1. Introduction

Quercus L., commonly known as oaks, is the largest genus in the beech family Fagaceae. Comprising around 400–600 species, oaks are distributed throughout temperate to tropical regions of the Northern Hemisphere (Nixon, 1997; Manos et al., 1999; Manos and Stanford, 2001; Denk et al., 2017). The subdivision of the genus has been discussed extensively. Here we follow the most recent subdivision of the genus in which Quercus is subdivided into two subgenera: subgenus Quercus (ca. 295 spp., including five sections: Protobalanus, Ponticae, Virentes, Quercus, Lobatae) and subgenus Cerris (ca. 140 spp., including three sections: Cyclobalanopsis, Cerris, Ilex), making eight sections in total (Denk et al., 2017). Among the eight sections, section Cyclobalanopsis has often been treated as a subgenus or genus, but is now recognized as a section within subg. Cerris restricted to East Asia. The other two sections of subg. Cerris are distributed in Europe and northern Africa (Denk et al., 2017). By contrast, the five sections of the subgenus Quercus are largely restricted to the Americas with the exception of two dispersals back to Eurasia: section Ponticae in mountainous areas of north-eastern Turkey and Transcaucasia, western Georgia; and section Quercus that grows in western Eurasia and East Asia (Denk et al., 2017; Manos and Hipp, 2021). The distribution patterns of the eight sections therefore, exhibit a deep biogeographic split (Manos and Hipp, 2021).

The fossil record shows that Quercus was widespread during the Cenozoic. Barrón et al. (2017) systematically reviewed the fossil record of Quercus and claimed that the earliest possible evidence of the genus in Europe was that of Q. subfalcata Friedrich from the late Paleocene of Ménat, France; but however, they agree with other authors (Jones, 1986; Zhou, 1993; Xing et al., 2013) that pre-Paleogene, and perhaps several pre-Eocene possible mega-remains of the genus are generally poorly preserved, lacking critical features required for definitive identification and should therefore be treated with caution. Nevertheless, the earliest unequivocal evidence of Quercus occurs in the middle Eocene of East Asia, represented by leaves and acorns of Cyclobalanopsis naitoi Huzioka from the late middle Eocene (early Bartonian) Ube flora in Southwest Honshu, Japan (Huzioka and Takahashi 1970) and leaves of Q. paleohypargyrea X-Y Liu et J-H Jin, Q. paleolamellosa X-Y Liu et J-H Jin, Q. cf. myrsinifolia Blume, Q. paleoargyrotricha X-Y Liu et J-H Jin and Q. changchangensis X-Y Liu et J-H Jin from the middle Eocene (Lutetian-Bartonian) of Hainan Island, South China (Liu et al., 2020). From the Oligocene through Quaternary, fossil leaves (with and without cuticle), wood, and pollen attributable to Quercus are common in floras of the Northern Hemisphere; however, records of fruits are uncommon in both North America and Eurasia (Barrón et al., 2017), except for a unique occurrence of an acorn from the early Oligocene of Maoming Basin, Guangdong Province, South China (Liu et al., 2019). Acorns are recognized as unequivocal evidence of Quercus in the fossil record (Barrón et al., 2017), although Lithocarpus, Notholithocarpus and some species of Castanopsis also produce acorns. Therefore, more acorns of the genus are needed to investigate the fossil history and evolution of these genera.

Here we report four new fossil species of Quercus section Cyclobalanopsis based on well-preserved mummified acorns and nuts from the late Oligocene Yongning Formation of the Nanning Basin, Guangxi, South China. The acorns and nuts resemble those of the extant species of Q. section Cyclobalanopsis providing strong evidence for evaluating their affinity with extant species and the evolutionary and paleogeographic history of oaks.

