Extinct genus Lagokarpos reveals a biogeographic connection between Tibet and other regions in the Northern Hemisphere during the Paleogene

Abstract

The biodiversity history on the Qinghai–Tibetan Plateau (QTP) has remained unclear for a long time. Recent paleobotanical investigations provide opportunities for revealing the phytogeographic history on the QTP in deep time and for testing phylogeographic hypotheses. Lagokarpos is an extinct genus with unknown modern affinities. It is easily distinguished by its fruits, which have two long wings and an elliptical fruit body. Previously, Lagokarpos fossils have only been found from North America and Germany, ranging from the latest Paleogene to early middle Eocene. Recently, we found fossil fruits of this genus from the Niubao Formation, near Bangoin County in the central QTP. A new species, namely Lagokarpos tibetensis H. Tang, T. Su & Z. K. Zhou sp. nov., is described. This is the first fossil record of the genus in Asia. The occurrence of L. tibetensis indicates a close floristic linkage between the QTP and other floras in the Northern Hemisphere during the Paleogene. According to the floristic assemblages, we suggest the central QTP experienced a tropical or subtropical humid climate during that period.

1 Introduction

The Qinghai–Tibetan Plateau (QTP) is the highest plateau in the world, with an average height of 4000–5000 m, its surface area is ca. 2.5 million km² (Zhang et al., 2002). The marginal areas of the QTP, for example, the Himalaya and the Hengduan Mountains, are counted among the most species‐rich regions of the world (Myers et al., 2000). However, the central high desert on the QTP at an altitude of over 4000 m, experiences semi‐arid conditions with some influence from the Southeast Asian Monsoon, receives annual precipitation of approximately 200 mm, and hosts alpine meadow vegetation dominated by Stipa purpurea Grisebach (Ni & Herzschuh, 2011). This predominantly dry landscape is thought by some to be long‐lived, achieving near modern high elevations during the Paleogene, based on isotope data (Rowley & Currie, 2006; Zhang et al., 2012; Ding et al., 2014; Deng & Ding, 2015). However, this view of ancient Tibet suggested by stable isotope paleoaltimetry is somewhat enigmatic when considering the diversity of Tibetan paleobiota as revealed in the fossil record (Deng et al., 2012; Wu et al., 2017).

The biogeographic history of the QTP, especially its connections with other regions in the Northern Hemisphere, is complicated. In the past two decades, hundreds of molecular phylogenetic and biogeographic interpretation works have been proposed based on modern plants from that region (Wen et al., 2014; Renner, 2016), but only a few studies have explored the biogeographic significance of the QTP based on fossil evidence (Deng et al., 2011; Wen et al., 2014). Some hypotheses have been proposed to explain the biogeographic significance of the QTP to the Northern Hemisphere as a whole, such as the “Out of Tibet” concept (Deng et al., 2011), the “Into Tibet” model (Wen et al., 2014), or the QTP serving as a biogeographic barrier for plant diversification in Eurasia. However, all these hypotheses were proposed to explain the connections during the Neogene or Quaternary. Little evidence has been reported exploring the biogeographic significant of the QTP during the Paleogene.

Fortunately, in recent years numerous fossils have been recovered from the QTP. Paleobotanical studies show that many plant species that once existed on the QTP have disappeared from this region (Xu et al., 2016; Wu et al., 2017; Su et al., 2019; Jiang et al., 2019; Xu et al., 2019). This could never be determined by molecular work, but these plant fossils provide us with hard evidence regarding the historical phytogeography of this region (Jia et al., 2019).

Lagokarpos McMurran & Manchester (Fig. 1), is an extinct genus with uncertain modern affinity previously reported by McMurran & Manchester (2010) based on fossil fruits. Previously, it had only been found in western North America and Germany (Messel Pit), with ages ranging from the latest Paleocene to the early middle Eocene (McMurran & Manchester, 2010). Lagokarpos is characterized by fruits with two wings with an appearance similar to that of rabbit ears. Lagokarpos exhibits similar fruit morphology to several extant taxa, such as Gyrocarpus Jacq. (Hernandiaceae), Alberta E. Meyer (Rubiaceae), and even some members of the typical tropical family Dipterocarpaceae. However, evidence is not strong enough to assign it to any one of these taxa using morphological comparison (McMurran & Manchester, 2010).

