Monsoon-driven assembly of the world’s largest evergreen broadleaved forest

ABSTRACT

As the world’s largest evergreen broadleaved forest (EBLF), East Asian EBLF houses high levels of biodiversity and endemism and is essential to regional carbon storage and cycling. However, how East Asian EBLF was shaped over time remains an open question. Here, we investigate the historical assembly of this biome by sampling 21 angiosperm clades (together encompassing 2028 species) that include evergreen and deciduous species. We show that the transition from deciduous to evergreen lineages, and in situ diversification and immigration of evergreen lineages in subtropical East Asia all experienced a dynamic process. Transition and immigration reached their first peaks and in situ diversification sharply increased at the Oligocene–Miocene boundary (OMB), and all of them reached their highest peaks in the late Miocene. Our results suggest that modern East Asian EBLF did not appear until the OMB and markedly deteriorated since the Pliocene, mainly driven by the evolution of Asian monsoon climate. This study suggests that East Asian EBLF has functioned as both museums and cradles for regional biodiversity, and serves as a transfer station for biotic exchanges between temperate and tropical regions, highlighting its great conservation value.

INTRODUCTION

Biodiversity is very unevenly distributed on Earth [1]. Understanding how biodiversity in an ecoregion or biome, especially species-rich, has developed over time is a fundamental question in ecology and evolutionary biology [2,3]. As the world’s largest evergreen broadleaved forest (EBLF) [4], East Asian EBLF covers southern China, southern Japan and southernmost Korea (Fig. 1) [5], and is characterized by high levels of species diversity and endemism compared to the regions at similar latitudes elsewhere on the planet, which are mostly arid and semiarid lands [6]. This biome is home to ∼2600 genera and 14 600 species of seed plants, of which >50% are endemics [7], with many relict species [8,9]. East Asian EBLF plays important roles in regional carbon storage and cycling, providing various biological resources, and promoting sustainable social development [10,11]. Nevertheless, the primeval EBLF in East Asia has been greatly diminished owing to anthropogenic activities [6,12] and only covers ∼5% of China’s total land area nowadays [13], underlining the urgency of understanding its historical assembly.

Figure 1.

Geographic map of East Asian EBLF. The range of East Asian EBLF (solid line) is modified from Song and Da [5] and Tang [6]. The freezing boundary (dashed line) is here defined as having a mean minimum annual temperature ≤0°C (calculated from WorldClim data https://worldclim.org/). Representative landscape and plants are shown on the right: upper, EBLF in southeastern QTP; middle left, Quercus cocciferoides (Fagaceae); middle right, Lindera megaphylla (Lauraceae); bottom left, Magnolia figo (Magnoliaceae); bottom right, Camellia crapnelliana (Theaceae). AWM, Asian winter monsoon; EASM, East Asian summer monsoon; SASM, South Asian summer monsoon. Review drawing number: GS 京(2026)2003号.

Unfortunately, the evolutionary history of East Asian EBLF remains contentious. Plant fossils and paleovegetational reconstructions suggest that this biome had emerged by the middle Eocene [14–16] or late Eocene–early Oligocene [17,18]. By integrating fossil data and modelling results, Li et al. [19] show that the transition from deciduous to evergreen habits in East Asian broadleaved forests occurred at the Oligocene–Miocene boundary (OMB). Dated phylogenies of representative components of East Asian EBLF support the rise of this biome in the Eocene [20–23], early Oligocene [24,25] or around the OMB [26–29]. Nevertheless, an organismal group could require a long timescale to adapt to a novel climatic regime or habitat, that is, an ‘evolutionary lag time’ often occurs [30]. This makes it challenging to draw a comprehensive picture of the historical assembly of a biome using a single taxon as the proxy. By analyzing the crown group ages of 72 so-called characteristic genera, Zhang et al. [31] suggest an early Oligocene origin for Chinese EBLF. These genera were selected based on the proportion of species in Chinese EBLF to the total number of species in China (≥20%) [31]. Under this criterion, monotypic or oligotypic genera were easily included, such as Cercidiphyllum, Cyclocarya, Euptelea and Sargentodoxa, but they are deciduous; moreover, some genera with many non-East Asian and/or non-evergreen species were also included, such as Acer, Ilex and Viburnum, but the original ages of the evergreen lineages in these genera are obviously younger than their crown group ages. ‘Evergreen’ is the most prominent feature for East Asian EBLF [5], and only the evolutionary dynamics of evergreen lineages can provide insights into the formation process of this biome [19,25–28,32]. To elucidate how East Asian EBLF was shaped over time, a molecular phylogenetic study of multiple clades with evergreen lineages across the angiosperm tree of life is essential.

