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Phylogeny and Biogeography of Altingiaceae: Evidence from Combined Analysis of Wve Non-Coding Chloroplast Regions

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Phylogeny and Biogeography of Altingiaceae: Evidence from Combined Analysis of Wve Non-Coding Chloroplast Regions Molecular Phylogenetics and Evolution 39 (2006) 512–528 www.elsevier.com/locate/ympev Phylogeny and biogeography of Altingiaceae: Evidence from combined analysis of Wve non-coding chloroplast regions Stefanie M. Ickert-Bond a,¤, Jun Wen b,c a Field Museum, Department of Botany, 1400 S. Lake Shore Dr., Chicago, IL 60605-2496, USA b Smithsonian Institution, Department of Botany, United States National Herbarium and National Museum of Natural History, MRC-166, P.O. Box 37012, Washington, DC 20013-7012, USA c Laboratory of Systematic and Evolutionary Botany and Herbarium, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, People’s Republic of China Received 31 August 2005; revised 6 December 2005; accepted 7 December 2005 Available online 24 January 2006 Abstract The Altingiaceae consist of »15 species that are disjunctly distributed in Asia and North America. The genus Liquidambar has been employed as a biogeographic model for studying the Northern Hemisphere intercontinental disjunctions. Parsimony and Bayesian analy- ses based on Wve non-coding chloroplast regions support that (1) Liquidambar is paraphyletic; (2) the temperate Liquidambar acalycina and Liquidambar formosana are nested within a large tropical to subtropical Asian clade; (3) Semiliquidambar is scattered in the eastern Asian clade and is of hybrid origin involving at least two maternal species: L. formosana and L. acalycina; and (4) the eastern North American Liquidambar styraciXua groups with the western Asian Liquidambar orientalis, but is highly distinct from other lineages. Bioge- ographically, our results demonstrate the complexity of biogeographic migrations throughout the history of Altingiaceae since the Creta- ceous, with migration across both the Bering and the North Atlantic land bridges. © 2005 Elsevier Inc. All rights reserved. Keywords: Biogeography; Phylogeny; Altingiaceae; Divergence times; Liquidambar; Hamamelidaceae 1. Introduction with the southern populations in Mexico and Central America formerly designated as a separate species, Liquid- Altingiaceae Horan. (the sweet gums) are a family of ambar macrophylla Oersted (Sosa, 1978). Most workers, »15 species in three genera, Liquidambar L., with four to however, recognize only one species in the New World that Wve species, Altingia Noronha, with six to eight species, and exhibits considerable variation in leaf and infructescence Semiliquidambar H.-T. Chang, with »three species. The size (e.g., Meyer, 1993). family shows a classic Asian/North American interconti- Altingiaceae are anemophilous trees with pentaporate nental biogeographic disjunction. The Altingiaceae are pollen, unisexual Xowers that lack a perianth, woody infr- most species rich in Asia, with two genera, Altingia and uctescences, and Xowers with several stamens each aggre- Semiliquidambar endemic to tropical and subtropical Asia. gated into staminate capitula (Ferguson, 1989). The The four species of Liquidambar are disjunctly distributed presence of resin ducts associated with vascular bundles of in eastern Asia (2 spp.), western Asia (1 sp.), and eastern stems, leaves, and Xoral organs is found throughout the North America to Central America (1 sp.). Some controver- Altingiaceae, but is also present in Hamamelidaceae s. str. sies concern the delimitation of Liquidambar styraciXua L., (Bogle, 1986). The Altingiaceae have been discussed exten- sively through studies of pollen morphology (Chang, 1959, X * Corresponding author. Fax: +1 312 665 7158. 1964; Zavada and Dilcher, 1986), oral anatomy (Bogle, E-mail address: [email protected] (S.M. Ickert-Bond). 1986; Wisniewski and Bogle, 1982), wood anatomy 1055-7903/$ - see front matter © 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2005.12.003 S.M. Ickert-Bond, J. Wen / Molecular Phylogenetics and Evolution 39 (2006) 512–528 513 (Greguss, 1959; Huang, 1986; Metcalfe and Chalk, 1950; coriaceous to chartacous and vary widely in size from 5 cm Moll and Janssonius, 1914; Rao and Purkayastha, 1972; in length in A. gracilipes Hemsl. to more than 12cm in A. Reinsch, 1890; Tang, 1943; Tippo, 1938) and relationships yunnanensis Rehder and Wilson. Two sections have been in Hamamelidaceae s. l. (Endress, 1989a,b,c, 1993; Endress recognized: sect. Altingia Noronha, including A. chinensis, and Igersheim, 1999; Endress and Stumpf, 1990). Based on A. obovata, A. yunnanensis, A. poilanei, and A. excelsa, has a gynoecium with two carpels and a stigma with multicellu- large spheroidal heads with numerous fruits, while sect. Oli- lar papillae, Altingiaceae have generally been placed in gocarpa H.