Evolutionary Trends in Leaf Morphology and Biogeography of Altingiaceae

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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

Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China

University of Chinese Academy of Sciences, Beijing 100049, China

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.

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

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- current taxonomical placement of the fossil species under Liq-

sionally entire in L. gracilipes (Hemsley) Ickert-Bond and J. uidambar. One is the misidentiﬁcation of other palmately-lobed

Wen (Fig. 2K). The regularly serrated margins can be especially taxa as Liquidambar (Fig. 3C, D). For instance, Massalongo

useful in differentiating Liquidambar from Acer and some other (1854, 1858) described leaf fossil species L. tyberina, L. italica,

taxa. In addition, the Altingiaceae species can be divided into L. afﬁne, L. vincianum, L. scarabellianum, and its three varieties

two distinct types by the leaf morphology: palmately 3-5(7)- L. scarabellianum var. truncatum, L. scarabellianum var. sub-

lobed leaves (Fig. 1A-D), and undivided leaves with pinnate cordatum, and L. scarabellianum var. cordatum from the Italian

venation (Fig. 1H–L). This division of Altingiaceae correlates Miocene sediments. All of these placements were corrected to

with its geographical distribution. The lobed lineages are found be Acer or Gossypium according to the conspicuously elevated

in the deciduous broadleaved forests in southeast America, the primary veins, the short secondaries, and more importantly, the

Mediterranean, East Asia, as well as the cloud forests of Cen- entire margins of these trilobate fossil leaves, (Massalongo,

tral America, whereas the undivided-leaved lineages are limited 1854, pl. iii, ﬁg. 5). Another two ﬁve-lobed fossil species, L.

to the evergreen forests in South China and the tropical moun- gracile Lesquereux from the Upper Cretaceous in Wyoming,

tain rainforest in southeast Asia. The Nanling Mountains region USA and L. keijisuzukii Murai from the Japanese Miocene

represents the boundary of the two types, where L. chingii (Met- sediments were corrected to be under Araliaceae (Lesquereux,

calf) Ickert-Bond and J. Wen (Fig. 1E–G) is distributed as the 1878; Hu and Chaney, 1940). There is also misidentiﬁcation that

transitional morphotypes. This modern distribution can be very treated Liquidambar as resembled taxa, such as the tri-lobed

informative in inferring the paleoclimate and the paleoenviron- leaf species Acer fujitogense from the Fujitoge Formation of the

ment where the fossils have been found, especially combined Aizu Basin, should be identical with Liquidambar by its glandu-

with the companion species. Huang and Song (2002) have lar teeth (Suzuki, 1961; Tanai, 1983; Uemura, 1988). The other

demonstrated that Altingiaceae and Carya might have migrated problem has to do with the fossil preservation. Although the

◦

southwards about 10 N from early Paleogene to late Neogene, fossil collection of Altingiaceae is abundant, the conditions for

they are also excellent indicators for the vegetation and climate the preservation of some fossils were not ideal, and some even

change in East Asia (Yamanoi, 1978). poorly preserved without enough evidence for identiﬁcation as

Liquidambar. There still exists some suspicious species (e.g., L.

418 Y.J. Lai et al. / Palaeoworld 27 (2018) 415–422

Fig. 3. Fossil leaves of Altingiaceae and resembling species. (A) Liquidambar europeum, USNM 8544. (B) L. californicum, USNM 8534. (C) L. convexum = Vitis

ﬂorissantella, USNM 407696. (D) L. integrifolius = Sterculia sp., USNM 657. (E–G) L. fontanella, USNM 39146; (F) enlarged lobelet, red arrow – ﬁnely crenate-

serrate, green arrow – glandular-serrate; (G) enlarged leaf base, red arrow – petiole, green arrow – three primary veins. (H) L. miocinica, NIGP 205; (I–L) polymorphic

leaves of L. maomingensis (photographs obtained with permission from Maslova et al., 2015, ﬁgs. 2, 9, 35, 37). Scale bar = 5 cm (except for F, G). (For interpretation

of the references to color in this ﬁgure legend, the reader is referred to the web version of this article.)

goeppertii, L. pseudoprotensa etc.) that need more materials to especially the small and recurved basal lobes, its geologic range

validate their authenticity of taxonomic status. differed from the protean species L. europaeum Al. Braun and

Combining all available data, we propose a possible evo- L. styraciﬂua. During the Upper Eocene, the undivided and pin-

lutionary path leading to the modern diversity in the leaf nate vein lineage expanded into South China, where the fossils

morphology of Altingiaceae (Fig. 4). The ancestral state of leaf of L. maomingensis Maslova et al. (Fig. 3I–L) were collected and

lobation was three-lobed, which is informed by the earliest leaf described (Maslova et al., 2015). The polymorphic leaves includ-

fossil record of L. fontanlla Brown from the Upper Cretaceous in ing both palmately lobed and undivided are similar to the extant

Wyoming, USA (Brown, 1933). The leaves of L. fontanlla were L. chingii (Fig. 1E–G), and the associated infructescences close

triparted with lanceolate lobelets, with the lateral lobe diverging to L. gracilipes and L. siamensis (Craib) Ickert-Bond and J. Wen.

