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Late Miocene occurrence of monogeneric family Oleandraceae from southwest China and its implications on evolution of eupolypods I
Accepted Manuscript Late Miocene occurrence of monogeneric family Oleandraceae from southwest China and its implications on evolution of eupolypods I
San-Ping Xie, Si-Hang Zhang, Tian-Yu Chen, Xian-Chun Zhang, Xu Zeng, Yang Yu PII: DOI: Reference:
S0034-6667(17)30208-7 doi:10.1016/j.revpalbo.2018.05.002 PALBO 3957
To appear in:
Review of Palaeobotany and Palynology
Received date: Revised date: Accepted date:
21 September 2017 9 May 2018 19 May 2018
Please cite this article as: San-Ping Xie, Si-Hang Zhang, Tian-Yu Chen, Xian-Chun Zhang, Xu Zeng, Yang Yu , Late Miocene occurrence of monogeneric family Oleandraceae from southwest China and its implications on evolution of eupolypods I. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Palbo(2017), doi:10.1016/j.revpalbo.2018.05.002
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ACCEPTED MANUSCRIPT Late Miocene occurrence of monogeneric family Oleandraceae from southwest China and its implications on evolution of eupolypods I
San-Ping Xie a, b, *, Si-Hang Zhang a, Tian-Yu Chen a, Xian-Chun Zhang c, Xu Zeng a,
a
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Yang Yu a
Key Laboratory of Mineral Resources in Western China (Gansu Province) and School of Earth Sciences, Lanzhou University, Lanzhou 730000, China
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State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany,
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c
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Geology and Paleontology, CAS, Nanjing 210008, China
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Chinese Academy of Sciences, Beijing 100093, China
* Corresponding author at: Key Laboratory of Mineral Resources in Western China
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(Gansu Province), School of Earth Sciences, and College of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, China.
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E-mail address: [email protected] (S.-P. Xie).
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ACCEPTED MANUSCRIPT ABSTRACT
Yunnan in SW China is a world renowned hotspot for diverse species of vascular plants such as ferns. However, fossil records of the Cenozoic ferns there are insufficient to clarify their phylogeny and historical biogeography from a geological perspective. Among these derived
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ferns, the monogeneric family Oleandraceae, with a pantropic distribution, is natural and distinctive; however, its origin and evolution remains unknown because of the absence of fossil records. In this study, we identified a new fossil species belonging to the genus Oleandra cav. (Oleandraceae s. s.) from the upper Miocene of Yunnan, China based on a detailed comparison of morphologically similar genera and within this genus. Oleandra
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bangmaii sp. n. is characterised by a simple fertile frond with an entire cartilaginous margin. Moreover, the venation system in this genus is unique and comprises a prominent midrib
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along with parallel, closely spaced secondary free veins. The sori are dorsally borne, with round kidney-shaped indusia. It represents the first fossil occurrence of the genus Oleandra
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(Oleandraceae) within its extant distribution, suggesting that its fossil history has been persisted for at least 10 Ma in Asia. Our finding, together with other existing evidence,
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suggests that the crown of eupolypods I (the node including families Oleandraceae, Davalliaceae and Polypodiaceae) has diversified and that the climate and vegetation of
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Keywords
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Yunnan have remained relatively stable since the late Miocene.
eupolypods I; fern; Miocene; Oleandra; Oleandraceae; Yunnan
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ACCEPTED MANUSCRIPT 1. Introduction
China possesses the most diverse lycophytes and ferns in the world with ca. 2,270 species and 178 genera belonging to 40 families (Zhou et al., 2016). Yunnan is a world famous biodiversity hotspot that is ranked first for the diversity of lycophytes
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and ferns with approximately 1,365 species (Zhou et al., 2016). Particularly, there are ca. 414 species of ferns that are endemic to China (with 30.33% in Yunnan alone) and 181 species endemic to Yunnan (43.72% of the total Chinese endemics). However, the origin and evolution of this high diversity in the Chinese ferns from the geological
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perspective, with emphasis on the Yunnan ferns, are little known. Some studies (Jacques et al., 2013; Su et al., 2011; Wen et al., 2013; Wu et al., 2012) have provided
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important clues on the evolution of the Cenozoic ferns in Yunnan; however, available fossil records are insufficient to study the richness of the extant fern diversity
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(Collinson, 2001; Rothwell and Stockey, 2008). Nevertheless, these fossil records can help us to better understand the origin of the large fern diversity in the modern world
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(Huang et al., 2016b).
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The monogeneric family Oleandraceae s. s., comprising 15–20 spp., has a pantropical distribution (Zhang and Hovenkamp, 2013). Previous reports based on
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morphology have suggested that three genera, namely Oleandra Cav. Arthropteris J. Smith, and Psammiosorus C. Christ., should be included in the family Oleandraceae s. l. (Kramer, 1990). However, molecular studies have indicated that this family comprise only one genus (Christenhusz et al., 2011; Smith et al., 2006) and the other two genera are sisters to the tectarioid ferns (Schuettpelz and Pryer, 2008). Phylogenetic analysis based on gene sequencing agrees that the family Oleandraceae
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ACCEPTED MANUSCRIPT comprises only one genus Oleandra, which is sister to the epiphytic Davalliaceae and polygrammoid ferns (Tsutsumi and Kato, 2006). The genus Oleandra (Oleandraceae) was considered to be distinct and natural in its morphology (Nayar et al., 1968); however, its delimitation at the species level is difficult, especially based on their frond morphology. Their high morphological
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similarity within the genus Oleandra leads to the inconsistency at species definition (Hovenkamp and Ho, 2012). Kramer (1990) stated there are ca. 40 spp. within the genus Oleandra, and a monograph is required for a formal subdivision of this genus. Tryon (1997) reduced the American species to four and briefly noted that these
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species also occurred in Africa, Asia, and the Pacific Islands. Tryon (2000) then identified six species in southeast Asia, Australia, and the Pacific regions. Lin (2000)
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confirmed that there are ca. 45 spp. in the world, of which three are in America and three are in Africa respectively, while the others inhabit in Asia and South Pacific
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Islands. Hovenkamp and Ho (2012) reduced the number of Asian species to nine. Schwartsburd et al. (2016) recognized five endemic species and one putative hybrid in
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the Brazilian Atlantic forest. Zhang and Hovenkamp (2013) revealed that there are ca.
