National Science Review BRIEF COMMUNICATION 7: 1765–1767, 2020 doi: 10.1093/nsr/nwaa138 Advance access publication 18 June 2020 Downloaded from https://academic.oup.com/nsr/article/7/11/1765/5859291 by Nanjing Institute of Geology and Palaeontology, CAS user on 14 November 2020

EARTH SCIENCES Middle–Late Jurassic fossils from northeastern China reveal morphological stasis in the catkin-yew Chong Dong1, Gongle Shi 1,∗, Fabiany Herrera2, Yongdong Wang1, Patrick S. Herendeen2 and Peter R. Crane3,4

Te , commonly known as the material includes the terminal portion of but its -bearing structures lack a dis- yews, are widely used in ornamental hor- a leafy shoot with atached seed-bearing tinct stalk. Austrotaxus, and ticulture and are an important source of structures (Fig. 1a and e), and a leafy have seed-bearing structures that chemotherapeutic drugs (e.g. Paclitaxel). shoot with two orders of branching in arise singly from the axil of a normal veg- Te Taxaceae have long been considered which each ultimate shoot has a terminal etative as in the Daohugou fossils, distinct from other , based on conical bud (Fig. 1b and f). Tese fossils but their are helically arranged and their axillary seed-bearing structures (for detailed description and illustration the seed-bearing stalks are very short and that are very diferent from most see Supplementary Data) bear a striking covered by dense scale leaves. cones, consisting of an axis bearing a resemblance to the leafy shoots and seed- A close relationship of the fossil ma- single terminal seed with a feshy aril, bearing structures of extant Amentotaxus terial to extant Amentotaxus is also sup- subtended by several bracts [1]. (Fig. 1c, d and i). ported by phylogenetic analyses based on Phylogenetic analyses based on As in extant Amentotaxus,theleafy morphological characters of living and molecular data recognize the Taxaceae shoots in the Daohugou fossils spread fossil Taxaceae (Supplementary Data). sensu stricto as monophyletic compris- more or less in a single plane; the leaves In an unconstrained analysis (Fig. 1k), ing fve genera [2]. Amentotaxus and are linear-lanceolate and appear to be and also an analysis with the relation- Torreya are sister taxa, and together are borne in two ranks, although they are de- ships of extant Taxaceae constrained to sister to the Taxeae, which comprises cussately inserted (Fig. 1b and f). Te the topology of the most recent molec- Taxus, Pseudotaxus and Austrotaxus. leaves also have a raised mid-vein on ular phylogeny (Fig. 1l), the Daohuguo Cephalotaxus is resolved as sister to Tax- the adaxial surface and two broad lat- fossils are resolved as sister taxa to ex- aceae sensu stricto. Te Taxaceae sensu eral stomatal bands on the abaxial surface. tant Amentotaxus, with Marskea jurassica stricto comprise about 25 extant , In the seed-bearing specimen from Dao- from the Middle Jurassic of Yorkshire, many of which have very restricted hugou, and also in extant Amentotaxus, England [4,5] sister to both. Te clade distributions and small population sizes, each seed is borne singly and erect on a comprising Amentotaxus, the Daohuguo and are endangered in the wild [3]. Fossil short, naked axis that arises in the axil of a fossils and M. jurassica is defned by the evidence of Taxaceae is based mainly on vegetative leaf (Fig. 1g, h and j, and Sup- naked seed stalks that each bear a sin- isolated leaves or leafy shoots for which plementary Fig. 4). Te seed is not visi- gle seed. It would therefore be reasonable the reproductive structures are unknown. ble in the Daohugou fossil, but this is of- to assign the Daohuguo fossils to the ex- However, several more complete fossils ten also the case in extant Amentotaxus, tant genus Amentotaxus, while also recog- with atached seed-bearing structures where the small, immature are of- nizing that there is currently insufcient show that Taxaceae had diverged from ten completely, or almost completely, information on pollen organs and other other conifers by the earliest Jurassic and enclosed by the opposite and decussate structures that could place it unequivo- were probably diverse during the Jurassic bracts (Fig. 1i). In all the features that cally in the crown group of the genus. and Cretaceous [4,5]. are preserved, the fossil material only dif- Te morphological distinctiveness of Here we add to knowledge of early fers from extant Amentotaxus in having Taxaceae has been used to suggest they Taxaceae based on fossils from the late shorter seed-bearing axes. are a separate line of evolution from other Middle–early Late Jurassic Daohugou All other extant genera of Taxaceae conifers[1],butevidencefrommolecular Bed (∼165–158 Ma) in eastern Inner difer from the Daohugou fossils. Tor- phylogenetics [2], as well as other assess- Mongolia, northeastern China [6]. Te reya has opposite to sub-opposite leaves, ments [7], include Taxaceae sensu stricto

