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Historical Biogeography of Melicope (Rutaceae) and Its Close Relatives with a Special Emphasis on Pacific Dispersals

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Historical Biogeography of Melicope (Rutaceae) and Its Close Relatives with a Special Emphasis on Pacific Dispersals Journal of Systematics JSE and Evolution doi: 10.1111/jse.12299 Research Article Historical biogeography of Melicope (Rutaceae) and its close relatives with a special emphasis on Pacific dispersals Marc S. Appelhans1,2*, Jun Wen2, Marco Duretto3, Darren Crayn4, and Warren L. Wagner2 1Department of Systematics, Biodiversity and Evolution of Plants, Albrecht-von-Haller Institute of Plant Sciences, University of Goettingen, Untere Karspuele 2, 37073 Goettingen, Germany 2Department of Botany, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA 3National Herbarium of New South Wales, Royal Botanic Gardens & Domain Trust, Mrs Macquaries Rd, Sydney NSW 2000, Australia 4Australian Tropical Herbarium, James Cook University, PO Box 6811, Cairns QLD 4870, Australia *Author for correspondence. E-mail: [email protected] Received 17 October 2017; Accepted 22 December 2017; Article first published online 8 February 2018 Abstract The genus Melicope (Rutaceae) occurs on most Pacific archipelagos and is perfectly suited to study Pacific biogeography. The main goal was to infer the age, geographic origin and colonization patterns of Melicope and its relatives. We sequenced three nuclear and two plastid markers for 332 specimens that represent 164 species in 16 genera of Rutaceae. Phylogenetic reconstruction, molecular dating, ancestral area reconstruction and diversification analyses were carried out. The two main clades (Acronychia-Melicope and Euodia) originated in Australasia and their crown ages are dated to the Miocene. Diversification rates differed among the subclades and were lowest in the Euodia lineage and highest in the Hawaiian Melicope lineage. The Malagasy and Mascarene species form a clade, which split from its SE Asian relatives in the Pliocene/Pleistocene. At least eight colonizations to the Pacific islands occurred. The timing of all colonizations except for the Hawaiian group is congruent with age of the island ages. Australia, New Guinea and New Caledonia have been the source of colonizations into the Pacific islands in the Melicope clade. Melicope shows high dispersability and has colonized remote archipelagos such as the Austral and Marquesas Islands each twice. Colonization of islands of the Hawaiian-Emperor seamount chain likely predates the ages of the current main islands, and the initial colonization to Kaua’i occurred after the splitting of the Hawaiian lineage into two subclades. Wider ecological niches and adaptations to bird-dispersal likely account for the much higher species richness in the Acronychia-Melicope clade compared to the Euodia clade. Key words: Acronychia, dispersal, Euodia, Melicope, Pacific biogeography, Rutaceae. 1 Introduction or non-standard vectors might account for LDD events (Higgins et al., 2003; Nathan et al., 2008). Molecular Due to their geographic isolation, mostly recent volcanic phylogenetic studies have identified examples of single LDD origin and their high endemicity, Pacific archipelagos are events across thousands of kilometers (Le Roux et al., 2014), particularly interesting for biogeographic and evolutionary as well as shorter distance events as stepping-stone dispersals studies. Most Pacific islands are of volcanic origin and have (Harbaugh et al., 2009). Since only a small percentage of never been in direct contact with continental landmasses the Pacific region consists of exposed land, successful (Neall & Trewick, 2008). Pacific islands that consist of colonizations, especially of the more remote islands, can be continental crust – e.g., New Caledonia and New Zealand – considered to be extremely rare. Many lineages once thought have long been separated from other continental landmasses to represent independent colonizations on a particular and elements of their floras and faunas arrived after their archipelago have been shown to be the result of an extensive isolation (Sharma & Wheeler, 2013). Colonizers of Pacific radiation after a single colonization event. The most notable islands most likely arrived by means of long-distance dispersal example being the Hawaiian Lobeliads (Campanulaceae), (LDD) events (Nathan et al., 2008). Different vectors the largest island radiation of angiosperms (Givnish et al., facilitating LDD have been identified; the most common 2009). Pacific lineages are mostly of Asian, Australasian or being birds, wind, ocean currents, and driftwood rafts (Donlan American origin and only a few examples of an African origin & Nelson, 2003; Cowie & Holland, 2006; Wenny et al., 2016). A are known (Baldwin & Wagner, 2010; Keeley & Funk, 2011). ‘standard vector’ of dispersal has been