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15–20 species in the world, of which five are distributed in China. Despite the obscure species delimitation, fossil records could provide important
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clues for the early evolution of this genus. In this study, a fossil species with distinctive characteristics conforming to the extant genus Oleandra was recognized from the upper Miocene, southwest China. This fossil occurrence represents the only fossil record of the genus so far and is highly informative of its evolutional history, historical biogeography, and palaeoclimate.
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ACCEPTED MANUSCRIPT 2. Materials and methods
2.1. Fossil material One specimen with its counterpart belonging to the family Oleandraceae was collected from an outcrop of the Bangmai Basin belonging to the Linxiang district,
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Lincang City, Yunnan Province. The basin was formed in the Cenozoic era and was deposited with the Miocene coal-bearing strata—the Bangmai formation (Ge and Li, 1999). Detailed lithological description of the strata is provided in Xie et al. (2014) and Liu et al. (2015). According to fossil association data and lithostratigraphy, the
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Bangmai formation occurred during the Late Miocene, which is comparable with that of the Xiaolongtan formation (Guo, 2011; Hu et al., 2009; Jacques et al., 2011a;
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Zhang, 1996). Recent magnetostratigraphic dating of the Xiaolongtan formation has confirmed that it was deposited ca. 12.7–10 Ma (Li et al., 2015b). Therefore, they
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should occurred at similar ages.
The flora of Bangmai was first described by Tao and Chen (1983) mainly based
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on fossil leaves. The detailed research history could consult Xie et al. (2016). Recent
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years' field collection has allowed us to recognize some new fossil taxa, including Citrus (Rutaceae) leaves (Xie et al., 2013), Firmiana (Malvaceae) fruits (Xie et al.,
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2014), Ventilago (Rhamnaceae) samaras (Liu et al., 2015), Albizzia fruits and leaves (Li et al., 2017) and ferns belonging to Polypodiaceae and Davalliaceae (Wen et al., 2013; Xie et al., 2016). For our study, fossil specimens were collected in 2015, carefully exposed in the laboratory, and photographed using a Canon 6D digital camera (Canon Corporation, Tokyo, Japan) fitted with a macro lens (EF 100 mm f/2.8L Macro IS USM). The details of margins and indusia were observed and
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ACCEPTED MANUSCRIPT photographed under a stereomicroscope (Leica S8APO) attached to a camera (Leica DFC295).
2.2. Extant materials Images of extant Oleandra species were directly obtained from the herbarium of
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the Institute of Botany, Chinese Academic of Science (PE) using a Sony DSC-RX100 camera. The details of venation and sori arrangement were observed and photographed under a stereomicroscope attached to a camera (Sony DSC-RX100).
2.3. Terminology
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The descriptive terminology of ferns follows Zhang (2012). The frond venation
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pattern refers to Zhang (2012) and to the leaf architectural manual of angiosperms (Ellis et al., 2009).
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3. Systematics
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Order Polypodiales Link, 1833
Family Oleandraceae Ching ex Pic. Serm., 1965
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Genus Oleandra Cav., 1799
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Species: Oleandra bangmaii sp. nov. San-Ping Xie and Xian-Chun Zhang (Plate I, 1–3; Plate II, 1–5) Holotype: LDGSW2015–1682(a, b) (Plate I, 1, 2). Repository: The Institute of Palaeontology and Stratigraphy, Lanzhou University, Gansu Province, China. Type locality: Bangmai Basin, Lincang City, Yunnan Province, China. Stratigraphic horizon: Bangmai Formation, upper Miocene (ca. 12.7–10 Ma).
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ACCEPTED MANUSCRIPT Etymology: The specific epithet refers to the Bangmai Basin of the Lincang city, Yunnan Province, from where this fern specimen was collected. Diagnosis: Lamina was simple, glabrous, and approximately linear-lanceolate shaped. The margin was cartilaginous and entire with a bit of undulation. Midrib was prominent and deeply grooved on the adaxial surface. Lateral veins were closely
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spaced, parallel to each other, and terminated at the margin with 65º–70º angle toward the midrib and sometimes forked once near the base. The sori were round, dorsally borne close to the midrib, and arranged in a line on either side of the midrib. Indusia were round-reniform shaped.
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Description: The frond was simple, 1.9–2.2 cm wide and more than 7.3 cm long (Plate I, 1–2) with a probable linear-lanceolate shape. The apex and base were not
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preserved (Plate I, 1–2). The margin was smooth, somewhat cartilaginous, and entire with a little undulation (Plate II, 1–3). The midrib of the frond was strong and
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prominent and was deeply grooved on the upper surface (Plate I, 2; Plate II, 4–5). Lateral veins extended from the midrib with a 65º–70º to the margin. They were
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parallel to each other and were closely spaced at approximately 1 mm (Plate I, 3).
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The veins alternatively occurred near the midrib either as single veins or with one bifurcation (Plate I, 3). The sori were round and dorsally borne on the single lateral
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vein (Plate II, 5). They were no more than 1 mm away from the midrib, forming one line on either side of the midrib (Plate I, 3). Indusia were present and were roundreniform shaped, which could be observed from their impressions (Plate II, 4–5).
