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.