Figure 1

Lagokarpos . A, E–O, Lagokarpos from Tibet, China. B, Lagokarpos from North America. C, Lagokarpos from Messel Pit (No. S.M.B Me 26455), stored at Senckenberg Forschungsinstitut und Naturmuseum in Frankfurt am Main, Germany. D, Reconstruction of Lagokarpos . E, Fruit body. F, Stripes on the fruit. G, Pinnate veins on the wings. H, Stripe at the base of the fruit. 1, Apex of the fruit. 2, Fruit body. 3, Mid‐vein. 4, Secondary vein. 5, Conical stipe. Scale bar = 0.5 cm (A–C, I, J, O), 0.2 cm (E–H), 1 cm (K–N).

Here we report on well‐preserved fossil fruits of Lagokarpo s, found from the Niubao Formation at a stratigraphic position that we ascribed to the early Eocene based on regional stratigraphy on the central QTP, comprising the first fossil record of this genus in Asia. Together with other fossil records from the Eocene in the western interior of North America and Europe, it reveals the intercontinental floristic linkage between the QTP and other parts of the Northern Hemisphere during the early Paleogene. Moreover, we discuss the paleoclimate conditions in the central QTP based on Lagokarpo s‐bearing floras.

2 Material and Methods

2.1 Geological setting

The fossil samples presented here were excavated from the Jianglang section (31°37.5′N, 90°1.5′E), Niubao Formation near Bangoin County (Tibet Autonomous Region, China) (Fig. 2). The strata (Fig. 3) are mainly composed of brownish red mudstone, siltstone interbedded with grayish green muddy shale, and silty mudstone, representing a fluvial to marginal lacustrine environment (Hetzel et al., 2011; Rowley & Currie, 2006). However, the age of the Niubao Formation is still under debate, ranging from the Late Cretaceous to Oligocene, based on ostracod, insect, palynological, and stratigraphic studies (Xia, 1982; Szwedo et al., 2015; Wang et al., 2019) but we estimate the most likely age is early Eocene.

Figure 2

Lagokarpos fossil locality near Bangoin County (Tibet Autonomous Region, China). A, Digital elevation map of the Tibetan Plateau and its neighboring region showing the main tectonic sutures of Tibet and the location of the Jianglang section. Star, location of the section; triangle, Lunpola Basin. B, Jianglang fossil‐bearing section. Arrows, fossil layers in this fossil‐bearing strata.

Figure 3

Stratigraphic column of the Jianglang fossil‐bearing section, Niubao Formation near Bangoin County (Tibet Autonomous Region, China). This section is composed of several layers of yellowish/brownish mudstone and brownish siltstone, and three layers of argillaceous shale rank at the top part of this section. Plenty of fossil leaves and fruits, including Lagokarpos , are found from the argillaceous shale layers. Fish fossils are found in the lower mudstone layers.

2.2 Morphological observation

All fossil specimens in this study are deposited in the Palaeobotanical Collections, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan, China. Photographs were taken using a Nikon D700 digital camera (Nikon, Tokyo, Japan). Detailed structures of these specimens were observed and photographed using a Leica S8AP0 stereomicroscope (Leica, Wetzlar, Germany). Fossils from Germany are stored at the Senckenberg Forschungsinstitut und Naturmuseum in Frankfurt am Main, Germany. The photographs were provided by Professor Steven Manchester. Fossils from Gainesville, USA (No. FOBU 9835) are stored at the Florida Museum of Natural History in Florida (Gainesville, FL).