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ACCEPTED MANUSCRIPT 4. Discussion
4.1. Comparisons with similar genera and within Oleandra The genus Oleandra is very distinctive in morphology and can be easily distinguished from the mass of polypod ferns. Current fossil specimens uncover a
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combination of distinctive characteristics, including a simple entire frond, lateral closely spaced parallel secondary veins, and round sori with round-reniform indusia (Plate II, 4–5), which conform to the extant genus Oleandra (Table 1). We compared the frond morphologies of other similar genera (Table 1), including Elaphoglossum
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(Dryopteridaceae), Coniogramme (Pteridaceae), and Pteris sect. Pteris (Pteridaceae), all of which share similar frond shape, margin type, prominent midrib, and secondary
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veins pattern (Table 1). However, the current fossil could be distinguished from the genus Elaphoglossum by the presence of round-reniform indusia (Plate I, 3) and
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pattern of sori distribution (Table 1). Pteris sect. Pteris, with linear indusia and marginal-lined sori, was different from the genus Oleandra, with contrasting indusia
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shape and sori distribution pattern (Table 1, Plate III, 6–10). The genus Coniogramme
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demonstrates ex-indusiate sori lining the secondary veins, and often forms hydathodes at fine vein tips (Table 1), which is in contrast with the characteristics of the current
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fossil. Thus, the morphological distinctiveness of the fossil specimens allowed us to assign them to the genus Oleandra. Among the genus Oleandra, ca. 15–20 species exhibit a pantropical distribution in the lower latitude (Fig. 1); five of them inhabit in southern China. Their fronds possess identical gross morphology (Plate III, 1–5), and our fossil species resembled all of them in general, except some minor difference. Our fossil species was smaller in frond width (approximately 2 cm) than Chinese extant species (2.5–3.5 cm; average, 3
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ACCEPTED MANUSCRIPT cm). No hair was observed on the surface of the fossil species (Plate I, 3; Plate II, 1– 5) and it seemed to be glabrous as seen in the extant species: O. wallichii (Hook.) Presl (Plate III, 6), O. undulata (Willd.) Ching (Plate III, 7), O. neriiformis Cavanilles (Plate III, 8), O. musifolia (Blume) Presl (Plate III, 9), and O. cumingii Smith (Plate III, 10). The sori in the fossil frond were less than 1 mm away from the midrib (Plate
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II, 4–5), similar to those in other Chinese species (Plate III, 6–8, 10) except O. musifolia (Plate III, 9), in which the distance was a bit further. Considering that the fossil species were from the late Miocene strata, we could not confirm their phylogenic lineages relative to the extant ones, and thus a new fossil species, O.
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bangmaii sp. nov., was proposed based on its frond morphology.
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4.2. diversification and palaeoclimatic implications
Firstly, Oleandra bangmaii presented the only confirmed record of this genus
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thus far, it was considered that this fossil could be a direct ancestral lineage of the extant Oleandra species in Asia and Pacific regions. The current disjunctive
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distribution of the extant Oleandra species in Asia, Africa, and tropical America (Fig.
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1) could be the result of exchange, isolation, and regional extinction. The occurrence of fossil species here in its modern territory (Fig. 1) demonstrated that the fossil
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history of the genus Oleandra in Asia has persisted since the Late Miocene times. Additionally, derived ferns (>80% of the living fern species) were diversified into Cretaceous (Regalado et al., 2017; Schneider et al., 2016), of which, eupolypods, as a more advanced clade, were deduced to occur 116.7 Ma of early Cretaceous (Schuettpelz and Pryer, 2009). Eupolypods has two subclades: eupolypods I and II (Schneider et al., 2004). Eupolypods I were estimated to originate at approximately 98.9 Ma (Schuettpelz and Pryer, 2009) or 93.61 Ma (Schneider et al., 2004), and the crown group of eupolypods I (including Oleandraceae, Davalliaceae and 9
ACCEPTED MANUSCRIPT Polypodiaceae) occurred at approximately 63.6Ma (Schuettpelz and Pryer, 2009) or 47.67 Ma (Schneider et al., 2004) based on molecular estimates (node 1 in Fig. 2). However, in these studies, fossil calibrations in the phylogenic analysis for eupolypods (including eupolypods I and II) were absent because of their poor fossil records (Schneider et al., 2004). Fossil records could provide solid minimum
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constraints on the divergence time. At the family level, the clades Polypodiaceae and Davalliaceae (node 2 in Fig. 2) were suggested to appear at 60.4 Ma, which was long before the occurrence of the first fossil Protodrynaria (van Uffelen, 1991) with affinity to Polypodiaceae (node c in Fig. 2). Reliable Davalliaceae fossil (von
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Ettingshausen, 1885) was reported from the Eocene (node b in Fig. 2) with ca. 44 Ma. This record was also after the phylogenic divergence time. Oleandra fossil frond in
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our study corresponded to an age of ca. 12.7–10 Ma (node a in Fig. 2) and represents the first confirmed macrofossil in the family Oleandraceae s. s., which is consistent
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with the data from molecular studies (Schuettpelz and Pryer, 2009). Recent reports on fern fossils from the Neogene of Yunnan (Jacques et al., 2013;
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Su et al., 2011; Wen et al., 2013; Wu et al., 2012; Xie et al., 2016; Xu et al., 2017)
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have implied that the crown of eupolypods I [including families Oleandraceae (this study), Davalliaceae(Wen et al., 2013), and particularly Polypodiaceae (Jacques et al.,
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2013; Su et al., 2011; Wen et al., 2013; Wu et al., 2012; Xie et al., 2016; Xu et al., 2017)] was already diversified at least from Miocene to present in Yunnan of China, which is consistent with previous estimates based on phylogenic computing (Schuettpelz and Pryer, 2009). Southwest China, such as Yunnan Province, accommodates abundant and diverse extant fern species (Zhang, 2012). Fossil fern occurrences in Yunnan provide good opportunites to investigate not only their evolutionary history but also underlying 10
ACCEPTED MANUSCRIPT paleoclimatic background. The persistence of the crown of eupolypods I in Yunnan since Miocene may be due to the stable climatic conditions of the Yunnan Province throughout the Neogene (Huang et al., 2016a). Previous palaeoclimatic reconstruction (Jacques et al., 2011a; 2011b) indicated that the mean annual precipitation (MAP) of Lincang (fossil locality in this study) was 1213–1394 mm, and mean annual
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temperature (MAT) was 18.5°C–19.0°C in the late Miocene, which are comparable to the modern values (MAP, 1179 mm and MAT, 17.3 °C). Other basins bearing the Neogene ferns in Yunnan (Huang et al., 2016b; Li et al., 2015a; Sun et al., 2011; Zhang et al., 2012) also demonstrate that palaeoclimatic conditions are comparable to
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the current conditions. This result further supports the above hypothesis. Another fact to supporting this hypothesis is the continuous survival of the Drynarioid ferns in
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Yunnan since the late Miocene (Huang et al., 2016a; Wen et al., 2013). The persistence of warm and humid climates throughout the Neogene in Yunnan (Huang
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et al., 2016a) could lead to stable flora composition with diversification of ferns.