C Te Author(s) 2020. Published by Oxford University Press on behalf of China Science Publishing & Media Ltd. Tis is an Open Access article distributed under the terms of the Creative Commons Atribution License (htp://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1766 Natl Sci Rev, 2020, Vol. 7, No. 11 BRIEF COMMUNICATION

ace Downloaded from https://academic.oup.com/nsr/article/7/11/1765/5859291 by Nanjing Institute of Geology and Palaeontology, CAS user on 14 November 2020

bd f

ghij

klCunninghamia konishii Cunninghamia konishii Cephalotaxus oliveri Cephalotaxus oliveri

Torreya taxifolia Torreyeae Torreya taxifolia Torreyeae Amentotaxus argotaenia 72 Amentotaxus argotaenia 64 67 59 Daohugou fossils * Amentotaxeae 61 Daohugou fossils * Amentotaxeae Marskea jurassica * 95 Marskea jurassica *

Taxus cuspidata 86 Taxus cuspidata

54 Pseudotaxus chienii 74 Pseudotaxus chienii Taxeae Taxeae 63 Austrotaxus spicata 70 Austrotaxus spicata Palaeotaxus rediviva * Palaeotaxus rediviva * BRIEF COMMUNICATION Dong et al. 1767

Figure 1. Fossil cf. Amentotaxus, extant Amentotaxus, and phylogenetic relationships of the fossils. (a), (b), (e), (f), (g), (h) and (j) cf. Amentotaxus from the Middle–Late Jurassic Daoguhou Bed in eastern Inner Mongolia, China. (a) Ultimate leafy shoot with attached axillary seed-bearing structures. B0498a (Institute of Vertebrate Paleontology and Paleoanthropology, CAS). (b) Leafy shoot of two orders spreading more or less in a single plane, with oppositely arranged ultimate shoots. PB23120a (Nanjing Institute of Geology and Palaeontology, CAS). (e) Reconstructive drawing of specimen Downloaded from https://academic.oup.com/nsr/article/7/11/1765/5859291 by Nanjing Institute of Geology and Palaeontology, CAS user on 14 November 2020 in (a) based on the part, counterpart and micro-CT volume rendering. (f) Line drawing of the two-order leafy shoot in (b). (g) Middle region of ultimate leafy shoot showing decussate leaves, each subtending a single seed-bearing structure. Counterpart of the specimen in (a). B0498b. (h) Detail of seed-bearing structure showing the short naked axis and decussate bracts subtending the seed. B0498b. (j) Line drawing of individual seed-bearing structure based on (h) showing the short naked axis and decussate bracts subtending and enclosing the terminal seed (see also Supplementary Data). (c), (d) and (i) Extant material of Amentotaxus for comparison. (c) A. yunnanensis, leafy shoot with attached, immature seed-bearing structures. (d) A. argotaenia, leafy shoot showing opposite branching. Herbarium specimen. KUN No. 0763276. (i) A. argotaenia, detail of seed-bearing structure showing immature seed nearly completely enclosed by subtending bracts. Herbarium specimen. NAS00165854. (k) and (l) Phylogenetic analyses of selected species of extant and fossil Taxaceae. Fossil species in bold type and indicated with a star; numbers at nodes indicate bootstrap support values. (k) Strict consensus of 14 most parsimonious (25 steps, consistency index [CI] = 0.72, retention index [RI] = 0.65) from an unconstrained parsimony analysis. (l) Single most parsimonious (26 steps, CI = 0.69, RI = 0.60) from molecular scaffold analysis with relationships of extant species fxed to a backbone based on molecular data [2]. Scale bars: (a), (b), (e) and (f) 1 cm; (d) 2 cm; (g), (h), (i) and (j) 1 mm. plus Cephalotaxus among other conifers Middle Jurassic of Henan, central China Confict of interest statement. None declared. as the sister group to Cupressaceae sensu [10]. Just as the seed-bearing structures lato (Fig. 1l). Te earliest reliable record of Daohugou fossils difer slightly from 1 1,∗ of Taxaceae is Palaeotaxus rediviva from those of extant Amentotaxus species, the Chong Dong , Gongle Shi , 2 1 the Early Jurassic (Hetangian) of south- seed-bearing structures of G. yimaen- Fabiany Herrera , Yongdong Wang , Patrick 