Lagokarpos fruits are described following the terminology of McMurran & Manchester (2010). Fruit length was measured from the tip of the longest wing to the point of pedicel attachment on the ovary. Measurements of wing length were taken from the tip of the longest wing to the point of origin. Wing width was measured at the widest point. Fruit body size was represented by its major axis × minor axis. Morphological measurements were made using the software ImageJ version 1.47 (http://rsb.info.nih.gov.ig/). Line‐drawings of the fossil specimens were created using the software Adobe Illustrator CC 2018 (San Jose, CA).

3 Systematics

• Order Unknown
• Family Unknown
• Genus Lagokarpos McMurran & Manchester, 2010
• Species Lagokarpos tibetensis H. Tang, T. Su & Z. K. Zhou sp. nov.
• Holotype XZBGJL1–0383 (Fig. 1A)
• Paratypes XZBGJL5–0793 (Fig. 1K), XZBGJL5–0808 (Fig. 1L).
• Other specimens observed XZBGJL5–0794, XZBGJL5–0795, XZBGJL5–0796, XZBGJL5–0797, XZBGJL5–0801, XZBGJL5–0802, XZBGJL5–0803, XZBGJL5–0804, XZBGJL5–0805, XZBGJL5–0806, XZBGJL5–0810 .
• Repository Palaeobotanical Collections, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan, China.
• Type locality Jianglang section (coordinates: 31.63°N, 90.03°E), Bangoin County, Tibet Autonomous Region, China.
• Etymology The specific epithet, “tibetensis ,” refers to where these fossils were collected.
• Diagnosis Fossil fruits consisting of two elongate V patterned wings arising from the apex of an elliptical fruit body. Wings entire‐margined and pinnate venation patterned.
• Description Fossil fruits consist of two elongate entire‐margined and V patterned wings arising from the apex of an elliptical fruit body (Figs. 1A, 1D, 1J, 1K, 1M, 1N). Symmetrical wings are entire‐margined, obovate, ranging from 3.2 cm to 3.5 cm long and 0.2 cm to 0.4 cm wide. The pinnate venation pattern of the wings consists of a strong midvein (Figs. 1A3, 1G3) with numerous lateral secondary veins (Figs. 1A4, 1G4) and tertiary veins. Decurrent secondary veins arise from the midvein at angles ranging from 5° to 20°. Tertiary veins are exmedially ramified. The fruit body is elliptical, smooth, ranging from 0.95 cm to 1.2 cm long and 0.58 cm to 0.83 cm wide, aspect ratio from 1.5 to 1.7, with several longitudinal ribs on the surface (Fig. 1F). The apex of one fruit shows a rounded bulge (Fig. 1A1) which is connected to the wings, 2.4 mm in diameter and 1.3 mm in height. The basal side of the fruits show a conical stripe (Figs. 1E5, 1H5), 2 mm to 2.5 mm in diameter and 1.1 mm to 1.8 mm in height.

4 Discussion

4.1 Comparison with Lagokarpos from North America and Europe

Compared to L. lacustris (McMurran & Manchester, 2010), the fruit body of L. tibetensis is larger, approximately 1.0 cm to 1.2 cm long and 0.6 cm to 0.8 cm wide (Table 1), whereas the largest fruit body from North America is 1.0 cm long and 0.6 cm wide. There are some stripes on the fruit bodies preserved on L. tibetensis that are not seen on L. lacustris . Moreover, the secondary vein approaches an intersection in an asymptotic manner in the basal direction in our fossil specimens; the angles of the secondary veins with mid‐vein range from 5° to 20°, narrower than those in L. lacustris , which range from 12° to 50°.

Table 1. Comparison of Lagokarpos fruits

	Lagokarpos lacustris	Lagokarpos (Germany)	Lagokarpos tibetensis
Length of wings (mm)	17.0–44.5	26.7	32.0–35.0
Width of wings (mm)	3.0–9.0	5.9	2.0–4.0
Length of fruit body (mm)	3.0–10.0	4.8	10.0–12.0
Width of fruit body (mm)	2.5–6.0	4.1	6.0–8.0
Number of longitudinal lines in fruit body	0	2	0–3
References	McMurran & Manchester, 2010		This study

Only one specimen of Lagokarpos was excavated from the Messel Pit and is not well preserved, but the gross morphology of the fruit clearly assigns it to Lagokarpos . The fruit body of Lagokarpos from the Messel Pit (0.48 cm × 0.41 cm) was smaller than L. tibetensis , more similar to the fossils from North America. A pattern of stripes can also be observed on the fruits. However, more specimens from Messel are expected to be collected to observe better the detailed morphology for identification at species level.

