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YMPEV 5375 No. of Pages 12, Model 5G 26 December 2015 Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 1 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev 5 6 3 Multi-locus plastid phylogenetic biogeography supports the Asian q 4 hypothesis of the temperate woody bamboos (Poaceae: Bambusoideae) a,b,d b a,b c a,b 7 Xian-Zhi Zhang , Chun-Xia Zeng , Peng-Fei Ma , Thomas Haevermans , Yu-Xiao Zhang , a,b,d b,⇑ a,b,⇑ 8 Li-Na Zhang , Zhen-Hua Guo , De-Zhu Li 9 a Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China 10 b Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming, Yunnan 650201, China 11 c Institut de Systématique, Évolution, Biodiversité ISYEB, Unité Mixte de Recherche 7205, Centre National de la Recherche Scientifique/Muséum national d’histoire naturelle/École 12 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 13 d Kunming College of Life Sciences, University of Chinese Academy of Sciences, Kunming, Yunnan 650201, China 1415 16 article info abstract 3218 19 Article history: In this paper we investigate the biogeography of the temperate woody bamboos (Arundinarieae) using a 33 20 Received 19 June 2015 densely-sampled phylogenetic tree of Bambusoideae based on six plastid DNA loci, which corroborates 34 21 Revised 22 November 2015 the previously discovered 12 lineages (I–XII) and places Kuruna as sister to the Chimonocalamus clade. 35 22 Accepted 26 November 2015 Biogeographic analyses revealed that the Arundinarieae diversified from an estimated 12 to 14 Mya, 36 23 Available online xxxx and this was followed by rapid radiation within the lineages, particularly lineages IV, V and VI, starting 37 from c. 7–8 Mya. It is suggested that the late Miocene intensification of East Asian monsoon may have 38 24 Keywords: contributed to this burst of diversification. The possibilities of the extant Sri Lankan and African temper- 39 25 Arundinarieae ate bamboo lineages representing ‘basal elements’ could be excluded, indicating that there is no evidence 40 26 Biogeography 27 Multi-locus plastid phylogeny to support the Indian or African route for migration of temperate bamboo ancestors to Asia. Radiations 41 28 Divergence time from eastern Asia to Africa, Sri Lanka, and to North America all are likely to have occurred during the 42 29 Rapid radiation Pliocene, to form the disjunct distribution of Arundinarieae we observe today. The two African lineages 43 30 Bambusoideae are inferred as being derived independently from Asian ancestors, either by overland migrations or long- 44 31 distance dispersals. Beringian migration may explain the eastern Asian–eastern North American 45 disjunction. 46 Ó 2015 Elsevier Inc. All rights reserved. 47 48 49 50 51 1. Introduction (BPG, 2012). Tribe Arundinarieae, containing about 28 genera and 63 530 species, is highly heterogeneous in terms of morphology with 64 52 The bamboos (Poaceae: Bambusoideae) are popularly known 12 major lineages (Triplett and Clark, 2010; Zeng et al., 2010; Yang 65 53 for their universal uses in human life, their adaptation to shady for- et al., 2013; Attigala et al., 2014). Tribe Bambuseae is divided into 66 54 ests, as well as being the exclusive staple food for the giant pandas two lineages, namely the paleotropical and the neotropical woody 67 55 (Judziewicz et al., 1999; Li, 1999) and for some Madagascan lemur bamboos, with the former group possessing four subtribes, c. 47 68 56 species (Bystriakova et al., 2004). The most recent studies based on genera, 400 species and the latter three subtribes, c. 19 genera, 69 57 plastid genomes and nuclear genes strongly support Bambusoideae and 370 species (Sungkaew et al., 2009; Kelchner and BPG, 70 58 as sister to Pooideae in the Poaceae ‘BEP clade’ (Zhang et al., 2011; 2013), while the Olyreae consists of three subribes with c. 21 gen- 71 59 Wu and Ge, 2012; Zhao et al., 2013). The Arundinarieae, i.e., tem- era and 120 species (BPG, 2012). 72 60 perate woody bamboos, is one of three well-supported Bambu- Extant bamboos display a markedly disjunct distribution partic- 73 61 soideae tribes, with the other two namely the Bambuseae ularly at the generic levels, occurring in every continent except 74 62 (tropical woody bamboos) and the Olyreae (herbaceous bamboos) Europe and Antarctica (Fig. 1, modified from Ohrnberger, 1999). 75 The biogeographic patterns exhibited by the Arundinarieae is of 76 particular interest: more than 510 species are distributed in east- 77 q This paper was edited by the Associate Editor Wang Xiao-Quan. ern and southeastern Asia (Li et al., 2006; BPG, 2012), around 20 78 ⇑ Corresponding authors at: Kunming Institute of Botany, Chinese Academy of in the Afro-Indian area (Sri Lanka, southern India, Africa and 79 Sciences, 132 Lanhei Road, Kunming 650201, China. Madagascar) (Ohrnberger, 1999), and only three species in eastern 80 E-mail addresses: [email protected] (Z.