2. Materials and methods 2.1. Geological setting

Fossil acorns of Quercus section Cyclobalanopsis discussed herein were recovered from the upper part of Yongning Formation of the Nanning Basin (22°52′50″N, 108°25′2″E) located in Santang Town, Nanning, Guangxi, South China (Fig. 1). The Yongning Formation occurring throughout most of the basin, is subdivided into three parts: lower, middle and upper, based on the lithic facies (Quan et al., 2016). The upper part of the formation yields abundant mummified fossil fruits, including those described here. Its geological age is considered as late Oligocene according to mammal fossil biostratigraphy based on the presence of Heothema nanningensis Zhao and H. youngi Zhao from Wutang, Nanning as well as Anthracotherium changlingensis Zhao from Changlingpo, Nanning (Zhao, 1981, 1983, 1993) and a Tragulidae fossil from the uppermost part of the formation (Quan et al., 2016).

2.2. Specimen preparation

Fossil and extant specimens examined here were photographed using a Zeiss Stereo Discovery V20 stereomicroscope (AxioCam HRc; Carl Zeiss, Göttingen, Germany) in the Museum of Biology, Sun Yat-sen University (Guangzhou, China). Fossil specimens studied here are preserved in a mixture of 50% alcohol and glycerol (50% alcohol: glycerol = 10:1) and held in the Museum of Biology of Sun Yat-sen University, Guangzhou, China.

Specimens NNF-037, NNF-232, NNF-346 and extant Quercus disciformis Chun et Tsiang and Q. bella Chun et Tsiang were scanned using a three-dimensional X-ray microscope (3D-XRM), Zeiss Xradia 520 versa at the micro-CT laboratory at the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (CAS). The specimen was wrapped with plastic wrap for stability without any other handling. Based on the large size of the present specimens, a CCD-based 0.4× objective was used. Scanning was undertaken using a target at 60 kV (power 5 W) and a filter (LE2) for the fossil and extant specimens. To obtain reconstructions and virtual sections, raw data was processed using VGstudio MAX 3.0 software (Volume Graphics, Germany). Images were adjusted uniformly for brightness and contrast using Adobe Photoshop CS5. All the extant specimens mentioned and cited in the text are listed in Table S1.

3. Systematics

Order Fagales

Family Fagaceae

Genus Quercus L. 1753

Subgenus Cerris Oerst.

Section Cyclobalanopsis (Oerst.) Benth. et Hook.

Species Quercus paleodisciformis X.Y. Liu et J.H. Jin sp. nov. (Fig. 2A–P)

Diagnosis Acorn sessile with a cupule covering the base of the nut; cupule shallowly saucer-shaped, recurved, with 7 concentric ring-shaped bracts; bract margins denticulate but apical 2 entire; nut oblate with smooth surface and acuminate apex; nut apex with concentric rings on the visible portion of the perianth, juncture of 2–3 persistent styles and 2–3 transmitting tissues; scar rounded, shallowly concave, the ratio of scar to nut 0.50–0.67, marginal part thicker than central part. Nut wall thick.

Holotype NNF-346.

Paratypes NNF-037, NNF-038, NNF-039, NNF-041, NNF-1515.

Etymology The specific epithet "paleodisciformis" refers to its close similarity to the extant Quercus disciformis Chun et Tsiang.

Description Acorn sessile, up to 21.6 mm high × 34.2 mm wide, with a cupule covering the base of the nut (Fig. 2A); Cupule shallowly saucer-shaped, recurved, 4–4.2 (mean = 4.1) × 23.5–34.2 (mean = 28.9) mm, with 7 bracts in concentric rings (Fig. 2A–G); bract margins denticulate but apical 2 entire, each bract 1.5–2.9 mm wide (Fig. 2C and G); nut oblate, 17–22 (mean = 19.6) × 23–35 (mean = 27.8) mm, with smooth surface and acuminate apex (Fig. 2A, B, E, F, I, J, M and N); apex 3–6 (mean = 4.6) mm long, 4–9 (mean = 5.6) mm in widest part with 4–5 concentric rings on the visible portion of the perianth (2.6 mm in diameter), two to three persistent styles (Fig. 2A, B, D–F, I, J and L) and 2–3 transmitting tissues (Fig. 2H, O and P); scar rounded, shallowly concave, 12–18 (mean = 15.3) mm in diameter, with punctate surface (Fig. 2E, K and M), the ratio of scar to nut 0.5–0.67, marginal part thicker than central part. Nut shell thick, exocarp, thick, 2–2.2 mm, endocarp, thin, 0.6 mm (Fig. 2E, M and N).