Biome assembly is closely associated with geoclimatic changes [33,34]. The India–Eurasia collision started in the Paleocene and subsequently caused the deformation and uplift of the Qinghai–Tibet Plateau (QTP) [35,36], which have had a profound impact on regional and even global climates and environments [37,38]. The data from ^δ18O levels in benthic foraminifera show that global temperature changed dramatically in the Cenozoic [39]. Importantly, the Asian monsoon climate, which can bring abundant rainfall, is generally considered to be the most important factor that influences the evolutionary process of East Asian EBLF [26–28]. Yet, the evolution of the Asian monsoon system was complex during the Cenozoic [37,40]. Some studies suggest that the Asian monsoon climate resembling the modern pattern was fully established around the OMB [38,41]. In contrast, other studies support that the Asian monsoon had emerged by the Eocene [42,43] or even Paleocene [44]. Nevertheless, tropical monsoon reached only low latitude regions in Asia (south of 20–22°N) due to seasonal fluctuation of the Intertropical Convergence Zone (ITCZ) in the early Cenozoic, and until ∼41 Ma, the Asian monsoon did not expand northward to subtropical southern China [38,45].

Here, we attempt to connect past geoclimatic changes to the biological processes that have driven the assembly of East Asian EBLF. We use evergreen lineages within the 21 selected angiosperm clades as the proxy to unravel the evolutionary history of East Asian EBLF at a global scale, by conducting a multi-taxon analysis. We investigate whether phylogenetic estimates of East Asian evergreen ancestry are temporally in agreement with the formation of modern-like Asian monsoon climate, and test whether geoclimatic events in East Asia left discernible imprints in the assembly of East Asian EBLF. Specially, we test whether the transition events from deciduous to evergreen habits in subtropical East Asia mainly took place around the OMB or experienced a dynamic process. We further investigate the temporal dynamics of in situ diversification and immigration events of evergreen lineages in East Asian EBLF. We show that modern-like East Asian EBLF began to appear around the OMB, flourished continuously throughout the Miocene and deteriorated since the Pliocene, which were mainly influenced by a long-term and complex evolution of Asian monsoon system. We further discover that East Asian EBLF is both evolutionary cradles and museums for East Asian biodiversity and serves as a transfer station for biotic exchanges between temperate and tropical regions.

RESULTS AND DISCUSSION

To illustrate the assembly process of East Asian EBLF, we selected 21 clades with 2028 species, belonging to 14 orders and 24 families across the angiosperm tree of life (Fig. S1 and Table S1). A total of 680 evergreen species (406 endemic) and 381 deciduous species (206 endemic) growing in subtropical East Asia are included. This sampling strategy maximized taxon representation in East Asian EBLF so far, especially covering the members of the first five dominant families in this biome, i.e. Fagaceae, Lauraceae, Magnoliaceae, Theaceae and Hamamelidaceae [5]. By integrating results of molecular dating, biogeographic and habit analyses for each of the 21 clades (Fig. S2), we compiled age credibility intervals of the transition from deciduous to evergreen habits in subtropical East Asia, and calculated the maximal number of observed transition events (MTE) per million year (Myr) (Fig. S3). Considering that the species diversity in a biome arises from both in situ diversification and immigration, we further compiled credibility intervals of age estimates for in situ diversification and dispersal events of evergreen lineages and calculated their maximal number of observed events (MDivE & MDisE) per Myr, respectively. In addition, we performed generalized least squares multiple regression analyses to test the possible correlation between evolutionary dynamics of evergreen lineages and environmental changes, i.e. East Asian annual precipitation and global temperature, over time and employed breakpoint regression analyses to test whether Asian monsoon climate change impacted the MTE, MDivE and MDisE.