2 3,4 ernSweden[4]. sis difer from those of extant Ginkgo S. Herendeen and Peter R. Crane 1 In addition to the Daohugou fossils, biloba [10]. Nevertheless, as in Ginkgo, State Key Laboratory of Palaeobiology and M. jurassica and P. rediviva, there are also the extent of structural stasis between Stratigraphy, Nanjing Institute of Geology and several detached seeds, seed-bearing axes Daohugou fossils and extant species of Palaeontology and Center for Excellence in Life and leafy shoots known from the Jurassic Amentotaxus is striking, and highlights and Paleoenvironment, Chinese Academy of Amentotaxus as a living fossil like Ginkgo Sciences, China; and Cretaceous. Together, these fossils 2 that has undergone litle morphological Chicago Botanic Garden, USA; clearly document that the lineage includ- 3 change since the Middle–Late Jurassic. Oak Spring Garden Foundation, USA and ing the fve extant genera had diverged 4 from other conifers by at least the Early School of Forestry and Environmental Studies, Jurassic and that the Taxaceae were di- Yale University, USA SUPPLEMENTARY DATA ∗Corresponding author. verse during the later Mesozoic. Recog- nition of Amentotaxus in the Daohugou Supplementary data are available at NSR online. E-mail: [email protected] biota, together with M. jurassica, indi- cates that diferentiation of the Amen- totaxeae was already underway by the ACKNOWLEDGEMENTS REFERENCES Middle Jurassic. We thank Xiaolin Wang and Fang Zheng for as- China is rich in species that were sistance with the loan of the Daohugou fossil ma- 1. Florin R. Bot Gaz 1948; 110: 31–9. once more widely distributed across the terial in the Institute of Vertebrate Paleontology 2. Ran J, Shen T and Wang M et al. Proc R Soc B Northern Hemisphere [8]. In most cases, and Paleoanthropology, CAS; Qidong Feng and Biol Sci 2018; 285: 20181012. the credible fossil record of relictual gen- Linbo Jia forprovidingphotographs ofextant Amen- 3. Farjon A. A Handbook of the World’s Conifers, 2nd era such as Craigia (Malvaceae), Davidia totaxus; Z.X. Luo and A.I. Neander for assistance edn. Leiden-Boston: Brill, 2017. (Nyssaceae), Cyclocarya (Juglandaceae) with X-ray tomography; Zhiyan Zhou and Lian- 4. Florin R. Acta Horti Bergiani 1958; 17: 257–402. ming Gao for helpful discussion; and Institute of and Metasequoia (Cupressaceae) extends 5. Harris TM. The Yorkshire Jurassic Flora, V. Botany, Jiangsu Province and CAS, and Kunming back to the early Cenozoic [8].Inafew Coniferales. London: British Museum Natural His- Institute of Botany, CAS, for providing access to ex- tory, 1979. other cases, the reliable fossil record tant material of Amentotaxus. of conifers such as Taiwania (Cupres- 6. Dong C, Yang X and Zhou Z. The . In saceae) and several angiosperm genera, Huang D (ed.). The Daohugou Biota. Shanghai: such as Hedyosmum (Chloranthaceae) FUNDING Shanghai Scientifc & Technical Publishers, 2016, [9], extends back into the Cretaceous. 262–302. However, there are few living genera of Tis work was supported by the National Nat- 7. Harris TM. Rev Palaeobot Palynol 1976; 21: ural Science Foundation of China (41802014, seed plants for which the fossil record 119–34. 41790454, 41688103), the US National Science extends back into the Jurassic, and still 8. Manchester SR, Chen Z and Lu A et al. J Syst Evol Foundation grant DEB-1748286, the Strategic 2009; 47: 1–42. fewer that are well documented based on Priority Research Program (B) of the Chi- details of both leaves and reproductive nese Academy of Sciences (XDB26000000, 9. Friis EM, Crane PR and Pedersen KR. IntJPlant structures. Te most comparable case to XDB18000000), the Youth Innovation Promotion Sci 2019; 180: 232–9. Amentotaxus is Ginkgo, which is well doc- Association, CAS (2017359) and the Oak Spring 10. Zhou Z and Zhang B. Palaeontogr Abt B 1989; 211: umented as Ginkgo yimaensis from the Garden Foundation. 113–33.