-T. Chang, including A. gracilipes and A. siamen- Hamamelidaceae s. l.(Chang, 1973, 1979; Cronquist, 1981; sis has no more than nine fruits per infructescence which is Endress and Igersheim, 1999). Endress (1993) concluded smaller, and hemispheroidal to turbinate in shape (Chang, that the Exbucklandiaceae are a link between the Hamam- 1979; Ferguson, 1989). Morphological analysis of infructes- elidaceae s. str. and Altingiaceae. Similarly, HuVord and cences in this genus is currently underway (S.M. Ickert- Crane (1989) based on a cladistic analysis of morphology Bond, K.B. Pigg, and J. Wen, in prep.) also showed that Exbucklandioideae, Rhodoleioideae, and Semiliquidambar from South and eastern China has Altingioideae form a subclade within Hamamelidaceae s. l. »three species (Figs. 1 and 2): S. cathayensis H.-T. Chang Recent molecular studies have shown this assemblage to be from Fujian, Guangdong, Guangxi, Guizhou, Hainan, and polyphyletic and support recognizing Altingiaceae and Jiangxi, S. caudata H.-T. Chang from Fujian and Zhejiang Hamamelidaceae s. str. as distinct families in the Saxifra- provinces, and S. chingii (Metcalf) H.-T. Chang from gales within a larger rosid clade (APG, 2003; Chase et al., Fujian, Guangdong, and Jiangxi province. Semiliquidambar 1993; Magallón et al., 1999; Soltis et al., 2000). The order cathayensis occupies a large area overlapping with Liquid- Altingiales, including Altingiaceae and Rhodoleiaceae, was ambar and Altingia in South China (Chang, 1962, 1979; recognized and included in the superorder Trochodendr- Ferguson, 1989). Leaves of Semiliquidambar combine char- anae along with the order Trochodendrales (Doweld, 1998). acters from Altingia (simple leaves with camptodromous Within Liquidambar, allozyme (Hoey and Parks, 1991, venation) and Liquidambar (palmately-lobed leaves with 1994) and phylogenetic analyses of DNA sequence data (Li actinodromous venation). Semiliquidambar was proposed et al., 1997a,b; Li and Donoghue, 1999; Shi et al., 1998) sug- to be a possible intergeneric hybrid between Liquidambar gest a sister-species relationship between the North Ameri- and Altingia (Bogle, 1986; Ferguson, 1989; Shi et al., 2001). can L. styraciXua L., and the western Asian Liquidambar The fossil record of Altingiaceae dates back to the Late orientalis Mill. While none of these studies addresses the Cretaceous, but its Neogene record is remarkably robust. monophyly of Liquidambar, several studies have docu- The earliest evidence for Altingiaceae fossils are recently mented the paraphyly of the genus (Shi et al., 1998, 2001; described Late Cretaceous mesofossils from New Jersey Wen, 1999). Two sections were traditionally recognized and the Allon Xora of central Georgia (Herendeen et al., within Liquidambar: sect. Liquidambar and sect. Cathayam- 1999; Zhou et al., 2001). Although these fossils cannot be bar Harms (Harms, 1930). Harms (1930) used the presence assigned to a modern genus, they show that spherical infr- of “Borsten” (“setae” sensu Bogle, 1986), in the inXores- uctescences composed of biloculate fruits were among some cences and infructescences of Liquidambar formosana as the of the earliest eudicot infructescences. A morphological cla- deWning character for his section Cathayambar. The distic analysis of Altingiaceae (Ickert-Bond et al., 2005) that remaining species (L. orientalis and L. styraciXua) were focused on intergeneric relationships in Liquidambar, found placed in sect. Euliquidambar (D sect. Liquidambar) and support for Microaltingia Zhou, Crepet, and Nixon from were stated as lacking these structures. When Liquidambar the Late Cretaceous of New Jersey, belonging to the stem acalycina was described (Chang, 1979), it was placed in sect. lineage of Altingiaceae. An additional globose infructes- Liquidambar along with L. orientalis and L. styraciXua. Liq- cence that has been assigned to the Altingiaceae is the uidambar formosana from Asia is highly distinct from oth- genus Steinhauera Presl., an infructescence that is known ers due to numerous long spinose phyllomes ( D setae of from many Eocene localities of Europe (Mai, 1968). Leaves, Bogle, 1986) between adjacent fruits, which are lacking infructescences, and seeds recognized as Liquidambar also from the eastern North American and the western Asian appear from the Eocene to the Pliocene in western North species (Ickert-Bond et al., 2005). The other eastern Asian America, Europe, and Asia (Ferguson, 1989; Manchester, species, L. acalycina overlaps with L. formosana in distribu- 1999; Pigg et al., 2004; Wolfe, 1973). The greatest occur- tional range, but replaces it at elevations above 1200 m. rence of the Altingiaceae is in the Miocene, where com- Unlike other Liquidambar species, L. acalycina shares sev- pressed leaves and fruits are commonly found in localities eral characters with Altingia (Ickert-Bond et al., 2005; Pigg in Asia, Europe, and North America (Manchester,
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