these regions may have received more Gondwanan plant lineages that were carried by the Indian plate and dispersed into the QTP after the Indian plate was collided with the Eurasian plate (Qian et al., 2019b; Li et al., 2022), compared to other regions on the QTP, because of more similar climates at low elevations and shorter geographic distances between each of these regions and the Indian plate. A greater degree of mixing in plant lineages from the two supercontinents (i.e., Gondwana and Laurasia) would presumably lead to greater phylogenetic distances (and thus greater phylogenetic dispersion) among species. These may explain, at least in part, why NRI for native species in the four southernmost regions of the QTP is not only smaller than NRI for natives in the other four regions but also smaller than NRI for naturalized species in their respective regions (Fig. 4a).

When phylogenetic relatedness is measured with the metric reflecting shallow evolutionary history used in this study (i.e., NTI), naturalized species in an angiosperm assemblage are phylogenetically more distantly related than native species (i.e., NRI for naturalized species < NRI for native species) in all the eight regions on the QTP (Fig. 4b). NTI measures phylogenetic relatedness of a species with its nearest species on the phylogeny, and such paired species are often sister species or congeneric species. It is well known that many plant species on the QTP were evolved from a relatively small number of genera (e.g., in the data set analyzed here, Rhododendron has 223 native species; Gentiana, 109; Pedicularis, 154; Primula, 143; Corydalis, 144). Many of the species of these genera evolved within the past few million years (e.g., Ren et al., 2015; Xia et al., 2021). Clustering of newly evolved species into a relatively small number of lineages in general, and genera in particular, would result in strong phylogenetic relatedness measured with a tip-weighted metric such as NTI. Thus, although NTI was positive for naturalized species in each of the eight regional angiosperm assemblages, reflecting phylogenetic clustering when the species are compared to the species pool including all angiosperms on the QTP, strong clustering of newly evolved species could lead to stronger phylogenetic relatedness for native species than for naturalized species when phylogenetic relatedness is measured with a metric focusing on phylogenetic relationships among species at the tips of a phylogenetic tree, as observed in this study (Fig. 4b).

Acknowledgements

We thank the two anonymous reviewers for their comments. This study was supported by grants from the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0502), the Strategic Priority Research Program of Chinese Academy of Sciences (XDA20050203), the National Natural Science Foundation of China-Yunnan joint fund to support key projects (U1802232), the Major Program for Basic Research Project of Yunnan Province (202101BC070002), the Yunnan Young & Elite Talents Project (YNWR-QNBJ-2019-033), the Ten Thousand Talents Program of Yunnan Province (202005AB160005) and the Chinese Academy of Sciences “Light of West China” Program.

Author contribution

H.Q. designed research, prepared data, analyzed data, and wrote the paper; T.D. prepared data, and generated maps; both authors participated in revising the paper.

Data availability statement

Data used in this study were obtained from various sources, which were cited in the article.

Declaration of competing interest

The authors declare no conflict of interest.