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Acknowledgments We thank Hong Li, Lei Wang, Wen-Wen Wen, Yi Yang, Ke-Nan Liu, YunFeng Wang from Lanzhou University for assistance in the fieldwork; Hong-Rui Zhang from the Institute of Botany, CAS helping to imaging the extant ferns. The
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final manuscript was improved according to the suggestions from two anonymous reviewers. This work was supported by National Natural Science Foundation of China (No. 41172021), the Foundation of the State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, CAS (No. 173126) and
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the Fundamental Research Funds for the Central Universities of China (No. lzujbky-
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2017-74).
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China. Review of Palaeobotany and Palynology 172, 1-9. Xie, S.P., Li, B.K., Zhang, S.H., Shao, Y., Wu, J.Y., Sun, B.N., 2016. First megafossil
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record of Neolepisorus (Polypodiaceae) from the late Miocene of Yunnan, Southwest China. PalZ 90, 413-423.
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Xie, S.P., Manchester, S.R., Liu, K.N., Wang, Y.F., Shao, Y., 2014. Firmiana
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(Malvaceae: Sterculioideae) fruits from the Upper Miocene of Yunnan, Southwest China. Geobios 47, 271-279.
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Xie, S.P., Manchester, S.R., Liu, K.N., Wang, Y.F., Sun, B.N., 2013. Citrus linczangensis sp. n., a leaf fossil of Rutaceae from the late Miocene of Yunnan, China. International Journal of Plant Sciences 174, 1201-1207. Xu, C.L., Huang, J., Su, T., Zhang, X.C., Li, S.F., Zhou, Z.K., 2017. The first megafossil record of Goniophlebium (Polypodiaceae) from the Middle Miocene of Asia and its paleoecological implications. Palaeoworld 26, 543-552.
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ACCEPTED MANUSCRIPT Zhang, Q.-Q., Ferguson, D.K., Mosbrugger, V., Wang, Y.-F., Li, C.-S., 2012. Vegetation and climatic changes of SW China in response to the uplift of Tibetan Plateau. Palaeogeography, Palaeoclimatology, Palaeoecology 363, 23-36. Zhang, X.C., 2012. Lycophytes and ferns of China. Beijing: Peking University Press (In Chinese).
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Zhang, X.C., Hovenkamp, P.H., 2013. Oleandraceae, in: Wu, Z.Y., Raven, P.H., Hong, D.Y. (Eds.), Flora of China, Vol. 2-3 (Pteridophytes). Beijing & Louis: Science Press & Missouri Botanical Garden Press, 747-748.
Zhang, Y.Z., 1996. The lithostratigraphy of Yunnan Province. Wuhan: China
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University of Geosciences Press (In Chinese).
Zhou, X.L., Zhang, X.C., Sun, J.Q., Yan, Y.H., 2016. Diversity and distribution of
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lycophytes and ferns in China. Biodiversity Science 24, 102-107 (In Chinese with
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English abstract).
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ACCEPTED MANUSCRIPT Table 1. A comparison of selected characteristics between the genus Oleandra and other morphologically similar genera.
Plate I. Oleandra bangmaii sp. n., holotype LDGSW2015-1682 (a, b).
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1 Specimen no. LDGSW2015-1682a showing the gross morphology. Scale=10 mm. 2 Specimen no. LDGSW2015-1682b showing the gross morphology. Scale=10 mm. 3 Close-up of 1 showing sori morphology and the lateral venation; arrows indicate
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round-reniform indusium. Scale=5 mm.
Plate II. Close-up of indusial impressions and cartilaginous margins in Oleandra
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bangmaii.
1–3 arrows indicate the entire, somewhat undulate cartilaginous margin. Scale=0.5
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mm in 1 and 3; scale=0.2 mm in 2.
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4–5 arrows indicate the impressions of round indusia. Scale=1 mm.
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Plate III. The gross morphology of extant Oleandra ferns and close-up of their sori
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and lateral veins.
1 O. wallichii (Hook.) Presl, collection no. 1388, Robert L. Fleming. Barcode: PE01771384, showing the gross morphology. 2 O. undulata (Willd.) Ching, collection no. 10419, W.T. Wang, showing the gross morphology. 3 O. neriiformis Cavanilles = O.pistillaris (Swartz) Christensen, collection no. 1742, Robert L. Fleming, Barcode: PE01771374, showing the gross morphology.
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ACCEPTED MANUSCRIPT 4 O. musifolia (Blume) Presl, collection no. 300, R.C. Ching. Barcode: PE00044958, showing the gross morphology. 5 O. cumingii Smith = O.intermedia Ching, collection no. 05065, B.C. Liu. Barcode: PE01786107, showing the gross morphology. 6 Close-up of 1 showing sori morphology and lateral venation; arrows indicate
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round-reniform indusial.
7 Close-up of 2 showing sori morphology and lateral venation; arrows indicate round-reniform indusial.
8 Close-up of 3 showing sori morphology and lateral venation; arrows indicate
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round-reniform indusial.
round-reniform indusial.
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9 Close-up of 4 showing sori morphology and lateral venation; arrows indicate
10 Close-up of 5 showing sori morphology and lateral venation; arrows indicate
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round-reniform indusial.
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Scale=10 mm in 1–5; scale=5 mm in 6-10.
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Figure 1. The extant distribution of Oleandra species and present fossil occurrence.
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Extant distribution was obtained from the website: http://www.gbif.org/
Figure 2. Estimated ages for molecular phylogeny and emergence of the crown of eupolypods I (including Oleandraceae, Davalliaceae, and Polypodiaceae) in the fossil record.
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ACCEPTED MANUSCRIPT Geologic timescale and subdivisions follow the International Chronostratigraphic Chart (v2017/02); abbreviations: Pa, Palaeocene; Eo, Eocene; Ol, Oligocene; Mi, Miocene; Pl, Pliocene; Q, Quaternary. 1 63.6 Ma, refers to Schuettpelz & Pryer, 2009.
a ca. 12.7–10 Ma, refers to this study. b ca. 44 Ma, refers to von Ettingshausen, 1885.
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c 33.9 Ma, refers to van Uffelen, 1991.
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2 60.4 Ma, refers to Schuettpelz & Pryer, 2009.