Comparison The present fossils can be assigned to Quercus section Cyclobalanopsis based on the concentric ring-shaped bracts, nut apex and scar (Fig. 2A–P). Although some species of Lithocarpus, such as L. cyrtocarpus (Drake) A. Camus, L. gymnocarpus A. Camus, L. harlandii (Hance ex Walpers), and L. silvicolarum (Hance) Chun, also have oblate nuts, the present fossils are distinct from those of Lithocarpus in terms of their edged concave scars and small apices without rings and prominent perianth in Lithocarpus. Our specimens have shallowly saucer-shaped cupules with concentric ring-shaped bracts, the basal 2–3 rings are denticulate, while the apical ones are entire. The cupule is recurved and there are two to three persistent styles on the nut apex with a concave scar with a thicker margin and thinner center, which is most similar to the extant Q. disciformis (Fig. 2Q–X). However, extant Q. disciformis usually has 8–10 ring-shaped bracts, which is more than exhibited by the present fossil species (Fig. 2S). Acorn apices of the present fossils and extant Q. disciformis are different (Fig. 2A, E, I, M, Q and U). The former has an elongate attenuate apex with 4–5 concentric rings, while the latter has a shorter apex with 3 rings (Fig. 2A, D, I, L, Q and T). Although Q. patelliformis Chun also has shallow cupule and oblate nut, it has concentric ring-shaped bracts with the apical rings being entire, while its basal 2–3 rings are dentate and the cupule is unrecurved so distinguishing it from the present fossils (Fig. 2A, C, G). The new fossil species resembles Quercus bella, Q. hui (Craib) Hu and Q. sichourensis (Hu) C.C. Huang et Y.T. Chang in having oblate nuts, but it is distinct from them by its recurved cupule, style numbers, and scar shape (Table 1). Compared with the unique Oligocene fossil fruit of the genus, Q. shangcunensis Liu, Han et Jin from South China (Liu et al., 2019), the present fossil has much a shallower cupule and more rings on the apex of the nut. Given the comparison above, the present specimens are assigned to a new species, Quercus paleodisciformis sp. nov.

Species Quercus paleohui X.Y. Liu et J.H. Jin sp. nov. (Fig. 3A–D)

Diagnosis Nut subglobose with smooth surface and acuminate apex with concentric rings and four persistent styles; scar rounded, deeply concave with elliptical punctate near the scar margin, the ratio of scar to nut 0.40–0.47.

Holotype NNF-143.

Paratypes NNF-040, NNF-1540.

Etymology The specific epithet "paleohui" refers to its close similarity to the extant Quercus hui (Craib) Hu.

Description Nut subglobose, 17–22 (mean = 20.3) mm high × 21–25 (mean = 22.7) mm wide, with smooth surface (Fig. 3A and B); apex acuminate, 2–3 (mean = 2.3) mm long, 4–5 (mean = 4.7) mm in widest part with 5 concentric rings and four persistent styles, each ring 1 mm wide (Fig. 3A, B and D); scar rounded, 9–10 (mean = 9.5) mm in diam., deeply concave (Fig. 3C), the ratio of scar to nut 0.40–0.47.

Comparison The present fossil nuts, having a very typical subglobose shape, a concave scar and an acuminate nut apex with concentric rings on the visible portion of the perianth as well as four persistent styles (Fig. 3A–D), confirm their assignment to Quercus section Cyclobalanopsis. The concave scars of the present fossils are distinguishable from edged concave scars of Lithocarpus. The present fossil specimens exhibit features similar to those of extant Q. bella and Q. hui in regard to their acuminate apices and the numbers of persistent styles (Fig. 3). The present fossils have four persistent styles and both Q. bella and Q. hui also have four persistent styles (Fig. 3D, H, L and P). However, the present nut can be easily distinguished from Q. bella by its scar size and the scar to nut ratio (Table 1). Scars of the present fossil nuts are 9–10 mm in diameter with a small scar to nut size ratio of 0.40–0.47 (Fig. 3C), whereas the scars of Q. bella are larger (10–16 mm in diam) with a larger scar to nut ratio (0.46–0.70) (Fig. 3G; Table 1). However, the nut shape, size and scar characteristics of the present fossil nuts are all within the range displayed by Q. hui whose nuts are 15–20 × 15–25 mm in size and whose scars are 7–10 mm in diam. with a scar to nut ratio of 0.39–0.56 (Table 1). The differences between the present fossils and extant Q. hui are nut shape and scar depth (Fig. 3A, C, M and O). Nuts are subglobose in the present fossils but oblate in Q. hui (Fig. 3A and M). In addition, the scars of the new species are deeper than those of Q. hui (Fig. 3C and O). Therefore, the present fossil is finally assigned to be Quercus paleohui sp. nov., based on its close similarity to the extant Q. hui.

