The family Symplocaceae includes over 300 species of trees and shrubs that have a disjunct distribution in the warm-temperate to tropical regions of eastern, southern, and southeastern Asia, eastern Australia, and the Americas. The family accommodates two genera, Cordyloblaste Hensch. ex Moritzi and Symplocos Jacq., which comprises two subgenera, subg. Palura (G. Don) P.W. Fritsch with only one species, Symplocos paniculata (Thunb.) Miq., and subg. Symplocos with three sections: sect. Barberina A. DC., sect. Lodhra G. Don, and sect. Symplocos (Fritsch et al., 2008; Almeda and Fritsch, 2009). Most of the species of subg. Symplocos are evergreen while subg. Palura has a deciduous habit. In China, both subgenera of Symplocos, with 42 extant species including 18 endemic species, are mainly distributed across the southern part of the country (Wu and Nooteboom, 1996).

The fruit of Symplocos can be described as an inferior pyrenarium containing a single pyrene (the hard inner portion of the pyrenarium) with (2–)3–5 locules, which are separated from each other by sclerenchymatous or/and parenchymatous false septa (Chirtoiü, 1918; Nooteboom, 1975, 2004). The pyrenes of Symplocos species vary in outlines from globose to ovoid, ellipsoid or ampulliform and are mostly truncate at the apex with cuneiform to circular apical pores (Mai and Martinetto, 2006; Tiffney et al., 2018; Manchester et al., 2021) (Figs. S1A–C). Histological structure of the fruits has been studied for several fossil and extant Symplocos species (Yamazaki, 1970; Corner, 1976; Plisko, 1991; Zolkin, 2013; Manchester and Fritsch, 2014). In this study, histological analysis was conducted for a fruit of extant S. paniculata (Figs. 1A and S1D–F).

The Symplocaceae (mainly genus Symplocos) have a rich fossil record of micro- and megafossils (Fig. S2). However, the biogeographic history of Symplocos in Asia remains obscure due to the rarity of reliable fossil records of this genus. Here we recognize three fossil species of Symplocos, including two new species, based on fruits from the late Oligocene and Miocene of Guangxi, South China. The details of geological settings, specimen preparation and applied research methods are provided in Appendix A. The fossils were identified as belonging to Symplocos on the basis of apically truncate woody pyrenes that possess 1–3 apical germination pores and seed locules, and a central vascular canal. The late Oligocene species represent the earliest megafossils of Symplocaceae in East Asia. These discoveries enhance our understanding of the diversity and evolution of Symplocos at low latitudes in Asia. Moreover, we used the Biomod2 ensemble species distribution model (SDM) to simulate the changes in the potential distribution of Symplocos in response to climate changes since the late Oligocene and compared the SDM results to the megafossil records of this genus to explore the importance of climate for driving the migration and diversification of Symplocos at low latitudes of Asia.

1. Systematic paleontology

Order: Ericales Bercht. et J. Presl, 1820

Family: Symplocaceae Desf., 1820

Genus: Symplocos Jacq., 1760

(1) Species: Symplocos ampullaris Xu et Jin sp. nov.

Etymology: The specific epithet "ampullaris" refers to the ampullate pyrene shape.

Holotype: NNF362, designated here (Figs. 1B, C and S3A–C).

Other material: NNF363 (Fig. S3D), NNF1003 (Fig. S3E–G, I–L), NNF1004, NNF1005 (Fig. S3H), NNF1008, GP395 (Fig. S4A–C, J–L), GP396 (Fig. S4D–F), GP402 (Fig. S4G–I).

Stratigraphic position and geological age: The Yongning Formation, Nanning Basin (NNF), late Oligocene; the Erzitang Formation, Guiping Basin (GP), Miocene.

Diagnosis: Pyrene ampulliform, with an apical neck bearing a marginal bulge. Apical pit rounded. Pyrene base rounded, basal pit prominent. Surface ornamented with 12–13 longitudinal regular ribs. Pyrene of mature fruits unilocular, central canal laterally shifted.

Description: Pyrenes are ampulliform in shape, circular in transverse section, 2.1–4.7 mm long and 3.0–5.3 mm in equatorial diameter. An apical neck bearing a marginal bulge is about 1 mm high (Figs. S3A, E, I and S4C, F, I, K); the apical pit is rounded, with a diameter of approximately 1–2 mm, the thickness of the edge is 0.3 mm (Figs. S3B, D, F, H and S4A, D, G). The base of the pyrene is rounded with a prominent basal pit coinciding with a longitudinal central vascular canal (Figs. S3C, G and S4B, E, H). The central canal is laterally shifted in some specimens (Figs. S3J, K and S4K, L). Pyrene wall is thin, about 1.5 mm (Figs. S3I–L and S4J–K). The relatively smooth pyrene surface is ornamented with 12–13 longitudinal regular ribs. Remains of an outer pericarp (epicarp and outer zone of mesocarp) are preserved as a thin layer of tissue (Figs. S3I–K and S4K). Pyrenes of mature fruits have a single well-developed ovary locule.