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ACCEPTED MANUSCRIPT Table 1 A comparison of selected characteristics between the genus Oleandra and other morphologically similar genera.
orbicu lar, ellipti clanceo late
Pteris sect. Pteris (Pteridacea e)
narro wly linear or lanceo late lanceo late or oblon glanceo late
Texture
Arrange ment of sori
Sori
Indus ia
cartilagi nous
promi nent
simple or 2forked, free
in single row on either side of midrib
indusia te
roun drenif orm
1.26
entire
promi nent
scatted on abaxial surface
exindu siate
absen t
0.83
serrulat e, cartilagi nous
promi nent
free, simple or forked and parallel almost to margin Simple or 2forked, free
herbace ous, papery, or leather y leather y
papery
linear along margin
indusia te
linear
2-7
entire or serrate
herbace ous to papery
along seconda ry veins
exindu siate
absen t
promi nent
vein tips enlarge d formin g hydath odes
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Coniogram me (Pteridacea e)
Lateral veins
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Elaphoglos sum (Dryopterid aceae)
Midri b
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lanceo late to linearlanceo late
Margin
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Oleandra (Oleandrac eae)
Fro nd wid th (cm ) 2.53.5
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Frond shape
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Genus/ or sect.
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Data refer to Zhang & Hovenkamp (2013)
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Highlights First fossil of the family Oleandraceae from late Miocene of Yunnan, SW China
The crown node of eupolypods I diversified since late Miocene in fossil records.
The stable climate in Yunnan since then contributes to ferns persistent surviving.
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Figure 1
Figure 2
San-Ping Xie, Si-Hang Zhang, Tian-Yu Chen, Xian-Chun Zhang, Xu Zeng, Yang Yu PII: DOI: Reference:
S0034-6667(17)30208-7 doi:10.1016/j.revpalbo.2018.05.002 PALBO 3957
To appear in:
Review of Palaeobotany and Palynology
Received date: Revised date: Accepted date:
21 September 2017 9 May 2018 19 May 2018
Please cite this article as: San-Ping Xie, Si-Hang Zhang, Tian-Yu Chen, Xian-Chun Zhang, Xu Zeng, Yang Yu , Late Miocene occurrence of monogeneric family Oleandraceae from southwest China and its implications on evolution of eupolypods I. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Palbo(2017), doi:10.1016/j.revpalbo.2018.05.002
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ACCEPTED MANUSCRIPT Late Miocene occurrence of monogeneric family Oleandraceae from southwest China and its implications on evolution of eupolypods I
San-Ping Xie a, b, *, Si-Hang Zhang a, Tian-Yu Chen a, Xian-Chun Zhang c, Xu Zeng a,
a
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Yang Yu a
Key Laboratory of Mineral Resources in Western China (Gansu Province) and School of Earth Sciences, Lanzhou University, Lanzhou 730000, China
b
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany,
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c
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Geology and Paleontology, CAS, Nanjing 210008, China
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Chinese Academy of Sciences, Beijing 100093, China
* Corresponding author at: Key Laboratory of Mineral Resources in Western China
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(Gansu Province), School of Earth Sciences, and College of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, China.
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E-mail address: [email protected] (S.-P. Xie).
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ACCEPTED MANUSCRIPT ABSTRACT
Yunnan in SW China is a world renowned hotspot for diverse species of vascular plants such as ferns. However, fossil records of the Cenozoic ferns there are insufficient to clarify their phylogeny and historical biogeography from a geological perspective. Among these derived
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ferns, the monogeneric family Oleandraceae, with a pantropic distribution, is natural and distinctive; however, its origin and evolution remains unknown because of the absence of fossil records. In this study, we identified a new fossil species belonging to the genus Oleandra cav. (Oleandraceae s. s.) from the upper Miocene of Yunnan, China based on a detailed comparison of morphologically similar genera and within this genus. Oleandra
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bangmaii sp. n. is characterised by a simple fertile frond with an entire cartilaginous margin. Moreover, the venation system in this genus is unique and comprises a prominent midrib
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along with parallel, closely spaced secondary free veins. The sori are dorsally borne, with round kidney-shaped indusia. It represents the first fossil occurrence of the genus Oleandra
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(Oleandraceae) within its extant distribution, suggesting that its fossil history has been persisted for at least 10 Ma in Asia. Our finding, together with other existing evidence,
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suggests that the crown of eupolypods I (the node including families Oleandraceae, Davalliaceae and Polypodiaceae) has diversified and that the climate and vegetation of
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Keywords
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Yunnan have remained relatively stable since the late Miocene.
eupolypods I; fern; Miocene; Oleandra; Oleandraceae; Yunnan
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ACCEPTED MANUSCRIPT 1. Introduction
China possesses the most diverse lycophytes and ferns in the world with ca. 2,270 species and 178 genera belonging to 40 families (Zhou et al., 2016). Yunnan is a world famous biodiversity hotspot that is ranked first for the diversity of lycophytes
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and ferns with approximately 1,365 species (Zhou et al., 2016). Particularly, there are ca. 414 species of ferns that are endemic to China (with 30.33% in Yunnan alone) and 181 species endemic to Yunnan (43.72% of the total Chinese endemics). However, the origin and evolution of this high diversity in the Chinese ferns from the geological
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perspective, with emphasis on the Yunnan ferns, are little known. Some studies (Jacques et al., 2013; Su et al., 2011; Wen et al., 2013; Wu et al., 2012) have provided
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important clues on the evolution of the Cenozoic ferns in Yunnan; however, available fossil records are insufficient to study the richness of the extant fern diversity
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(Collinson, 2001; Rothwell and Stockey, 2008). Nevertheless, these fossil records can help us to better understand the origin of the large fern diversity in the modern world
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(Huang et al., 2016b).