Our biogeographic and habit analyses identified 48 transition events from deciduous to evergreen habits in subtropical East Asia. A total of 788 biogeographic events related to subtropical East Asian evergreen species examined here were found, including 773 in situ diversification events and 15 dispersal events. In situ diversification events overwhelmingly predominated over dispersal events by ∼52 times (773/15), implying that indigenous elements contributed far more than immigrants to the current biodiversity of East Asian EBLF. Considering the relatively low sampling for some clades, this hypothesis needs to be tested in the future by sampling more taxa. The transition from deciduous to evergreen habits and in situ diversification initially occurred in the Lower Cretaceous (Fig. S3). Transition events accelerated at ∼56, 35 and 27 Ma, and peaked around 25–23 Ma and 8–7 Ma (Fig. 2a). In situ diversification events accelerated at ∼48, 23 and 16 Ma, and peaked around 8–6 Ma (Fig. 2b). Dispersal events into subtropical East Asia started at ∼36 Ma and peaked around 26–23 Ma and 6–5 Ma, which were from two source regions: temperate Eurasia and tropical Asia (Fig. 2c). Our multiple regression analyses support the positive relationship between evergreen lineage occurrence, in situ diversification, dispersal and East Asian annual precipitation, respectively (Fig. 3 and Table S2), highlighting the important roles of the precipitation regime in promoting the diversification of evergreen lineages.

Figure 2.

Evolutionary dynamics of evergreen lineages in subtropical East Asia and potential driving factors. (a) Transition rates from deciduous to evergreen habits based on the MTE per Myr. (b) In situ diversification rates of evergreen lineages based on the MDivE per Myr. Details for transition and in situ diversification dynamics in a broader timeframe can be found in Fig. S3. Arrowheads indicate estimated inflection points. (c) Dispersal rates of evergreen lineages from other regions to subtropical East Asia based on the MDisE per Myr. (d) Elevation changes of different parts of the QTP [35] and the Qilian Shan [56], global mean temperature difference to today [39], Asian climatic records [38] and suitable area (grid cell) dynamics of East Asian EBLF. EECO, Early Eocene Climatic Optimum; Pli, Pliocene; Q, Quaternary.

Figure 3.

Partial regression plots showing correlations between the three events related to East Asian subtropical evergreen lineages and annual precipitation in East Asia. The solid line and gray shading indicate the regression line and 95% credible interval separately, with circles showing the raw data.

In situ diversification began at ∼125 Ma, by ancestral lineage of the Altingiaceae–Hamamelidaceae clade (Figs S2 and S3). Transition started at ∼93 Ma, mainly by ancestral lineage of Magnolia (Figs S2 and S3 and Table S3). These suggest that some ancient elements of East Asian EBLF might have occurred in the Lower to Upper Cretaceous, implying that the EBLF functions as a museum for plant species diversity in East Asia. During this period, global average temperature was considerably high without large and permanent icecaps [46], and angiosperm-dominated forests started to arise [47,48] along with the Cretaceous Terrestrial Revolution [49].