Species Quercus nanningensis X.Y. Liu et J.H. Jin sp. nov. (Fig. 4A–H)

Diagnosis Acorn sessile with a cupule covering half the nut; cupule shallowly bowl-shaped with 8 concentric ring-shaped bracts; bract margins denticulate or entire; nut oblate as high as the depth of cupule, surface smooth, apex depressed with concentric rings on the visible portion of the perianth, juncture of five persistent styles, and five transmitting tissues. Nut wall thick.

Holotype NNF-232.

Paratype NNF-406.

Etymology The specific epithet "nanningensis" recognizes the Nanning Basin, the fossil locality for this new species.

Description Acorn sessile up to 9–11.5 (mean = 10.3) mm high × 14–18 (mean = 16) mm wide, with a cupule covering half the nut (Fig. 4A and B); cupule shallowly bowl-shaped, 7 × 18 mm, with 8 bracts in concentric rings (Fig. 4A); bract margins denticulate or entire, each bract 3 mm wide (Fig. 4C), 1.2 mm thick; nut oblate, 9 × 14 mm, as high as the depth of cupule, surface smooth, apex depressed with concentric rings on the visible portion of the perianth, junction of five persistent styles and five transmitting tissues (Fig. 4A, B and D); nut wall (including exocarp, mesocarp and endocarp) 0.6–1.2 mm thick (Fig. 4E); scar 8.5 mm in diam., 0.9 mm in thick (Fig. 4E).

Comparison The present fossils have typical features of Quercus section Cyclobalanopsis, such as the ringed cup and ringed apex of the nut, so they are confirmed as belonging to the section. Within the section, the degree to which the cupule covers the nut is an important character in specific identification. Cupules of our specimens are shallowly bowl-shaped and cover half the nut with the uncovered part flattened and as high as the cup (Fig. 4A, B, E). Among extant species of section Cyclobalanopsis, our specimens resemble Q. kerrii Craib in that they both have shallowly bowl-shaped cupules covering half the nut, an oblate nut with a depressed apex, 5 styles and a similar number of rings (Fig. 4I–L). However, our specimens have a scar of uniform thickness (Fig. 4E), whereas the extant Q. kerrii has a non-uniform scar with one side very thick and another side much thinner (Fig. 4M). In addition, bract width is different (Fig. 4A, C, I and K). Compared with Q. kerrii, the present fossils have more regular and wider bracts. Although the partly compressed acorn of Q. bella also has similarities with this specimen, the present fossils can be easily distinguished from Q. bella by the numbers of styles (Table 1). CT scanning sections of the nut apex show that our specimens have five transmitting tissues, indicating that it had five styles (Fig. 4G and H), whereas Q. bella only has 3–4 styles (Fig. 3L). Overall, these differences justify the establishment of a new species, Quercus nanningensis sp. nov., referring the Nanning Basin, the fossil locality for this new species.

Species Quercus yongningensis X.Y. Liu et J.H. Jin sp. nov. (Fig. 4N and O)

Diagnosis Acorn sessile ellipsoid, with a cupule covering more than one third of the nut; cupule deeply bowl-shaped with 7 concentric ring-shaped bracts; bract margins denticulate; nut elongated ellipsoid, with multiple longitudinal ridges on the surface, apex rounded with a visible portion of the perianth where the styles join.

Holotype NNF-303.

Paratype NNF-250.

Etymology The specific epithet "yongningensis" recognizes the Yongning Formation of the Nanning Basin, from which the specimens of this new species were collected.