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The monogeneric family Oleandraceae s. s., comprising 15–20 spp., has a pantropical distribution (Zhang and Hovenkamp, 2013). Previous reports based on
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morphology have suggested that three genera, namely Oleandra Cav. Arthropteris J. Smith, and Psammiosorus C. Christ., should be included in the family Oleandraceae s. l. (Kramer, 1990). However, molecular studies have indicated that this family comprise only one genus (Christenhusz et al., 2011; Smith et al., 2006) and the other two genera are sisters to the tectarioid ferns (Schuettpelz and Pryer, 2008). Phylogenetic analysis based on gene sequencing agrees that the family Oleandraceae
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ACCEPTED MANUSCRIPT comprises only one genus Oleandra, which is sister to the epiphytic Davalliaceae and polygrammoid ferns (Tsutsumi and Kato, 2006). The genus Oleandra (Oleandraceae) was considered to be distinct and natural in its morphology (Nayar et al., 1968); however, its delimitation at the species level is difficult, especially based on their frond morphology. Their high morphological
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similarity within the genus Oleandra leads to the inconsistency at species definition (Hovenkamp and Ho, 2012). Kramer (1990) stated there are ca. 40 spp. within the genus Oleandra, and a monograph is required for a formal subdivision of this genus. Tryon (1997) reduced the American species to four and briefly noted that these
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species also occurred in Africa, Asia, and the Pacific Islands. Tryon (2000) then identified six species in southeast Asia, Australia, and the Pacific regions. Lin (2000)
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confirmed that there are ca. 45 spp. in the world, of which three are in America and three are in Africa respectively, while the others inhabit in Asia and South Pacific
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Islands. Hovenkamp and Ho (2012) reduced the number of Asian species to nine. Schwartsburd et al. (2016) recognized five endemic species and one putative hybrid in
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the Brazilian Atlantic forest. Zhang and Hovenkamp (2013) revealed that there are ca.
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15–20 species in the world, of which five are distributed in China. Despite the obscure species delimitation, fossil records could provide important
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clues for the early evolution of this genus. In this study, a fossil species with distinctive characteristics conforming to the extant genus Oleandra was recognized from the upper Miocene, southwest China. This fossil occurrence represents the only fossil record of the genus so far and is highly informative of its evolutional history, historical biogeography, and palaeoclimate.
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ACCEPTED MANUSCRIPT 2. Materials and methods
2.1. Fossil material One specimen with its counterpart belonging to the family Oleandraceae was collected from an outcrop of the Bangmai Basin belonging to the Linxiang district,
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Lincang City, Yunnan Province. The basin was formed in the Cenozoic era and was deposited with the Miocene coal-bearing strata—the Bangmai formation (Ge and Li, 1999). Detailed lithological description of the strata is provided in Xie et al. (2014) and Liu et al. (2015). According to fossil association data and lithostratigraphy, the
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Bangmai formation occurred during the Late Miocene, which is comparable with that of the Xiaolongtan formation (Guo, 2011; Hu et al., 2009; Jacques et al., 2011a;
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Zhang, 1996). Recent magnetostratigraphic dating of the Xiaolongtan formation has confirmed that it was deposited ca. 12.7–10 Ma (Li et al., 2015b). Therefore, they
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should occurred at similar ages.
The flora of Bangmai was first described by Tao and Chen (1983) mainly based
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on fossil leaves. The detailed research history could consult Xie et al. (2016). Recent
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years' field collection has allowed us to recognize some new fossil taxa, including Citrus (Rutaceae) leaves (Xie et al., 2013), Firmiana (Malvaceae) fruits (Xie et al.,
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2014), Ventilago (Rhamnaceae) samaras (Liu et al., 2015), Albizzia fruits and leaves (Li et al., 2017) and ferns belonging to Polypodiaceae and Davalliaceae (Wen et al., 2013; Xie et al., 2016). For our study, fossil specimens were collected in 2015, carefully exposed in the laboratory, and photographed using a Canon 6D digital camera (Canon Corporation, Tokyo, Japan) fitted with a macro lens (EF 100 mm f/2.8L Macro IS USM). The details of margins and indusia were observed and
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ACCEPTED MANUSCRIPT photographed under a stereomicroscope (Leica S8APO) attached to a camera (Leica DFC295).
2.2. Extant materials Images of extant Oleandra species were directly obtained from the herbarium of
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the Institute of Botany, Chinese Academic of Science (PE) using a Sony DSC-RX100 camera. The details of venation and sori arrangement were observed and photographed under a stereomicroscope attached to a camera (Sony DSC-RX100).
2.3. Terminology
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The descriptive terminology of ferns follows Zhang (2012). The frond venation
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pattern refers to Zhang (2012) and to the leaf architectural manual of angiosperms (Ellis et al., 2009).
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3. Systematics
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Order Polypodiales Link, 1833
Family Oleandraceae Ching ex Pic. Serm., 1965
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Genus Oleandra Cav., 1799
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Species: Oleandra bangmaii sp. nov. San-Ping Xie and Xian-Chun Zhang (Plate I, 1–3; Plate II, 1–5) Holotype: LDGSW2015–1682(a, b) (Plate I, 1, 2). Repository: The Institute of Palaeontology and Stratigraphy, Lanzhou University, Gansu Province, China. Type locality: Bangmai Basin, Lincang City, Yunnan Province, China. Stratigraphic horizon: Bangmai Formation, upper Miocene (ca. 12.7–10 Ma).
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ACCEPTED MANUSCRIPT Etymology: The specific epithet refers to the Bangmai Basin of the Lincang city, Yunnan Province, from where this fern specimen was collected. Diagnosis: Lamina was simple, glabrous, and approximately linear-lanceolate shaped. The margin was cartilaginous and entire with a bit of undulation. Midrib was prominent and deeply grooved on the adaxial surface. Lateral veins were closely
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spaced, parallel to each other, and terminated at the margin with 65º–70º angle toward the midrib and sometimes forked once near the base. The sori were round, dorsally borne close to the midrib, and arranged in a line on either side of the midrib. Indusia were round-reniform shaped.
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Description: The frond was simple, 1.9–2.2 cm wide and more than 7.3 cm long (Plate I, 1–2) with a probable linear-lanceolate shape. The apex and base were not
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preserved (Plate I, 1–2). The margin was smooth, somewhat cartilaginous, and entire with a little undulation (Plate II, 1–3). The midrib of the frond was strong and
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prominent and was deeply grooved on the upper surface (Plate I, 2; Plate II, 4–5). Lateral veins extended from the midrib with a 65º–70º to the margin. They were
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parallel to each other and were closely spaced at approximately 1 mm (Plate I, 3).