◦

at an angle more than 60 from the middle (Fig. 3E, F). The lobes Coincidentally, the type of trilobate, undivided and transition

are more narrow, longer and restricted at the basal region com- coexists in modern East Asia. So there has sufﬁcient reason to

pared with living Liquidambar. Unfortunately, no more details propose that L. maomingensis is the ancestor of the extant types

of the epidermal or cuticular substance of the leaf remain. But the limited to East Asia with undivided leaf and pinnate venation

numerous fossil leaf fragments permitted to reconstruct an entire lineages. Subsequently, the fossil materials of Liquidambar con-

leaf (Brown, 1933, ﬁg. 1), and therefore justify the assignment tinuously increased from the Neogene, but there are three main

of the trilobated, three strong veins and ﬁnely crenate-serrate species including L. europaeum, L. californicum Lesquereux,

margin leaf fossil to Liquidambar (Fig. 3F, G). The pentalobate and L. miosinica Hu and Chaney (Fig. 3A, B, H) distributed

and the undivided-leaved lineages were both derived from the in Europe, western North America, and East Asia respectively

trilobate ancestor. The trilobate group (e.g., L. miosinica) con- until the modern distribution pattern.

tinued to exist till today mainly in western North America, East Considering the evidence from molecular phylogenetics of

Asia, and Europe. The fossil evidence suggests that Liquidambar Ickert-Bond and Wen (2006) in this family, we found that

migrated to southeastern North America from western North our interpretation of the leaf morphological evolution in Altin-

America at least as early as the Eocene. L. wilcoxianum Berry giaceae not merely non-conﬂict, but also can support each

from the Lower Eocene Wilcox Flora in Tennessee, USA pro- other. The phylogenetic tree (Ickert-Bond and Wen, 2006;

vided the evidence of transitional morphotypes from three-lobed Figs. 1 and 2) shows that the living Altingiaceae can be split

to ﬁve-lobed (Berry, 1930). As to L. wilcoxianum with medium into three lineages: one undisputed group containing pentalobate

palmately ﬁve-lobed leaves, margin with small serrate teeth, species L. styraciﬂua and L. orientalis corresponds with fossil

Y.J. Lai et al. / Palaeoworld 27 (2018) 415–422 419

Fig. 4. A diagram with fossil leaf reconstructions showing the proposed evolutionary paths of leaf morphology in Altingiaceae with the temporal scale. K – Cretaceous;

Pal – Paleocene; Eo – Eocene; Ol – Oligocene; Mio – Miocene; Pli – Pliocene; Q – Quaternary. (Fossil reconstruction illustrations by Shu-Jie Li.)

pentalobate lineage (from trilobate to pentalobate); another con- phic leaved species L. maomingensis including trilobate, entire

taining undivided leaved taxa form Indochina clade, the other and intermediate type, provided strong evidence to explain evo-

clade containing trilobate species L. formosana and L. acalycina lutionary path of the Asia clade. The undivided type evolved

nested in Altingia s.s. is limited in East Asia. But the phyloge- independently due to the moist and warm climate and dominated

netics topology of three clades is a not well-resolved pectinate in Altingiaceae during the Eocene, and continued to present in

(comb-like) tree, especially the Indochina and East Asia lin- subtropical and tropical region of East Asia. The trilobate group

eages including both undivided and trilobate types. If we only only has L. formosana and L. acalycina remaining in the north-

consider the Asia lineage that trilobate species nested in the undi- ern subtropical region of East Asia. More fossil materials and

vided group, the entire leaf as the ancestral state seems more molecular evidence are needed to reveal the true evolutionary

reasonable. But when we expand to the family and outgroup history of Alitngiaceae, but based on current limited evidence,

and/or even to whole Saxifragales, we found that the trilobate we propose that the divided or trilobate leaf is the ancestral state

leaf state exists extensively in the basal (Paeoniaceae) and ter- in this family.

minal (Grossulariaceae) lineages of Saxifragales. Furthermore, The biogeographic history of Altingiaceae is complex. Ickert-

no entire leaved fossil has been assigned to Altingiaceae from Bond and Wen (2006) proposed that Altingiaceae migrated

Late Cretaceous so far. The latest new fossil record — polymor- across both the Bering and North Atlantic land bridges since