The MTE curve initially accelerated at ∼56 Ma (Fig. 2a), which temporally coincides with the transition from the ‘Warmhouse’ to ‘Hothouse’ climate state (Fig. 2d) [39]. The MDivE curve first accelerated at ∼48 Ma (Fig. 2b), in line with the Early Eocene Climatic Optimum (Fig. 2d). Geological data indicate the uplift of southern (∼55 Ma) and central (∼45 Ma) parts of the QTP caused by the India–Eurasia collision [35]. The orogenic events in the QTP, as well as the migration of Pacific warm pool back to Asia, resulted in the dominance of ITCZ-type monsoonal climate in East Asia and thereby brought more precipitation [37]. We also identified an increased point of the MTE curve in the late Eocene (∼35 Ma; Fig. 2a). During this period, subtropical monsoon climate gradually prevailed in southern China and expanded northward (Fig. 2d), along with significant increase in precipitation [38,45,50,51]. Based on our ancestral range and habit reconstructions (Fig. S2), most evergreen lineages that originated in the Eocene are currently distributed in southern China to Southeast Asia, such as some species of Lithocarpus (Fagaceae), Actinodaphne henryi and Sinosassafras flavinervium (Lauraceae) and the Viburnum punctatum–V. lepidotulum clade (Viburnaceae). Thus, EBLF might have only appeared in low latitudes of subtropical East Asia during the Eocene. Paleobotanical data also indicate that dominant genera in southern Chinese EBLF started to occur in the Paleocene–early Eocene, and peaked in the middle Eocene [16].

Transition further accelerated in the late Oligocene (∼27 Ma) and later reached the first peak around 25–23 Ma (Fig. 2a). The MDivE curve sharply increased at ∼23 Ma (Fig. 2b), and the MDisE curve peaked around 26–23 Ma (Fig. 2c). Moreover, MDivE and MDisE curves that were calculated based on the evergreen lineages only from the first five dominant families in East Asian EBLF significantly increased around the OMB (Fig. S4). In the late Oligocene–early Miocene, the dramatic uplift of central and southern QTP occurred (Fig. 2d), which largely reorganized Asian climate and shaped the modern-like Asian monsoon system (Fig. 2d) [38,41]. During this period, East Asian summer monsoon started to establish [52], and South Asian summer monsoon intensified [53], contributing to more summer precipitation [54] and the emergence of spring persistent rainfall [40] in East Asia. Meanwhile, the weakening of Asian winter monsoon increased winter precipitation in East Asia [19]. The breakpoint regression analyses supported that the formation of modern-like Asian monsoon system influenced all of the MTE, MDivE and MDisE (Table 1). Our modelling analysis indicates significant increase of suitable area of East Asian EBLF at ∼25 Ma (Fig. 2d), in agreement with the result of Guo et al. [55] that a wide humid belt similar to the modern one occurred in subtropical East Asia near the OMB. Importantly, considering the credibility intervals of estimated times, 85%, 88% and 93% of transition, in situ diversification and dispersal events took place after the OMB (∼23 Ma). We also found that ∼95% of the evergreen species in East Asian EBLF and ∼96% of the evergreen species endemic to this biome occurred after ∼23 Ma (Fig. 4), suggesting that East Asia EBLF acted as an evolutionary cradle for East Asian biodiversity. Thus, our data show that the modified monsoon system resulted in the humidification of East Asia and thereby promoted the modernization of the EBLF in this region around the OMB, as supported by the results of modelling and fossil data [19].

Table 1.

Model evaluation for breakpoint regression analyses using Bayesian inference on the temporal dynamics of transition (MTE), in situ diversification (MDivE) and dispersal (MDisE) events. Model description: Null, model with no break points; E, model with a break point around ∼41 Ma, representing northward expansion of Asian monsoon to subtropical southern China; M, model with a break point between 25 and 23 Ma, representing formation of modern-like Asian monsoon system; P, model with a break point between 3.6 and 2.6 Ma, representing decrease in East Asian precipitation. Models with an estimated log posterior density (ELPD) difference of zero are considered to be the optimal model (in bold).

	ELPD difference ± standard error
Model	MTE	MDivE	MDisE
Null	−36.8 ± 6.6	−41.4 ± 5.8	−13.2 ± 4.6
E	−7.0 ± 8.8	−27.1 ± 5.4	N/A
M	−4.6 ± 3.2	0.0 ± 0.0	−0.2 ± 1.7
P	−37.8 ± 6.6	−40.9 ± 5.8	−14.0 ± 4.5
EM	−16.9 ± 7.8	−26.7 ± 5.4	N/A
EP	−5.8 ± 9.1	−27.8 ± 5.8	N/A
MP	0.0 ± 0.0	−0.2 ± 1.3	0.0 ± 0.0
EMP	−5.8 ± 9.0	−27.8 ± 5.8	N/A

Figure 4.