4.2 Floristic affinity of the QTP with other regions of the Northern Hemisphere

Although its systematic affinity is still unresolved, Lagokarpos can provide us with crucial evidence of floristic interchanges between the QTP and the rest of the Northern Hemisphere during the Paleogene. It indicates Paleogene floristic exchange before the formation of high elevations across the whole of the QTP. Recently, more and more fossils with rich records distributed across the Northern Hemisphere, such as Koelreuteria Laxm. (Sapindaceae) (Jiang et al., 2019), Cedrelospermum Saporta (Ulmaceae) (Jia et al., 2019), and Limnobiophylum Krassilov (Araceae) (Wu et al., 2017) have been found in the Upper Oligocene Dingqing Formation in the Lunpola and Nyima basins on the central QTP. These particular fossil genera suggest a close floristic relationship between the QTP and other floras during the Paleogene, implying relatively easy exchange. For example, Cedrelospermum , an extinct fruit genus, was widely distributed in the Northern Hemisphere during the middle Eocene to middle Miocene (Jia et al., 2019).

It is interesting to explore the pathways for the floristic linkage between the QTP, North America, and Europe during the Paleogene. During the early Cenozoic global warming period (late Paleocene–middle Eocene) (Zachos et al., 2008), warm‐temperate vegetation and even tropical elements existed at high latitudes in the Northern Hemisphere and palm and subtropical mangroves were able to expand into latitudes >60°N (Tiffney & Manchester, 2001; Sunderlin et al., 2011; Guillaume et al., 2017). This implied warmth at high latitudes would have made it possible for subtropical and even tropical elements to migrate by way of the North Atlantic Land Bridge (NALB) or the Bering Land Bridge (BLB) (Fig. 4). Based on fossil records, we suggest that Lagokarpos migrated from North America to East Asia and Europe by way of the BLB and NALB (Fig. 4).

Figure 4

Paleographic map of the world during the early Paleogene. This map was revised from the PALEOMAP PaleoAtlas for Gplates (https://www.earthbyte.org/paleomap‐paleoatlas‐for‐gplates/). The red circles on the map show the Lagokarpos fossil localities in North America and the Messel Pit, Germany. Green circle indicates Jianglang near Bangoin city, China. Red lines show the possible dispersal route. BLB, Bering Land Bridge; NALB, North Atlantic Land Bridge.

Previously, based on pollen records, the early Paleogene Northern Hemisphere was divided into two biogeographic regions, one was western North America plus most of Asia, and the other was eastern North America plus Europe (Tiffney, 1985). During the Paleogene, East Asia and Europe were totally separated by the Turgai Strait seaway until its closure in the late Oligocene (Tiffney & Manchester, 2001). However, a close biogeographic linkage between QTP and Europe before the closure of the Turgai Strait seaway is indicated by plant fossils from other sites. Fossil records from the latest Paleocene of the Liuqu conglomerates in southern Tibet share many genera in common with floras in the Northern Hemisphere, especially in Europe, such as the London Clay (Tiffney & Manchester, 2001). This indicates the presence of a Tethys Paleogene evergreen flora in the QTP (Sun & Li, 2003). Moreover, a combined molecular and fossil data analysis based on Malpighiaceae indicates that populations of the family in Asia were dispersed from Europe during the Eocene (Davis et al., 2002).

The finding of L. tibetensis greatly increases the biogeographic significance of plant fossil records from the QTP. It indicates active floral interchanges during the latest Paleocene to early middle Eocene in the Northern Hemisphere, including the QTP. However, plant fossils from the QTP are rare and more fossils of different geological ages and localities from the QTP are urgently needed to decipher the phytogeographic importance of the QTP for the floristic exchanges in the Northern Hemisphere.