Remarks: Taxonomic remarks and comparison with other species of Symplocos are given in Appendix A.

(2) Species: Symplocos unilocularis Xu et Jin sp. nov.

Etymology: The specific epithet refers to the pyrene with a single locule.

Holotype: NNF483, designated here (Figs. 1F–J and S5A, B, E, I, N–P).

Other material: NNF286, NNF378 (Fig. S5F and J), NNF477, NNF478 (Fig. S5G), NNF479, NNF480, NNF481 (Fig. S5C), NNF482, NNF483, NNF484 (Fig. S5D, H, K), NNF485 (Fig. S5Q–T), NNF486 (Fig. S5L and M), NNF1523, NNF1524.

Stratigraphic position and geological age: The Yongning Formation, Nanning Basin, late Oligocene.

Diagnosis: Pyrenarium ovate. Apical pit wide, lacking a marginal bulge. Fruit base rounded, with a small basal, laterally shifted pit. Surface coarsely rugose, with irregular longitudinal grooves. Fruits unilocular, central canal lacking. Epicarp and outer zone of mesocarp represented by several layers of thin-walled cells. Pyrene composed of 12–14 layers of sclereids. Endocarp consists of one layer of thin-walled cells.

Description: Pyrenaria are slightly flattened, ovate in lateral view (Fig. S5A–D, E, I), widest in basal third, 8.8–11.0 mm long, 4.2–5.4 mm wide, and 3.7–4.9 mm deep; the length to width ratio (L/W) ranges from 1.8 to 2.3. A distinct apical pit is elliptic in outline, without a marginal bulge, and reaches 1/4 to 1/2 of the total fruit diameter (Fig. S5E–H). The pyrenarium base is rounded; a small basal pit is laterally shifted (Fig. S5I–L). The fruit wall is thin, usually less than 0.5 mm (Fig. S5N–P). The outer surface of the pyrenarium is coarsely rugose with irregular shallow grooves running from apex to base (Fig. S5A, D, E, I, K, L). Pyrenes possess one large locule and lack a central vascular canal (Fig. S5M−P). The peripheral zone of the fruit wall (the epicarp and outer zone of the mesocarp) is represented by several layers of thin-walled cells (Fig. S5Q and R), and constitutes about one fourth of the fruit wall thickness. The pyrene is composed of ca. 12–14 layers of sclereids with different outlines, mostly radially-elongated on the periphery and slightly tangentially elongated in the inner zone (Figs. S5S and T). The endocarp is represented by one layer of thin-walled cells (Fig. S5Q).

Remarks: Taxonomic remarks and comparison with other species of Symplocos are given in Appendix A.

(3) Species: Symplocos cf. pseudogregaria Kirchheimer

Specimens: NNF337 (Figs. 1N, O, P and S6A, F, K, Q–S), NNF906, NNF907, NNF909, NNF910, NNF911 (Figs. 1Q and S7), NNF912, NNF913 (Fig. S6B, G, L), NNF915, NNF916, NNF917 (Figs. 1L, M and S6C, H, M), NNF918, NNF919 (Fig. S6D, I, N), NNF921–NNF925, NNF926 (Fig. S6E, J, O). Most of the specimens represent pyrenes of the fruits, however, some specimens (e.g., NNF911, NNF926) preserves fragments of the epicarp and outer zone of the mesocarp on the pyrene surface.

Stratigraphic position and geologic age: The Yongning Formation, Nanning Basin, late Oligocene.

Description: The pyrenes are broadly ellipsoidal and circular in cross section with longitudinally wrinkled surface, truncate apex without a marginal bulge and rounded base with a small pit coinciding with a longitudinal central vascular canal. A distinct apical pit contains three germination pores, each leading to one of three locules separated by radially arranged false septa. The peripheral zone of the fruit wall formed by the epicarp and the outer zone of the mesocarp is represented by several layers of thin-walled cells. The pyrene is composed of more than 20 layers of sclereids with different outlines. The endocarp is represented by one layer of cells with U-shaped thickening of the walls. A more detailed description of Symplocos cf. pseudogregaria Kirchheimer, taxonomic remarks and comparison with other species are provided in Appendix A.

2. Model performance and climatically suitable habitats of Symplocos since the late Oligocene

Among the five algorithms, the RF model had the best performance (TSS = 0.951, ROC = 0.997), followed by GBM, MARS, MaxEnt.Phillips.2, GLM (Fig. S8).