proposed for many Melicope J.R.Forst. & G.Forst. (Rutaceae; Citrus family) and species based on morphological characters (Carlquist, 1967). its close relatives (hereinafter the Acronychia-Euodia-Melicope However the relationship between morphology and dispersal group) occur on most Pacific archipelagos and the group is is difficult to quantify and it has been proposed that multiple therefore perfectly suited to study Pacific biogeography and © 2018 Institute of Botany, Chinese Academy of Sciences November 2018 | Volume 56 | Issue 6 | 576–599 Pacific biogeography of Melicope (Rutaceae) 577 dispersal routes. Recent phylogenetic studies have demon- (2015) with several additional species mainly from Pacific strated that Melicope is not monophyletic and several genera archipelagos sampled. A total number of 332 specimens, need to be merged into it or into Acronychia J.R.Forst. & representing 164 species and 16 genera, were included in this G.Forst. and Euodia J.R.Forst. & G.Forst. to ensure monophyly study (Table 1): Melicope (118 out of 235 species and 12 of each genus (Appelhans et al., 2014a, 2014b; Holzmeyer unidentified specimens), Acronychia (24/48), Brombya (1/2), et al., 2015). Melicope (240 spp.) is the largest genus in Comptonella (4/8), Dutaillyea (1/2), Euodia (4/6), Macluroden- Rutaceae and occurs in Madagascar and the Mascarene dron (1/6), Medicosma (1/25), Perryodendron (1/1), Picrella (2/3), Islands, throughout SE Asia, Malesia, Australasia, and on most Pitaviaster (1/1), Sarcomelicope (1/9), Tetractomia (1/6). Dutail- Pacific archipelagos. Its centers of species richness and liopsis, Boronia section Cyanothamnus, Neobyrnesia and Zieria endemicity are the Hawaiian Islands and New Guinea (Hartley, were the only putative relatives that were not sampled. We 2001). Acronychia (49 spp.) is the second largest genus of the sampled throughout the distributional range of Melicope and Acronychia-Euodia-Melicope group and is mainly confined to its relatives with particularly comprehensive sampling of the eastern Australia and New Guinea with two species extending Pacific species (72/111). One specimen of Boronia (section west to Java and India, and two eastward to the Solomon Boronella (Baill.) Duretto & Bayly) and three specimens of Islands and New Caledonia (Hartley, 1974, 2013; Holzmeyer Myrtopsis O.Hoffm. were included as outgroups based on et al., 2015). Euodia (7 spp.) is more restricted and is present in previous phylogenetic studies (Bayly et al., 2013; Appelhans eastern Australia, New Guinea and the South Pacific from New et al., 2014a). Britain and New Caledonia to Samoa and Niue (Hartley, 2001). For the ancestral area reconstructions (AAR) and diversifi- The Acronychia-Euodia-Melicope group consists of 15 cation analyses, a reduced dataset containing only a single genera and about 360 species (Kubitzki et al., 2011; Appelhans specimen for each species was used. For species found to be et al., 2014a). Of these, Comptonella Baker f., Dutaillyea Baill., polyphyletic, one specimen for each evolutionary lineage was Picrella Baill. (all New Caledonia), Platydesma H.Mann included. This dataset contains 166 species/specimens (Table 1, (Hawaii) and Sarcomelicope Engl. (Australia to Fiji) are nested specimens in bold type). within Melicope while Maclurodendron T.G.Hartley (Malay Peninsula to the Philippines and Hainan) is nested within 2.2 Molecular lab work and phylogenetic analyses Acronychia. Platydesma has recently been merged into Our datasets included nuclear markers ETS, ITS and NIAi3 and Melicope (Appelhans et al., 2017). Medicosma Hook.f (New plastid markers psbA-trnH and trnL-trnF. DNA extraction, PCR Guinea, E Australia, New Caledonia) and Tetractomia Hook.f amplification, contig assembly, construction of alignments (Malay Peninsula to the Solomon Islands) are consecutive and model selection followed Appelhans et al. (2014b). All sister groups of the Acronychia-Melicope clade. Brombya F. sequences were deposited at EMBL/Genbank (Table 1). Muell. (Australia), Pitaviaster T.G.Hartley (Australia), along Alignment was straightforward except for the psbA-trnH with Melicope vitiflora (F.Muell.) T.G.Hartley, group with region which contained many, often large (ca. 100 bp) indels. Euodia,andthiscladeissistertoPerryodendron T.G.Hartley After excluding bases that could not be aligned with (Moluccas to New Britain) (Appelhans et al., 2014a). The confidence, the psbA-trnH alignment was reduced from 1101 monotypic Dutailliopsis T.G.Hartley (New Caledonia) is a to 509 bp. Phylogenetic reconstructions were conducted with potential member of the Melicope clade based on morpho- mrbayes 3.2.5 (Ronquist et al., 2012) using the best-fit models logical characters (Hartley, 1997, 2001; Bayly et al., 2013), but of sequence evolution for each marker (Table 2) and applying it has not been sampled in any molecular phylogenetic study. the settings
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