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Molecular Phylogenetics and Evolution 96 (2016) 118–129 Molecular Phylogenetics and Evolution 96 (2016) 118–129 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Multi-locus plastid phylogenetic biogeography supports the Asian hypothesis of the temperate woody bamboos (Poaceae: Bambusoideae) q Xian-Zhi Zhang a,b,d, Chun-Xia Zeng b, Peng-Fei Ma a,b, Thomas Haevermans c, Yu-Xiao Zhang a,b, ⇑ ⇑ Li-Na Zhang a,b,d, Zhen-Hua Guo b, , De-Zhu Li a,b, a Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China b Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming, Yunnan 650201, China c Institut de Systématique, Évolution, Biodiversité ISYEB, Unité Mixte de Recherche 7205, Centre National de la Recherche Scientifique/Muséum national d’histoire naturelle/École Pratique des Hautes Études/Université Pierre-et-Marie-Curie, Muséum national d’histoire naturelle, Sorbonne Universités, 57 Rue Cuvier, CP39, F-75231 Paris cedex 05, France d Kunming College of Life Sciences, University of Chinese Academy of Sciences, Kunming, Yunnan 650201, China article info abstract Article history: In this paper we investigate the biogeography of the temperate woody bamboos (Arundinarieae) using a Received 19 June 2015 densely-sampled phylogenetic tree of Bambusoideae based on six plastid DNA loci, which corroborates Revised 22 November 2015 the previously discovered 12 lineages (I–XII) and places Kuruna as sister to the Chimonocalamus clade. Accepted 26 November 2015 Biogeographic analyses revealed that the Arundinarieae diversified from an estimated 12 to 14 Mya, Available online 23 December 2015 and this was followed by rapid radiation within the lineages, particularly lineages IV, V and VI, starting from c. 7–8 Mya. It is suggested that the late Miocene intensification of East Asian monsoon may have Keywords: contributed to this burst of diversification. The possibilities of the extant Sri Lankan and African temper- Arundinarieae ate bamboo lineages representing ‘basal elements’ could be excluded, indicating that there is no evidence Biogeography Multi-locus plastid phylogeny to support the Indian or African route for migration of temperate bamboo ancestors to Asia. Radiations Divergence time from eastern Asia to Africa, Sri Lanka, and to North America all are likely to have occurred during the Rapid radiation Pliocene, to form the disjunct distribution of Arundinarieae we observe today. The two African lineages Bambusoideae are inferred as being derived independently from Asian ancestors, either by overland migrations or long- distance dispersals. Beringian migration may explain the eastern Asian–eastern North American disjunction. Ó 2015 Elsevier Inc. All rights reserved. 1. Introduction (BPG, 2012). Tribe Arundinarieae, containing about 28 genera and 530 species, is highly heterogeneous in terms of morphology with The bamboos (Poaceae: Bambusoideae) are popularly known 12 major lineages (Triplett and Clark, 2010; Zeng et al., 2010; Yang for their universal uses in human life, their adaptation to shady for- et al., 2013; Attigala et al., 2014). Tribe Bambuseae is divided into ests, as well as being the exclusive staple food for the giant pandas two lineages, namely the paleotropical and the neotropical woody (Judziewicz et al., 1999; Li, 1999) and for some Madagascan lemur bamboos, with the former group possessing four subtribes, c. 47 species (Bystriakova et al., 2004). The most recent studies based on genera, 400 species and the latter three subtribes, c. 19 genera, plastid genomes and nuclear genes strongly support Bambusoideae and 370 species (Sungkaew et al., 2009; Kelchner and BPG, as sister to Pooideae in the Poaceae ‘BEP clade’ (Zhang et al., 2011; 2013), while the Olyreae consists of three subtribes with c. 21 Wu and Ge, 2012; Zhao et al., 2013). The Arundinarieae, i.e., tem- genera and 120 species (BPG, 2012). perate woody bamboos, is one of three well-supported Bambu- Extant bamboos display a markedly disjunct distribution partic- soideae tribes, with the other two namely the Bambuseae ularly at the generic levels, occurring in every continent except (tropical woody bamboos) and the Olyreae (herbaceous bamboos) Europe and Antarctica (Fig. 1, modified from Ohrnberger, 1999). The biogeographic patterns exhibited by the Arundinarieae is of particular interest: more than 510 species are distributed in east- q This paper was edited by the Associate Editor Wang Xiao-Quan. ern and southeastern Asia (Li et al., 2006; BPG, 2012), around 20 ⇑ Corresponding authors at: Kunming Institute of Botany, Chinese Academy of in the Afro-Indian area (Sri Lanka, southern India, Africa and Sciences, 132 Lanhei Road, Kunming 650201, China. Madagascar) (Ohrnberger, 1999), and only three species in eastern E-mail addresses: [email protected] (Z.