The results obtained for the percent contribution of bioclimatic variables showed that the most important variables affecting the species distributions of Symplocos were BIO1, BIO12, BIO18, BIO6, BIO16, BIO17, BIO4, BIO5, BIO8, BIO2, BIO3, BIO9, BIO15, and BIO19 with importance scores of 0.42, 0.18, 0.13, 0.10, 0.09, 0.08, 0.07, 0.05, 0.05, 0.04, 0.03, 0.03, 0.03, and 0.02, respectively (Fig. S9).

The response curves crafted through the Random Forest (RF) model for Symplocos, reveal profound insights into the nuanced relationships between climatic variables and habitat suitability (Fig. S10). BIO1 exhibits Symplocos habitat suitability spanning a temperature span from −4 ℃ to 24 ℃ within the confines of the 0.6 threshold. Regarding BIO12, habitat suitability is greatest if the precipitation level exceeds 1000 mm, aligning with the above-mentioned threshold. Habitat suitability tends to improve with BIO18 when its value surpasses 325 mm, and BIO6 generally performs better when maintaining a value above −12 ℃, both these observations being pertinent within the confines of the 0.6 threshold. Habitat suitability is also enhanced when BIO16 exceeds 480 mm, and BIO17 exceeds 95 mm, values determined by the 0.6 threshold. Within this same threshold context, BIO4 is best below 1100 mm, BIO5 exceeds 23 ℃, and BIO8 is greater than 10 ℃. The pivotal BIO2 spans from 7 to 14 ℃, BIO3 surpasses 28, and BIO9 is recommended to be above −3 ℃, all at the 0.6 threshold for habitat suitability. BIO15 within the 0.6 threshold ranges from 50 to 105 mm, and BIO19 maintains suitability greater than 0.6 when it is within the interval of 100–550 mm.

The Biomod2 ensemble SDM run for Symplocos (Fig. 1R–W) showed that during the late Oligocene (25 Ma) (Fig. 1R), the climatically suitable habitats with high suitability index (> 0.75) are mostly confined to middle latitudes in the Northern Hemisphere. However, the climate at low latitudes of eastern Asia, especially South China, is also highly suitable for the survival and diversification of this genus. The climatically suitable habitats at low latitudes of Asia further expanded since the Miocene (Fig. 1S–V). At present (Fig. 1W), the most climatically suitable habitats occur in East and Southeastern Asia, eastern Australia, and the Americas, matching the actual distribution of Symplocos. However, there are also highly suitable habitats in Europe and Africa despite the fact that Symplocos is absent in these areas now. The fossil records align with the SDM, from the late Oligocene to the Pliocene, with abundant fossil records from the middle latitudes of Europe, and some records from East Asia and North America. These fossil records are generally located in the projected 'highly suitable' index area.

3. Biogeographic history of Symplocos

All recent studies of the biogeographic history of Symplocos indicate a Eurasian origin of this genus (Wang et al., 2004; Fritsch et al., 2015). On the basis of phylogenetic analysis from DNA sequence data, Wang et al. (2004) inferred an eastern Asian origin for Symplocos with subsequent dispersal to the Americas. This hypothesis was supported by the fact that both first-diverging lineages of Symplocaceae, genus Cordyloblaste and subgenus Palura (Wang et al., 2004; Fritsch et al., 2008), are native to eastern and southeastern Asia. Based on a combination of fossil-calibrated divergence time estimates and ancestral geographical range analyses, Fritsch et al. (2015) inferred a Eurasian origin for crown-node Symplocaceae at ca. 52 Ma, followed by dispersal to North America between 52 and 38 Ma. However, occurrences of the earliest known fruit fossils of Symplocos in the lower Eocene of Europe may indicate a European origin of the genus with subsequent dispersal to eastern Asia and westward migration to North America via the North Atlantic Land Bridge (Manchester and Fritsch, 2014; Fritsch et al., 2015; Tiffney et al., 2018). Based on the closest affinity of the Miocene to Pliocene European species Symplocos incurva to extant Asian species, and its clear distinction from extant Neotropical species, Manchester and Fritsch (2014) assumed that dispersal of Symplocos between Europe and Asia began after closure of the Turgai Strait between Europe and Asia in the Oligocene.

The late Oligocene species of Symplocos from Guangxi described here are the earliest known Asian megafossils of this genus. The occurrence of three different species suggests that Symplocos was already quite diverse in Guangxi at the end of the Oligocene and has subsequently persisted in that region. These findings are consistent with Biomod2 ensemble SDM results, which show that there have been increasing climatically suitable habitats at low latitudes within Asia, including Guangxi, South China, since the late Oligocene (Fig. 1R–W), indicating the vital importance of climate for driving the migration and diversification of Symplocos in Asian low latitudes. The results of the SDM also show that the two most important bioclimatic variables influencing the distribution of Symplocos are BIO1 (Annual mean temperature, ℃) and BIO12 (Annual precipitation, mm). Symplocos exhibits high habitat suitability (≥ 0.6) if the BIO1 ranges from −4 ℃ to 24 ℃ and/or the BIO12 exceeds 1000 mm (Fig. S10). By using the multivariate relation model between dicotyledonous wood anatomical characters and climate parameters established by Wiemann et al. (1998, 1999), Huang (2020) reconstructed quantitatively the paleoclimate of the late Oligocene of the Nanning Basin and the Miocene of the Guiping Basin, Guangxi, with a mean annual temperature (MAT = BIO1) of 13 ℃ and a mean annual precipitation (MAP = BIO12) exceeding 1000 mm (1120 mm and 2050 mm, respectively), which is consistent with the results of the Biomod2 ensemble SDM for Symplocos habitat suitability.

