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Evolutionary Trends in Leaf Morphology and Biogeography of Altingiaceae

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Evolutionary Trends in Leaf Morphology and Biogeography of Altingiaceae Available online at www.sciencedirect.com ScienceDirect Palaeoworld 27 (2018) 415–422 Evolutionary trends in leaf morphology and biogeography of Altingiaceae based on fossil evidence a,b c a,∗ Yang-Jun Lai , Shu-Jie Li , Wei-Ming Wang a Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China b University of Chinese Academy of Sciences, Beijing 100049, China c Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA Received 26 March 2018; received in revised form 17 May 2018; accepted 27 June 2018 Available online 2 July 2018 Abstract The extant woody family Altingiaceae, consisting of only one genus Liquidambar L. with ca. 15 species, demonstrates a typical disjunctive distribution among East Asia, North America, and the Mediterranean. However, the fossil record throughout the Cenozoic indicates that Altingiaceae was once widespread in the Northern Hemisphere. After studying the abundant Altingiaceae fossil leaf collections, we revised the easily-confused fossil leaves and corrected the misidentifications. Consequently, we proposed an evolutionary history of Altingiaceae leaf morphology in consulting the modern leaf characteristics. It is revealed that the trilobated leaf morphology is the ancestral character state, whereas both the pentalobated and the undivided, pinnate-veined lineages evolved separately. The latter diverged from the trilobated ancestor in South China in Eocene. The lobed and undivided lineages represent the deciduous and evergreen, respectively. An extensive fossil database of Altingiaceae was built to reconstruct its biogeographical history. We reconfirmed that Altingiaceae developed into a temperate and a subtropical-tropical patterns and migrated across both the Bering and North Atlantic land bridges since Cretaceous, independently. It was widespread in the early Neogene of North America and Eurasia, and became extinct in the high latitude triggered by the global cooling and aridification. The modern disjunctive distribution was finally formed, with southeast Asia as its modern diversity center. This study provides new fossil evidence for understanding the morphology and biogeography of the family Altingiaceae. © 2018 Elsevier Ireland Ltd Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier B.V. All rights reserved. Keywords: Altingiaceae; Liquidambar; Leaf morphology; Evolution; Biogeography 1. Introduction than tricolpate in Hamamelidaceae, as well as molecular anal- yses, Liquidambar has been raised to the family rank as Altingiaceae is a woody family with a single genus Liq- Altingiaceae within the Saxifragales in APG system (Chang, uidambar L. and ca. 15 recognized species (Ickert-Bond 1958, 1959, 1964; Qiu et al., 1998; Shi et al., 1998, 2001; and Wen, 2013). Liquidambar consists of Liquidambar sensu Stevens, 2001 onwards; Ickert-Bond et al., 2005, 2007; Ickert- stricto, Altingia Noronha, and Semiliquidambar H.T. Chang Bond and Wen, 2006, 2013). that were treated within the family Hamamelidaceae in the tra- The modern Altingiaceae species are distributed in the ditional system (Harms, 1930; Chang, 1973, 1979; Endress, temperate to tropical montane rainforests of the Northern Hemi- 1989; Zhang et al., 2003). Based on perianth, capitulum inflo- sphere. The temperate and subtropical species, which have rescence/infructescence, highly diverse phyllome structures, 3-5(7)-lobed leaves and persistent phyllomes, are distributed in winged seeds, and pentaporate spheroidal pollen grain rather East Asia (L. formosana Hance and L. acalycina H.T. Chang), the Mediterranean (L. orientalis Miller), and North and Central America (L. styraciflua L.). The subtropical and tropical species with undivided leaves and deciduous phyllomes are limited to ∗ Corresponding author. East Asia (Altingia sensu stricto). In general, the geographi- E-mail addresses: [email protected] (Y.J. Lai), [email protected] (S.J. cal distribution pattern of Altingiaceae is a typical Northern Li), [email protected] (W.M. Wang). https://doi.org/10.1016/j.palwor.2018.06.002 1871-174X/© 2018 Elsevier Ireland Ltd Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier B.V. All rights reserved. 