-H. Guo), [email protected] North America (Triplett and Clark, 2010). Bambuseae displays a (D.-Z. Li). http://dx.doi.org/10.1016/j.ympev.2015.11.025 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. X.-Z. Zhang et al. / Molecular Phylogenetics and Evolution 96 (2016) 118–129 119 C B A D G E H F Fig. 1. Present geographic distribution of bamboos. Labels A–H show the eight area units used in biogeographic analyses. pantropical disjunction: the neotropical lineage being distributed 2013), in an attempt to understand the sudden diversification of from northern Mexico, Central America to Chile in South America, the Arundinarieae. However, although 7 representatives of the and the paleotropical one in southern China, Indo-Malaya, north- Arundinarieae endemic to Sri Lanka and one from Madagascar ern Australia, New Guinea, New Caledonia, Madagascar and Africa were included in a recent molecular phylogeny study (Attigala (Judziewicz et al., 1999; Wong, 2004). Olyreae mainly diversified in et al., 2014), the phylogenetic position of the former and the iden- the Neotropics, with one species (Buergersiochloa bambusoides tity of the latter were not conclusive to shed light on whether India Pilg.) being restricted to New Guinea, and another variable species or Madagascar hold taxa basal to the tribe, or to investigate where (Olyra latifolia L.) found throughout tropical America, Africa and northern temperate bamboos first evolved. Madagascar (Judziewicz et al., 1999; Ohrnberger, 1999). To date Hodkinson et al. (2010) using two markers, trnL-F and ITS there are very few bamboo macrofossils i.e. culms and leaves that (without cloning), based on 34 Arundinarieae species mostly from have been studied comprehensively. Well preserved Guadua culm the Phyllostachys clade (Clade V, Zeng et al., 2010) plus 8 species of fossils were described from the Neotropics (Brea and Zucol, Bambuseae and Olyreae, suggested that temperate woody bam- 2007; Olivier et al., 2009; Brea et al., 2013). Other well-preserved boos underwent a rapid late Miocene radiation. Based on phyloge- Miocene bamboo fossils (leaves and culm segments) were nomic analyses of 7 Arundinarieae species, 3 Bambuseae species unearthed recently from China (Wang et al., 2013b, 2014), how- and 1 species of Olyreae, Burke et al. (2012) suggested that North ever, it is not possible to ascertain their membership in a tribe. American Arundinaria gigantea (Walter) Muhl. diverged from Based on phytoliths surveys, Strömberg (2005) documented late within Arundinarieae between 1.9 and 3.9 Mya (million years Eocene Chusquea-like fossils from North America. A few putative ago). However, it has been shown that appropriate and extensive bambusoid fossils were also reported from Europe (Worobiec and taxon sampling is particularly significant for accurate phylogenetic Worobiec, 2005), but much better evidence for their assignment estimation and ancestral distribution inference that are derived to Bambusoideae is necessary. from phylogenetic trees (Heath et al., 2008; Lamm and Redelings, Clark’s (1997) hypothesis of a Gondwanan origin for the Bam- 2009). An inadequacy of taxon sampling probably impaired the busoideae was widely accepted with evidence from available results of previous studies (e.g., Hodkinson et al., 2010; Burke grasses (including bamboos) systematics (GPWG, 2001; Bremer, et al., 2012), as increasing taxon sampling to include proper fossil 2002; GPWG II, 2012). Two theories have been presented to calibration nodes is a better option than relying on secondary cal- explain the disjunct distribution of the temperate woody bamboos ibration in molecular dating analyses (Ho and Phillips, 2009; (Hodkinson et al., 2010). An ‘Asian hypothesis’ suggested that Sauquet et al., 2012). Including all the extant 12 Arundinarieae lin- ancestors of the Arundinarieae dispersed to Asia at an early date eages sampled throughout their known geographic ranges, within but failed to diversify until recent times; while the ‘outside Asia the context of a broad phylogenetic framework for the Bambu- hypothesis’ suggested that ancestors of the Arundinarieae evolved soideae, is of great importance to analyze the biogeography of this outside Asia (for example in Africa or India) and arrived in Asia group. recently, concurrently with their radiation. Collision of the African The present paper provides, to the best of our knowledge, the or the Indian plate with the Eurasian plate was suggested as pro- first molecular biogeographic analyses for the Arundinarieae with viding an opportunity for a recent arrival of the Arundinarieae in a deep tribal and subtribal sampling for the Bambusoideae
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