Description Acorn sessile ellipsoid, up to 49 mm high × 27 mm wide, with a cupule covering more than one third of the nut (Fig. 4N); cupule deeply bowl-shaped 19 × 27 mm, with 7 bracts in concentric rings (Fig. 4N and O); bract margins denticulate, each bract 2.5 mm wide (Fig. 4O); nut elongate ellipsoid, 44 × 23 mm, with multiple longitudinal ridges on the surface, apex rounded, 2 mm long and 2 mm wide in the widest part, with a visible portion of the perianth where the styles join (Fig. 4N).

Comparison The present fossils can be assigned to Quercus section Cyclobalanopsis based on the typical concentric ringed cupule. The present fossil acorns are sessile and ellipsoid with a bowl-shaped cupule and an ellipsoid nut, meaning it is similar to the extant Q. neglecta Schottky, Q. blakei Skan, Q. albicaulis Chun et W.C. Ko, Q. kouangsiensis A. Camus and Q. dinghuensis C.C. Huang (Fig. 4N–U; Table 1). However, the present cupules are deeply bowl-shaped and cover more than one third of the nut but do not extend to cover half the nut, making them distinct from those of Q. neglecta and Q. blakei, whcih are saucer-shaped or shallowly bowl-shaped and cover only the base of the nut (Fig. 4R–U). In addition, the cupules of the present fossils are 19 mm high × 27 mm wide and the nuts are 44 × 23 mm, dimensions that are distinctly larger than those of Q. neglecta with cupule and nut sizes of 5–10 × 13–15 (–18) mm and 15–25 × 10–16 mm, respectively, and of Q. blakei, with cupule and nut sizes of 5–10 mm × 20–30 mm and 25–35 × 15–30 mm (Table 1). Moreover, the number of rings on the bracts of our specimens is 7, which is similar to that of the extant Q. blakei (Fig. 4S), but different from that of Q. neglecta which has 4–6 rings (Fig. 4U). The present fossil is distinct from Q. kouangsiensis in terms of the size and extent to which the cupule covers the nut (Table 1). Quercus kouangsiensis specimens have much bigger cupules (ca. 25 × 25–34 mm, ) and nuts (ca. 50 × 25 mm) enclosing more than half of the nut, and more bracts in 8 or 9 rings with dentate margins (Table 1). The present fossil is closest to Q. dinghuensis because of its similar cupule shape and size (ca. 18 × 20–25 mm) enclosing about one third of the nut (Fig. 4N–Q). However, our fossil has 7 rings on the cupule, which is less than Q. dinghuensis, which has 9–11 rings (Fig. 4N, P; Table 1). In addition, the nut of our fossil is 44 mm high and 23 mm wide, which is much larger than Q. dinghuensis (30–35 × 17–20 mm) (Table 1). Moreover, the present fossil differs from Q. dinghuensis in terms of the thickness of its cupule wall, which is 1 mm in the former but 4 mm and hard in the latter. Compared with the fossil Q. shangcunensis (Liu et al., 2019), the present fossils have more elongate acorns. Therefore, the present specimens are assigned as a new species, Quercus yongningensis sp. nov. recognizing the Yongning Formation of the Nanning Basin, from which the specimens of this new species were collected.