-H. Guo), [email protected] North America (Triplett and Clark, 2010). Bambuseae displays a 81 (D.-Z. Li). http://dx.doi.org/10.1016/j.ympev.2015.11.025 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. Please cite this article in press as: Zhang, X.-Z., et al. Multi-locus plastid phylogenetic biogeography supports the Asian hypothesis of the temperate woody bamboos (Poaceae: Bambusoideae). Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.11.025 YMPEV 5375 No. of Pages 12, Model 5G 26 December 2015 2 X.-Z. Zhang et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 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. 82 pantropical disjunction: the neotropical lineage being distributed 2013), in an attempt to understand the sudden diversification of 117 83 from northern Mexico, Central America to Chile in South America, the Arundinarieae. However, although 7 representatives of the 118 84 and the paleotropical one in southern China, Indo-Malaya, north- Arundinarieae endemic to Sri Lanka and one from Madagascar 119 85 ern Australia, New Guinea, New Caledonia, Madagascar and Africa were included in a recent molecular phylogeny study (Attigala 120 86 (Judziewicz et al., 1999; Wong, 2004). Olyreae mainly diversified in et al., 2014), the phylogenetic position of the former and the iden- 121 87 the Neotropics, with one species (Buergersiochloa bambusoides tity of the latter were not conclusive to shed light on whether India 122 88 Pilg.) being restricted to New Guinea, and another variable species or Madagascar hold taxa basal to the tribe, or to investigate where 123 89 (Olyra latifolia L.) found throughout tropical America, Africa and northern temperate bamboos first evolved. 124 90 Madagascar (Judziewicz et al., 1999; Ohrnberger, 1999). To date Hodkinson et al. (2010) using two markers, trnL-F and ITS 125 91 there are very few bamboo macrofossils i.e. culms and leaves that (without cloning), based on 34 Arundinarieae species mostly from 126 92 have been studied comprehensively. Well preserved Guadua culm the Phyllostachys clade (Clade V, Zeng et al., 2010) plus 8 species of 127 93 fossils were described from the Neotropics (Brea and Zucol, Bambuseae and Olyreae, suggested that temperate woody bam- 128 94 2007; Olivier et al., 2009; Brea et al., 2013). Other well-preserved boos underwent a rapid late Miocene radiation. Based on phyloge- 129 95 Miocene bamboo fossils (leaves and culm segments) were nomic analyses of 7 Arundinarieae species, 3 Bambuseae species 130 96 unearthed recently from China (Wang et al., 2013a,b,c, 2014), how- and 1 species of Olyreae, Burke et al. (2012) suggested that North 131 97 ever, it is not possible to ascertain their membership in a tribe. American Arundinaria gigantea (Walter) Muhl. diverged from 132 98 Based on phytoliths surveys, Strömberg (2005) documented late within Arundinarieae between 1.9 and 3.9 Mya (million years 133 99 Eocene Chusquea-like fossils from North America. A few putative ago). However, it has been shown that appropriate and extensive 134 100 bambusoid fossils were also reported from Europe (Worobiec and taxon sampling is particularly significant for accurate phylogenetic 135 101 Worobiec, 2005), but much better evidence for their assignment estimation and ancestral distribution inference that are derived 136 102 to Bambusoideae is necessary. from phylogenetic trees (Heath et al., 2008; Lamm and Redelings, 137 103 Clark’s (1997) hypothesis of a Gondwanan origin for the Bam- 2009). An inadequacy of taxon sampling probably impaired the 138 104 busoideae was widely accepted with evidence from available results of previous studies (e.g., Hodkinson et al., 2010; Burke 139 105 grasses (including bamboos) systematics (GPWG, 2001; Bremer, et al., 2012), as increasing taxon sampling to include proper fossil 140 106 2002; GPWG II, 2012). Two theories have been presented to calibration nodes is a better option than relying on secondary cal- 141 107 explain the disjunct distribution of the woody bamboos ibration in molecular dating analyses (Ho and Phillips, 2009; 142 108 (Hodkinson et al., 2010). An ‘Asian hypothesis’ suggested that Sauquet et al., 2012). Including all the extant 12 Arundinarieae lin- 143 109 ancestors of the Arundinarieae dispersed to Asia at an early date eages sampled throughout their known geographic ranges, within 144 110 but failed to diversify until recent times; while the ‘outside Asia the context of a broad phylogenetic framework for the Bambu- 145 111 hypothesis’ suggested that ancestors of the Arundinarieae evolved soideae, is of great importance to analyze the biogeography of this 146 112 outside Asia (for example in Africa or India) and arrived in Asia group.
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