420 Y.J. Lai et al. / Palaeoworld 27 (2018) 415–422

Fig. 5. Reconstruction of the biogeographical history of Altingiaceae based on fossil records. Solid lines refer to the formation of the extant distribution, while

dashed lines indicate that Altingiaceae has been extinct in the area. Red lines represent the migration route of the tropical type, and blue lines represent the temperate

type. K – Cretaceous; Pal – Paleocene; Eo – Eocene; Ol – Oligocene; Mio – Miocene. (For interpretation of the references to color in this ﬁgure legend, the reader

is referred to the web version of this article.)

the Cretaceous based on molecular evidence. Focusing on the tribution in North America, the Mediterranean, and East Asia,

local species L. styraciﬂua, Graham (1999) hypothesized that with Southeast Asia becoming the modern center of diversity.

the North America and Central America population split was The earliest leaf and infructescence fossil evidence of Altin-

probably due to the climatic warming and drying during the giaceae suggested that this family probably originated from

late Miocene to the early Pleistocene based on fossil pollen. North America in Upper Cretaceous, which is corresponding

However, Ruiz-Sanchez and Ornelas (2014) suggested that with the estimated stem age of 98.69 Ma (Tank et al., 2015).

Mesoamerican populations originated in southeastern North The fossil evidence also demonstrated that the time for eastern

America, split by the Trans-Mexican Volcanic Belt during Asia and western Europe lineages diverged from North Amer-

the Pliocene to the Quaternary. Unfortunately, we still lack a ica is older than the previous estimates. In this study, we only

full understanding of the history of migration in Altingiaceae. make a reassessment of leaf fossils in Altingiaceae to give a

Therefore, based on the macrofossil and palynological records morphological trend in leaf evolution. For further research, we

(Supplementary Table 1), we propose a reconstruction of the bio- need to combine the additional vegetative and reproductive fos-

geographical history of Altingiaceae (Fig. 5). The earliest fossil sils although they were rarely collected in the same sediments,

records of Altingiaceae are respectively from the western and and resolve the dynamics of the biogeographic diversiﬁcation in

eastern North America in the Late Cretaceous, separated by a the living eastern Asian lineages.

large inland sea. Based on each companion species, the western

Acknowledgments

interior Cretaceous vegetation demonstrated warm temperate or

subtropical habitat (Equisetum, Laurus, Ficus, Cinnamomum,

We are grateful to Drs. Maria Alejandra Gandolfo and Zhi-

Sassafras, Prunus, Salix, Smilax, Liquidambar, etc.), and the

Duan Chen for the constructive discussions and suggestions;

eastern was tropical montane rainforest (Lauraceae, Magno-

Jing-Jing Tang for her valuable assistance in the lab; Drs. Jun

liales, Clusiaceae, Altingiaceae, Iteaceae, Ericaceae, Theaceae,

Wen, Scott L. Wing, Jonathan G. Wingerath, Münir Oztur, Bing

Triuridaceae, Nymphaeales, etc.). Hence we infer that two lin-

Liu, Yao-Wu Xing, Jian Huang, Gong-Le Shi, Chew Ming Yee

eages of Altingiaceae appeared in western and southeastern

and Hans Joachim Gregor for the great help; and the reviewers

North America, representing the subtropical and the tropical

Drs. Zhe-Kun Zhou and Rob Harbert for helpful suggestions.

types respectively during the Late Cretaceous. Altingiaceae

We also thank the herbaria BH, E, NAS, NIGP, NMNH, PE,

reached to the Far East area and the east coast of the Neo-Tethys

and SYS for providing the fossil and herbarium specimens and

Ocean (the modern Middle-East area) at least in the Paleogene.

other related materials used in this study. This work was sup-

In the Eocene, the range of Altingiaceae distribution expanded

ported by the National Natural Science Foundation of China (No:

to East Asia, as far as South China, and western Europe. The

41472010, 41771219) and the Strategic Priority Research Pro-

southeastern North American Altingiaceae migrated to Central

gram of the Chinese Academy of Sciences (No: XDB26030404).

America along the coasts of the Atlantic Ocean and the Gulf of

Mexico. By the Neogene, Altingiaceae had been widespread in

Appendix A. Supplementary data

North America and Eurasia. Triggered by the global cooling and

aridiﬁcation in Central Asia, the Altingiaceae populations in the

Supplementary data associated with this arti-

high latitudes of the Northern Hemisphere continued to decline.

cle can be found, in the online version, at

Their eventual extinction ﬁnally formed the modern disjunct dis- https://doi.org/10.1016/j.palwor.2018.06.002.

Y.J. Lai et al. / Palaeoworld 27 (2018) 415–422 421

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