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The veins alternatively occurred near the midrib either as single veins or with one bifurcation (Plate I, 3). The sori were round and dorsally borne on the single lateral
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vein (Plate II, 5). They were no more than 1 mm away from the midrib, forming one line on either side of the midrib (Plate I, 3). Indusia were present and were roundreniform shaped, which could be observed from their impressions (Plate II, 4–5).
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ACCEPTED MANUSCRIPT 4. Discussion
4.1. Comparisons with similar genera and within Oleandra The genus Oleandra is very distinctive in morphology and can be easily distinguished from the mass of polypod ferns. Current fossil specimens uncover a
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combination of distinctive characteristics, including a simple entire frond, lateral closely spaced parallel secondary veins, and round sori with round-reniform indusia (Plate II, 4–5), which conform to the extant genus Oleandra (Table 1). We compared the frond morphologies of other similar genera (Table 1), including Elaphoglossum
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(Dryopteridaceae), Coniogramme (Pteridaceae), and Pteris sect. Pteris (Pteridaceae), all of which share similar frond shape, margin type, prominent midrib, and secondary
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veins pattern (Table 1). However, the current fossil could be distinguished from the genus Elaphoglossum by the presence of round-reniform indusia (Plate I, 3) and
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pattern of sori distribution (Table 1). Pteris sect. Pteris, with linear indusia and marginal-lined sori, was different from the genus Oleandra, with contrasting indusia
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shape and sori distribution pattern (Table 1, Plate III, 6–10). The genus Coniogramme
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demonstrates ex-indusiate sori lining the secondary veins, and often forms hydathodes at fine vein tips (Table 1), which is in contrast with the characteristics of the current
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fossil. Thus, the morphological distinctiveness of the fossil specimens allowed us to assign them to the genus Oleandra. Among the genus Oleandra, ca. 15–20 species exhibit a pantropical distribution in the lower latitude (Fig. 1); five of them inhabit in southern China. Their fronds possess identical gross morphology (Plate III, 1–5), and our fossil species resembled all of them in general, except some minor difference. Our fossil species was smaller in frond width (approximately 2 cm) than Chinese extant species (2.5–3.5 cm; average, 3
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II, 4–5), similar to those in other Chinese species (Plate III, 6–8, 10) except O. musifolia (Plate III, 9), in which the distance was a bit further. Considering that the fossil species were from the late Miocene strata, we could not confirm their phylogenic lineages relative to the extant ones, and thus a new fossil species, O.
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bangmaii sp. nov., was proposed based on its frond morphology.
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4.2. diversification and palaeoclimatic implications
Firstly, Oleandra bangmaii presented the only confirmed record of this genus
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thus far, it was considered that this fossil could be a direct ancestral lineage of the extant Oleandra species in Asia and Pacific regions. The current disjunctive
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distribution of the extant Oleandra species in Asia, Africa, and tropical America (Fig.
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1) could be the result of exchange, isolation, and regional extinction. The occurrence of fossil species here in its modern territory (Fig. 1) demonstrated that the fossil
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history of the genus Oleandra in Asia has persisted since the Late Miocene times. Additionally, derived ferns (>80% of the living fern species) were diversified into Cretaceous (Regalado et al., 2017; Schneider et al., 2016), of which, eupolypods, as a more advanced clade, were deduced to occur 116.7 Ma of early Cretaceous (Schuettpelz and Pryer, 2009). Eupolypods has two subclades: eupolypods I and II (Schneider et al., 2004). Eupolypods I were estimated to originate at approximately 98.9 Ma (Schuettpelz and Pryer, 2009) or 93.61 Ma (Schneider et al., 2004), and the crown group of eupolypods I (including Oleandraceae, Davalliaceae and 9
ACCEPTED MANUSCRIPT Polypodiaceae) occurred at approximately 63.6Ma (Schuettpelz and Pryer, 2009) or 47.67 Ma (Schneider et al., 2004) based on molecular estimates (node 1 in Fig. 2). However, in these studies, fossil calibrations in the phylogenic analysis for eupolypods (including eupolypods I and II) were absent because of their poor fossil records (Schneider et al., 2004). Fossil records could provide solid minimum
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constraints on the divergence time. At the family level, the clades Polypodiaceae and Davalliaceae (node 2 in Fig. 2) were suggested to appear at 60.4 Ma, which was long before the occurrence of the first fossil Protodrynaria (van Uffelen, 1991) with affinity to Polypodiaceae (node c in Fig. 2). Reliable Davalliaceae fossil (von
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Ettingshausen, 1885) was reported from the Eocene (node b in Fig. 2) with ca. 44 Ma. This record was also after the phylogenic divergence time. Oleandra fossil frond in
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our study corresponded to an age of ca. 12.7–10 Ma (node a in Fig. 2) and represents the first confirmed macrofossil in the family Oleandraceae s. s., which is consistent
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with the data from molecular studies (Schuettpelz and Pryer, 2009). Recent reports on fern fossils from the Neogene of Yunnan (Jacques et al., 2013;
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Su et al., 2011; Wen et al., 2013; Wu et al., 2012; Xie et al., 2016; Xu et al., 2017)
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have implied that the crown of eupolypods I [including families Oleandraceae (this study), Davalliaceae(Wen et al., 2013), and particularly Polypodiaceae (Jacques et al.,
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2013; Su et al., 2011; Wen et al., 2013; Wu et al., 2012; Xie et al., 2016; Xu et al., 2017)] was already diversified at least from Miocene to present in Yunnan of China, which is consistent with previous estimates based on phylogenic computing (Schuettpelz and Pryer, 2009). Southwest China, such as Yunnan Province, accommodates abundant and diverse extant fern species (Zhang, 2012). Fossil fern occurrences in Yunnan provide good opportunites to investigate not only their evolutionary history but also underlying 10
ACCEPTED MANUSCRIPT paleoclimatic background. The persistence of the crown of eupolypods I in Yunnan since Miocene may be due to the stable climatic conditions of the Yunnan Province throughout the Neogene (Huang et al., 2016a). Previous palaeoclimatic reconstruction (Jacques et al., 2011a; 2011b) indicated that the mean annual precipitation (MAP) of Lincang (fossil locality in this study) was 1213–1394 mm, and mean annual
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temperature (MAT) was 18.5°C–19.0°C in the late Miocene, which are comparable to the modern values (MAP, 1179 mm and MAT, 17.3 °C). Other basins bearing the Neogene ferns in Yunnan (Huang et al., 2016b; Li et al., 2015a; Sun et al., 2011; Zhang et al., 2012) also demonstrate that palaeoclimatic conditions are comparable to
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the current conditions. This result further supports the above hypothesis. Another fact to supporting this hypothesis is the continuous survival of the Drynarioid ferns in
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Yunnan since the late Miocene (Huang et al., 2016a; Wen et al., 2013). The persistence of warm and humid climates throughout the Neogene in Yunnan (Huang
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et al., 2016a) could lead to stable flora composition with diversification of ferns.