416 Y.J. Lai et al. / Palaeoworld 27 (2018) 415–422 Fig. 1. Leaves of selected extant Altingiaceae species demonstrating the different degrees of leaf lobation among species. (A) Liquidambar formosana, Mao et al. 80, PE. (B) L. acalycina, Qiannandui 2599, PE. (C) L. orientalis, K.H. Rechinger 8550, NMNH. (D) L. styraciflua, Inserillo 15, NYBG. (E-G) L. chingii, Ren-Chang Ching 2244. (H) L. gracilipes, Jun Wen 12048, NMNH. (I) L. siamensis, Anonymous 20961, PE. (J) L. caudata, Anonymous s.n., PE. (K) L. chinensis, C. Wright s.n., NMNH. (L) L. yunnanensis, K.M. Feng 13733, PE. Scale bar = 2 cm. Hemisphere intercontinental disjunction. This distribution pat- leaf shape and entire rather than serrate margin. Addition- tern has provided new insight into understanding the floristics ally, there have been over forty fossil species of Liquidambar of angiosperms in the Northern Hemisphere (Wen, 1999, 2001; described from fossilized leaves (Knowlton, 1919; LaMotte, Ickert-Bond and Wen, 2006; Ruiz-Sanchez and Ornelas, 2014). 1944, 1952; Maslova et al., 2015). Given that so many other The earliest recognizable fossils of Altingiaceae were found taxa have been mistaken as Liquidambar, this number of the in the Upper Cretaceous strata from Wyoming, Oklahoma, and fossil species thus seems doubtful, and further research is highly New Jersey in USA (Brown, 1933; Hedlund, 1966; Zhou et al., necessary to revise and clarify those problematic materials. 2001). The Cenozoic Altingiaceae fossil record is abundant, In this study, we revised the leaf fossil species of Altingiaceae but confines to the Northern Hemisphere. These preservations and proposed a theory on the evolution of the leaf morphol- include leaf compression, fossilized wood, inflorescence, fruit, ogy. Based on our new findings, a biogeographical history of seed, and resin, etc. (Reid and Chandler, 1933; Greguss, 1969; Altingiaceae was reconstructed. Grimaldi et al., 1989; Mai, 1995; Manchester, 1999; Pigg et al., 2004; Taylor et al., 2009; Oskolski et al., 2012; Maslova et al., 2. Material and methods 2015), whereas the pollen grains of pentaporate, spheroidal fea- ture are the most common (Kuprianova, 1960; Graham and The herbarium specimens of extant Altingiaceae species Jarzen, 1969; Muller, 1981; Song et al., 1999). Among these examined in this study are from the herbaria of A, BH, fossils, however, the palmately lobed leaves can be easily mis- BK, F, NAS, NY, PE, SYS, US (abbreviations following taken for the foliage of other resembling groups. For instance, the Index Herbariorum (Thiers, 2012)). The fossil materials fossil leaves of Gossypium, Aralia, Acanthopanax, Acer, Ster- include the type specimens and other fossil specimens from culia, Parthenocissus, and Vitis have all been treated as potential the herbaria of BK, NIGP, SYS, US, and original descriptions. candidates of or even substitute for Liquidambar (Massalongo, The fossil database of Altingiaceae (Supplementary Table 1) 1854, 1858; Lesquereux, 1878; Nathorst, 1883; Kurtz, 1899; was built based on the references and Fossilworks Database MacGinitie, 1941; Suzuki, 1961; Gregor et al., 2006). The (Behrensmeyer and Turner, 2013). Materials were examined inaccurate identifications can mislead our understanding of bio- under Carl Zeiss Stereo Discovery V20 stereo microscope and geography, paleoenvironment, and paleoclimate. For example, photographed with Nikon D300s DSLR camera. The biogeog- Kurtz (1899) identified a palmately lobed fossil leaf from the raphy map was generated with CorelDRAW X7 software. Cerro Baguales Flora, Patagonia, Argentina, as L. integrifolium Lesquereux. This material was once treated as the evidence for 3. Results and discussion Liquidambar record in the Southern Hemisphere and species migration between North and South America in the Late Cre- A study on the herbarium specimens of living Altin- taceous until Berry (1937) suggested this was an erroneous giaceae species leads to the conclusion that leaf characteristics identification. Berry proposed that this leaf fossil belonged to (Figs. 1 and 2) are very important in distinguishing Liquidambar Sterculia (Sterculiaceae) based on the characteristics of round from resembling taxa. This also applies to the fossil leaves Y.J. Lai et al. / Palaeoworld 27 (2018) 415–422 417 Fig. 2. Leaf margins of selected extant Altingiaceae species. (A) Liquidambar obovata, H.Y. Liang 64734, NMNH. (B) L. excels, Hong Wang 5697, PE. (C) L. siamensis, Anonymous 20961, PE. (D) L. chingii, S.K. Lau 4356. (E) L. yunnanensis, K.M. Feng 13733, PE. (F) L. multinervis, B.Q. Zhong 256, PE. (G) L. formosana, Anonymous s.n., CU. (H) L. orientalis, K.H. Rechinger 8550, NMNH. (I) L. acalycina, Qiannandui 2599, PE. (J) L. chinensis, C. Wright s.n., NMNH. (K) L. gracilipes, Jun Wen 12048, NMNH. (L) L. caudata, Anonymous s.n., PE. in Altingiaceae, especially without presence of reproductive In an effort to revise the abundance of the fossil species in organs. In Altingiaceae, the leaves are lanceolate to ovate, Altingiaceae, we checked the original species descriptions and obovate or elliptic, petiolate and leathery-textured. The leaf related specimens, and summarized two main problems in the margins are usually serrate, crenate or glandular-serrate, occa-
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