It is worth noting that at least one of the new fossil species from Guangxi, Symplocos unilocularis, closely resembles in fruit morphology and anatomy species of the deciduous subgenus Palura, an early-diverging lineage within Symplocos. Furthermore, three species of Symplocos-type pollen grains closely related to those of the subgenus Palura were recently described from the middle-upper Eocene of the Changchang Basin, Hainan Island, South China based on LM and SEM studies. These pollen grains resemble Symplocos pollen from the upper Eocene of Germany (Haselbach), which most likely also belong to this subgenus (Hofmann et al., 2019). Hence, the basal subgenus Palura presumably had already appeared in South China in the middle-upper Eocene, much earlier than the Turgai Strait closure. Apparently, the Turgai Strait has not always served as a physical barrier to the migration of terrestrial biota (Iakovleva et al., 2001; Iakovleva, 2011). Hence, the similarity between the fossil species of Symplocos described here and some of extinct species from Europe supports the hypothesis of a Eurasian origin of the genus. However, the direction of Symplocos dispersal between Europe and Asia remains unresolved.

A similar biogeographic pattern is revealed for Styrax L. (Styracaceae). Phylogenetic analysis of Styrax based only on DNA data supports its East Asian origin (Fritsch, 2001), while the earliest fossil records of the genus were found in the Eocene of Europe (Chandler, 1961). In addition, the earliest fossil records of many endemic East Asian genera occur in Europe, such as Choerospondias B.L. Burtt & A.W. Hill (Anacardiaceae), and Rehderodendron Hu (Styracaceae), or North America, such as Davidia Baill. (Nyssaceae) and Trochodendron Siebold & Zucc. (Trochodendraceae), indicating that eastern Asia served as a refugium after Oligocene for many taxa that were formerly spread elsewhere in the Northern Hemisphere (Tiffney, 1985; Manchester, 1999; Manchester et al., 2009).

Acknowledgements

This study was supported by the National Natural Science Foundation of China (grant nos. 42072020, 42172015, 41820104002), the research fund from Shenzhen (szbo202407), the State program (No. 123032400066-1 Geological Institute, Russian Academy of Sciences), the research project No 122042700002-6 (Tsitsin Main Botanical Garden, Russian Academy of Sciences), the M.V. Lomonosov Moscow State University theme "Spatial and temporal organization of ecosystems in conditions of environmental changes" and the Development program of the Interdisciplinary Scientific and Educational School of M.V. Lomonosov Moscow State University "Future planet and global environmental change". The authors thank P.S. Iovlev and A.S. Timchenko for the assistance with producing sections of modern Symplocos fruits, S.S. Popova for providing the information and for supplying a copy of paper, Prof. Robert A. Spicer (The Open University, UK) for valuable advice and language improvement.

Data accessibility statement

Extant plant distribution data were generated from the Global Biodiversity Information Facility (GBIF) web portal (http://www.gbif.org/). Current climate data were obtained from WorldClim dataset (version1.4, http://www.worldclim.org/). Data of historical climate change were derived from the HadCM3 simulations downloaded from the BRIDGE Earth System Modelling results server (https://www.paleo.bristol.ac.uk/resources/simulations/).

CRediT authorship contribution statement

Sheng-Lan Xu: Writing – original draft, Visualization, Investigation, Conceptualization. Tatiana Kodrul: Writing – review & editing, Investigation, Formal analysis, Conceptualization. Mikhail S. Romanov: Writing – review & editing, Visualization, Investigation. Alexey V.F. Ch Bobrov: Writing – review & editing, Visualization, Investigation. Natalia Maslova: Writing – review & editing, Visualization. Shu-Feng Li: Writing – review & editing, Methodology, Formal analysis. Qiong-Yao Fu: Investigation, Data curation. Wei-Ye Huang: Software, Methodology, Data curation. Cheng Quan: Writing – review & editing, Resources, Conceptualization. Jian-Hua Jin: Writing – review & editing, Resources, Conceptualization. Lu-Liang Huang: Writing – review & editing, Supervision, Methodology, Formal analysis, Conceptualization.

Declaration of competing interest

The authors have no competing interest to declare.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.pld.2024.09.001.