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Acknowledgments We thank Hong Li, Lei Wang, Wen-Wen Wen, Yi Yang, Ke-Nan Liu, YunFeng Wang from Lanzhou University for assistance in the fieldwork; Hong-Rui Zhang from the Institute of Botany, CAS helping to imaging the extant ferns. The
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final manuscript was improved according to the suggestions from two anonymous reviewers. This work was supported by National Natural Science Foundation of China (No. 41172021), the Foundation of the State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, CAS (No. 173126) and
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the Fundamental Research Funds for the Central Universities of China (No. lzujbky-
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2017-74).
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ACCEPTED MANUSCRIPT Table 1. A comparison of selected characteristics between the genus Oleandra and other morphologically similar genera.
Plate I. Oleandra bangmaii sp. n., holotype LDGSW2015-1682 (a, b).
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1 Specimen no. LDGSW2015-1682a showing the gross morphology. Scale=10 mm. 2 Specimen no. LDGSW2015-1682b showing the gross morphology. Scale=10 mm. 3 Close-up of 1 showing sori morphology and the lateral venation; arrows indicate
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round-reniform indusium. Scale=5 mm.
Plate II. Close-up of indusial impressions and cartilaginous margins in Oleandra
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bangmaii.
1–3 arrows indicate the entire, somewhat undulate cartilaginous margin. Scale=0.5
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mm in 1 and 3; scale=0.2 mm in 2.
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4–5 arrows indicate the impressions of round indusia. Scale=1 mm.
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Plate III. The gross morphology of extant Oleandra ferns and close-up of their sori
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and lateral veins.
1 O. wallichii (Hook.) Presl, collection no. 1388, Robert L. Fleming. Barcode: PE01771384, showing the gross morphology. 2 O. undulata (Willd.) Ching, collection no. 10419, W.T. Wang, showing the gross morphology. 3 O. neriiformis Cavanilles = O.pistillaris (Swartz) Christensen, collection no. 1742, Robert L. Fleming, Barcode: PE01771374, showing the gross morphology.
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ACCEPTED MANUSCRIPT 4 O. musifolia (Blume) Presl, collection no. 300, R.C. Ching. Barcode: PE00044958, showing the gross morphology. 5 O. cumingii Smith = O.intermedia Ching, collection no. 05065, B.C. Liu. Barcode: PE01786107, showing the gross morphology. 6 Close-up of 1 showing sori morphology and lateral venation; arrows indicate
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round-reniform indusial.
7 Close-up of 2 showing sori morphology and lateral venation; arrows indicate round-reniform indusial.
8 Close-up of 3 showing sori morphology and lateral venation; arrows indicate
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round-reniform indusial.
round-reniform indusial.
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9 Close-up of 4 showing sori morphology and lateral venation; arrows indicate
10 Close-up of 5 showing sori morphology and lateral venation; arrows indicate
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round-reniform indusial.
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Scale=10 mm in 1–5; scale=5 mm in 6-10.
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Figure 1. The extant distribution of Oleandra species and present fossil occurrence.
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Extant distribution was obtained from the website: http://www.gbif.org/
Figure 2. Estimated ages for molecular phylogeny and emergence of the crown of eupolypods I (including Oleandraceae, Davalliaceae, and Polypodiaceae) in the fossil record.
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ACCEPTED MANUSCRIPT Geologic timescale and subdivisions follow the International Chronostratigraphic Chart (v2017/02); abbreviations: Pa, Palaeocene; Eo, Eocene; Ol, Oligocene; Mi, Miocene; Pl, Pliocene; Q, Quaternary. 1 63.6 Ma, refers to Schuettpelz & Pryer, 2009.
a ca. 12.7–10 Ma, refers to this study. b ca. 44 Ma, refers to von Ettingshausen, 1885.
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c 33.9 Ma, refers to van Uffelen, 1991.
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2 60.4 Ma, refers to Schuettpelz & Pryer, 2009.
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ACCEPTED MANUSCRIPT Table 1 A comparison of selected characteristics between the genus Oleandra and other morphologically similar genera.
orbicu lar, ellipti clanceo late
Pteris sect. Pteris (Pteridacea e)
narro wly linear or lanceo late lanceo late or oblon glanceo late
Texture
Arrange ment of sori
Sori
Indus ia
cartilagi nous
promi nent
simple or 2forked, free
in single row on either side of midrib
indusia te
roun drenif orm
1.26
entire
promi nent
scatted on abaxial surface
exindu siate
absen t
0.83
serrulat e, cartilagi nous
promi nent
free, simple or forked and parallel almost to margin Simple or 2forked, free
herbace ous, papery, or leather y leather y
papery
linear along margin
indusia te
linear
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entire or serrate
herbace ous to papery
along seconda ry veins
exindu siate
absen t
promi nent
vein tips enlarge d formin g hydath odes
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Coniogram me (Pteridacea e)
Lateral veins
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Elaphoglos sum (Dryopterid aceae)
Midri b
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lanceo late to linearlanceo late
Margin
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Oleandra (Oleandrac eae)
Fro nd wid th (cm ) 2.53.5
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Frond shape
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Genus/ or sect.
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Data refer to Zhang & Hovenkamp (2013)
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Highlights First fossil of the family Oleandraceae from late Miocene of Yunnan, SW China
The crown node of eupolypods I diversified since late Miocene in fossil records.
The stable climate in Yunnan since then contributes to ferns persistent surviving.
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Figure 1
Figure 2