Distribution of estimated origination ages of evergreen species in East Asian EBLF.

The MDivE curve shows a virtually linear increase between 23 and 8 Ma (Fig. 2b) and peaked in the late Miocene (∼8–5 Ma), during which MTE and MDisE curves also reached their high peaks (Fig. 2a–c). This temporally coincides with the uplift of Qilian Shan (Fig. 2d) [56]. From ∼12 to 4 Ma, an intensified Asian monsoon dominated East Asia, which might have contributed to the more persistent wet season through the year [37,51], and the East Asian spring persistent rainfall reached its modern-day geographic distribution [40]. The EBLF thereby flourished continuously in East Asia throughout the Miocene.

From ∼4 Ma onwards, the MTE, MDivE and MDisE curves all decreased (Fig. 2a–c), which temporally coincides with a marked decrease of precipitation in East Asia [37,40] and the transition from the ‘Coolhouse’ to ‘Coldhouse’ climate state (Fig. 2d). The freezing temperature is a key factor limiting the distribution of evergreen broadleaved species [5,28]. The breakpoint regression analyses also found that this decrease in precipitation had an impact on the MTE and MDisE curves (Table 1). In addition, our modelling results suggest the significant decrease of suitable areas of East Asian EBLF occurred at this time (Fig. 2d). Thus, temperature and precipitation drop could have hampered the diversification of evergreen lineages and have progressively deteriorated East Asian EBLF since the Pliocene.

Among the referred 15 dispersal events of evergreen lineages into subtropical East Asia (Table S4), most of them were from tropical Asia (∼73%), and the remaining were from temperate Eurasia (∼27%), suggesting the great contribution of tropical Asia to species diversity of East Asian EBLF. In addition, we also identified 225 dispersal events out of East Asian EBLF spanning from 90.42 to 0.29 Ma, most of which (∼81.3%) colonized tropical Asia, followed by temperate Eurasia (∼14.7%), North America (∼2.2%), South America (∼1.3%) and Africa (∼0.4%) (Fig. S5). Altogether, these results suggest that East Asian EBLF serves as not only a sink, but also an important source region for species diversity of other regions of the world, and thus promotes biotic exchanges between temperate and tropical regions, highlighting the importance of its conservation.

In summary, our multi-taxon study provides new insights into the historical assembly of East Asian EBLF over a broad period of ∼125 Myr. All of the MTE, MDivE and MDisE curves experienced a dynamic process. The occurrence of in situ diversification is much earlier than that of dispersal, and the former overwhelmingly predominated over the latter. Our results support that the modernization of East Asian EBLF did not take place until the OMB, which was driven by the formation of modern-like Asian monsoon climate system. East Asian EBLF has functioned as both evolutionary museums and cradles for evergreen species diversity of East Asia, and served as a transfer station for biotic exchanges between temperate and tropical regions, emphasizing the conservation priority for this world’s largest EBLF. Many herbaceous and deciduous species also inhabit East Asian EBLF. Whether they have similar trends through time to evergreen species needs to be investigated in the future.

MATERIALS AND METHODS

Detailed materials and methods are available in the Supplementary material.

DATA AVAILABILITY

The data underlying this article are available at Figshare (https://doi.org/10.6084/m9.figshare.30162892).

FUNDING

This work was supported by the National Natural Science Foundation of China (32361133549 and 32400175), the Beijing Natural Science Foundation (5264044), the National Key Research and Development Program of China (2023YFF0805800) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31030000).

AUTHOR CONTRIBUTIONS

W.W. conceived the research. H.-W.P., L.H. and W.W. collected data. H.-W.P., L.H., X.-Q.L. and W.W. analyzed data. H.-W.P., R.C.O., F.J. and W.W. wrote the paper with input from all the authors.

Conflict of interest statement. None declared.