4. Discussion 4.1. Taxonomic comparisons

Within the family Fagaceae, the cup-like cupule only occurs in Quercus, Lithocarpus, Notholithocarpus, and the Castanopsis "fissa" group. Among these genera, the ring-like bracts on the cupule wall occur in Quercus section Cyclobalanopsis, a few species of Lithocarpus (such as Lithocarpus cf. cautleyanua (King) Rehder, L. lucidus (Roxb.) Rehder, L. sericobalanus E.F. Warb., L. lamponga Rehder; Liu et al., 2019) and the Castanopsis "fissa" group [such as C. cerebrina (Hickel et A. Camus) Barnett, C. calathiformis (Skan) Rehder et E.H. Wilson, C. fissa (Champion ex Bentham) Rehder et E.H. Wilson, C. sclerophylla (Lindl. et Paxton) Schottky]. However, in Lithocarpus the ring-like bracts are spirals rather than rings and in Castanopsis these bracts are basally transversely adnate to unparallel rib rings, while those in Q. section Cyclobalanopsis are concentric rings. The present fossil nut apexes usually have rings with big a prominent visible portion of the perianth where the styles join on the top, which is consistent with the diagnosis of Q. section Cyclobalanopsis. In addition, the morphology of the scar formed by detachment of the nut from the cap is also an important feature in distinguishing Quercus from Lithocarpus. The main difference between Quercus and Lithocarpus is mainly on the seed scar. In Quercus, the seed scar does not have a concave edge, but the "acorn" fruit type in Lithocarpus possess such a concave edge of the seed scar. Therefore, combining the cupule and nut characteristics, all the present fossil specimens can be attributed into Q. section Cyclobalanopsis. The acorn morphology is diverse, indicating the central lineage of section Cyclobalanopsis arose no later than the Oligocene and certainly not after the Oligocene, and the distribution ranges of the fossil forms overlap closely with the distribution ranges of the extant species. All this indicates a long-term stable environment from the Late Paleogene to the present.

4.2. Paleogeographical implications

Quercus is subdivided into two subgenera: subgenus Quercus, which is distributed throughout Northern Hemisphere, and subgenus Cerris, which is confined to the Old World (Denk et al., 2017). Quercus, as the largest genus in Fagaceae and throughout the Northern Hemisphere, has the most abundant fossil records. Among these, it is interesting that Quercus section Cyclobalanopsis have a wider distribution range in geological time than in modern times (Fig. 5). The section now is only present in tropical and subtropical Asia, but during the Oligocene and Miocene it occurred in temperate regions of East and West Asia and during the Pliocene extended into Southeast Europe (Bulgaria) (Takhtajan, 1982; Palamarev and Kitanov, 1988; Palamarev and Tsenov, 2004). Quercus simulata Knowlton is common from the Oligocene to the Neogene in both North America and East Asia (Axelrod, 1956; Axelrod, 1992; Axelrod, 1995; WGCPC, 1978). Although it was compared with species belonging to section Cyclobalanopsis (Axelrod, 1956; Graham, 1965; Becker, 1969), its affinity with the section is still uncertain (Barrón et al., 2017). Because of this we excluded it when we investigated the fossil records of Cyclobalanopsis.

In the Eocene, the unequivocal fossil records of the section in the middle Eocene of East Asia are represented by leaves from the middle (Lutetian-Bartonian) South China (Liu et al., 2020), as well as leaves and compressed acorns of Cyclobalanopsis naitoi Huzioka from the late middle Eocene (early Bartonian) Ube flora in Southwest Honshu, Japan (Huzioka and Takahashi 1970) as well as leaves of Quercus scottii (Lesquereux) MacGinitie and Q. nervosum (Wang et Tao) Z.K. Zhou from the late Eocene of the Jianchuan Basin, Yunnan, Southwest China (WGCPC, 1978; Zhou, 1996). The geological age of Jianchuan Basin was considered as Miocene previously by many authors (e.g. WGCPC, 1978; Tao, 2000), however, the coal-bearing Shuanghe Formation within the basin yielding the fossils is now radiometrically dated as 37.2–33.9 Ma (Gourbet et al., 2017). Quercus paleocarpa Manchester from the middle Eocene of Oregon, North America used to be related to section Cyclobalanopsis (Manchester, 1994; Liu et al., 2019; 2020), but this assignment is regarded as ambiguous because the stigma is not preserved (Denk et al., 2017).