4.3 Tropical or subtropical broadleaved forests in central Tibet during the Paleogene

Although the modern affinity of Lagokarpos is unclear, it might have affinities to Gyrocarpus , Alberta , Astronium Jacq. (Anacardiaceae), Triplaris Loefl. (Polygonaceae) and Dipterocarpaceae, which are subtropical and tropical elements. So far, Lagokarpos has only been reported from North America, Messel, and the QTP. Considering the paleoclimate reconstruction work that has been done in relation to fossil localities from North America and Messel, the presence of Lagokarpos (Table 2) could represent a warm and humid subtropical or tropical climate in central Tibet during the late Paleocene to middle Eocene. This is supported by thermochronologic and cosmogenic nuclide data showing that the Eocene red beds of 50–40 million years ago were deposited with a near‐surface temperature of 15–20 °C, in a lowland peneplain that existed in the Bangoin suture zone near our fossil locality (Hetzel et al., 2011).

Table 2. Paleoclimate of Lagokarpos fossil localities

Location	Geologic horizon	Geological age	MAT (°C)	WMMT (°C)	CMMT (°C)	MAP (mm)	P dry (mm)	P wet (mm)	P warm (mm)	Mean relative humidity, %	References
Messel Pit, Germany	Messel Formation	Middle Eocene	16.8–23.9	24.7–27.9	10.6–19.4	803–2540	9–56	175–329	139–154	77–73	Grein et al., 2011
Horsefly, British Columbia, Canada	Horsefly Beds	Early Eocene	~8–13		5	>1000					Jin et al., 2009; Gushulak et al., 2016; Mathewes et al., 2016
Little Mountain, Wyoming, USA	Laney Member, Green River Formation	50 Ma	10.0–12.0								Wilf, 2000

• CMMT, coldest mean month temperature; MAP, mean annual precipitation; MAT, mean annual temperature; P dry, driest mean month precipitation; P warm, warmest mean month precipitation; P wet, wettest mean month precipitation; WMMT, warmest month mean temperature.

5 Conclusion

Well‐preserved fossil fruits of Lagokarpos were found in the Jianglang section, Niubao Formation near Bangoin County, central QTP. This finding is the first fossil record of Lagokarpos in continental Asia and greatly expands the known distribution of Lagokarpos . In comparison with former fossil records from North America and Europe, the new record is defined as a new species, L. tibetensis H. Tang, T. Su & Z. K. Zhou, sp. nov. Based on the fossil history, the occurrence of Lagokarpos on the central QTP suggests the age of the Jianglang section could be latest Paleocene to early middle Eocene. The occurrence of these special extinct fossil fruits of Lagokarpos indicate there were close floristic affinities throughout the Northern Hemisphere, including QTP, facilitated by exchanges by way of the NALB and the BLB. Moreover, this finding indicates subtropical humid environments during the latest Paleocene to middle Eocene.

Acknowledgements

We are grateful to Professor Steven Manchester for the identification and for providing photographs of the fossils. We also thank Professor Volker Mosbrugger and Dr. Stephan Schaal from Senckenberg Research Institute for providing fossil specimen information from the Messel Pit in Germany. Colleagues from the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences (CAS) and Xishuangbanna Tropical Botanical Garden (XTBG), CAS assisted in fossil collection. The Public Technology Service Center, XTBG helped with imaging. This work is supported by the National Natural Science Foundation of China (No. 41661134049), the Strategic Priority Research Program, CAS (Nos. XDA 20070301, XDB26000000, and XDA20070203), the Key Research Program of Frontier Sciences, CAS (No. QYZDB‐SSW‐SMC016), Youth Innovation Promotion Association, CAS (Nos. 2017439 and 2017103), and the CAS 135 program (No. 2017XTBG‐F01). We thank the editor Steven Manchester for numerous constructive suggestions.