In the Oligocene, section Cyclobalanopsis is only present in Asia, including Azerbaijan, Hokkaido, Kitami, Japan, as well as Jinggu, Yunnan and Maoming Basin, Guangdong, Southwest and South China (WGCPC, 1978; Takhtajan, 1982; Tanai, 1995; Liu et al., 2019). In the Miocene, the single occurrence of the section in Europe is reportedly Cyclobalanopsis kryshtofovichii Kolak from Abkhazia (Takhtajan, 1982). Other Miocene occurrences are leaf fossils from Asia, including West Georgia, Hanoi in Vietnam, the Noto Peninsula, Takaya and Northeast Honshu in Japan, and Yunnan, Xizang and Zhejiang in China (Table 2; Colani, 1917; Kryshtofovich, 1926; Huzioka, 1963; Ishida, 1970; WGCPC, 1978; Zhou, 1996; Tao, 2000; Palamarev and Tsenov, 2004; Yabe, 2008; Jia et al., 2009; 2015; Guo, 2011; Xing et al., 2013; Hu et al., 2014; Xu et al., 2016; Barrón et al., 2017). Cyclobalanopsis kryshtofovichii was described based on an incomplete leaf with unclear venation. Therefore, we regard this assignment as suspect and consider that species of section Cyclobalanopsis have only been found in Asia during the Miocene. During the Pliocene, occurrences of the section only occur in subtropical China (Jiangxi, Sichuan and Yunnan; Guo, 1978; Zhang, 1978; Li and Guo, 1982) except for C. stojanovii Palamarev and Kitanov (2004) from Bulgaria. By the Pleistocene, the section is represented in South China and India (Lakhanpal et al., 1976). Barrón et al. (2017) agreed with Jia et al. (2015) that section Cyclobalanopsis has a Paleogene record in mid to low latitude East Asia and western North America, and that it is restricted to Asia during the Neogene. However, based on the paleogeographical records considered above, we recognize that section Cyclobalanopsis first occurred in the middle Eocene of East Asia (Sino-Japan) and has diversified in situ with a few elements scattered into West Asia and southern Europe since the Oligocene and Pliocene, respectively. This suggests that the section might have originated in, and diversified from, East Asia before spreading into West Asia at least by the Oligocene and southern Europe by the Pliocene.

Extant Cyclobalanopsis is mainly distributed in tropical and subtropical areas of Asia where the climate is warm and humid. Southern Europe and West Asia have a mainly Mediterranean climate characterized by drought during summer and rainfall occurring mainly in winter (Escudero et al., 2017), which is not suitable for the biology of members of section Cyclobalanopsis. There are no fossil occurrences beyond the modern distribution range of the section after the Pleistocene (Fig. 5), indicating that the disappearance of the section from southern Europe and West Asia might be related to the appearance of the summer dry Mediterranean climate (Suc, 1984) and climate cooling during the Pleistocene. The occurrence of Quercus section Cyclobalanopsis in the Oligocene of Guangxi, South China, suggests that the section has diversified in its extant distribution center since the Oligocene, which is earlier than the inference based on a comprehensive genomic phylogeny analysis that section Cyclobalanopsis originated at the late Eocene or early Oligocene with fast lineage divergence and demographic changes during the middle to late Neogene (Deng et al., 2018).

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Nos. 41872015, 31770241, 41820104002, and 41661134049), and the grant of the Natural Environment Research Council of Research Councils UK (No. NE/P013805/1). We sincerely thank post-doctoral fellows and graduate students majoring in Ecology and Botany at Sun Yat-sen University for participating in collecting the fossils in the field; Dr. Yi-Gang Song from Shanghai Chenshan Plant Science Research Center (CAS) for providing many acorns of extant species of Quercus section Cyclobalanopsis for comparison, and discussing the identification of the fossils; the staff of the herbaria of Harvard University, Florida Museum of Natural History, South China Botanical Garden, and Sun Yat-sen University for permission to examine and photograph the extant specimens of Fagaceae. We are very grateful to Prof. Robert A. Spicer from Open University and Prof. Steven R. Manchester from Florida Museum of Natural History, University of Florida, USA for their helpful comments and language help, and Ms. Su-Ping Wu from the Experimental Technologies Center of Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, China for her assistance in CT scanning.

Author contributions

XYL, JHJ, and CQ designed the research. HZS, XKW, JHJ and CQ collected the fossil specimens. XYL and JRH photographed fossil and modern specimens. XKW and WYH prepared CT scanning and 3D reconstruction of the fossils. XYL, JHJ, and CQ analyzed and interpreted the results. XYL carried out the data analyses and wrote the manuscript. HZS formatted the references and figures. All authors contributed on drafts and approved the final manuscript.

Declaration of competing interest

There is no conflict of interest.

Appendice A and B. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.pld.2022.08.002