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Oleaceae) Based on Plastid and Nuclear Ribosomal DNA Sequences: Tertiary Climatic Shifts and Lineage Differentiation Times

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Oleaceae) Based on Plastid and Nuclear Ribosomal DNA Sequences: Tertiary Climatic Shifts and Lineage Differentiation Times Annals of Botany 104: 143–160, 2009 doi:10.1093/aob/mcp105, available online at www.aob.oxfordjournals.org Phylogenetics of Olea (Oleaceae) based on plastid and nuclear ribosomal DNA sequences: Tertiary climatic shifts and lineage differentiation times Guillaume Besnard1,2,†,*, Rafael Rubio de Casas3,4,†,‡, Pascal-Antoine Christin1 and Pablo Vargas4 1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland, 2Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK, 3Departamento de Biologı´a Vegetal 1, UCM, Jose´ Antonio Novais 2, 28040 Madrid, Spain and 4Royal Botanic Garden, Madrid, CSIC, Plaza de Murillo 2, 28014 Madrid, Spain Received: 29 July 2008 Returned for revision: 25 November 2008 Accepted: 30 March 2009 Published electronically: 25 May 2009 † Background and Aims The genus Olea (Oleaceae) includes approx. 40 taxa of evergreen shrubs and trees classi- fied in three subgenera, Olea, Paniculatae and Tetrapilus, the first of which has two sections (Olea and Ligustroides). Olive trees (the O. europaea complex) have been the subject of intensive research, whereas little is known about the phylogenetic relationships among the other species. To clarify the biogeographical history of this group, a molecular analysis of Olea and related genera of Oleaceae is thus necessary. † Methods A phylogeny was built of Olea and related genera based on sequences of the nuclear ribosomal internal transcribed spacer-1 and four plastid regions. Lineage divergence and the evolution of abaxial peltate scales, the latter character linked to drought adaptation, were dated using a Bayesian method. † Key Results Olea is polyphyletic, with O. ambrensis and subgenus Tetrapilus not sharing a most recent common ancestor with the main Olea clade. Partial incongruence between nuclear and plastid phylogenetic reconstructions suggests a reticulation process in the evolution of subgenus Olea. Estimates of divergence times for major groups of Olea during the Tertiary were obtained. † Conclusions This study indicates the necessity of revising current taxonomic boundaries in Olea. The results also suggest that main lines of evolution were promoted by major Tertiary climatic shifts: (1) the split between subgenera Olea and Paniculatae appears to have taken place at the Miocene–Oligocene boundary; (2) the separation of sections Ligustroides and Olea may have occurred during the Early Miocene following the Mi-1 glaciation; and (3) the diversification within these sections (and the origin of dense abaxial indumentum in section Olea) was concomitant with the aridification of Africa in the Late Miocene. Key words: Internal transcribed spacer (ITS), relaxed molecular clock, olive tree, leaf peltate scales, plastid DNA, Tertiary climatic shifts, systematics. INTRODUCTION Australia, New Zealand and the Pacific islands (Green, 2002; Besnard et al., 2007b). Section Ligustroides includes eight Oleaceae comprise about 600 species and 24 genera (Johnson, species from central and southern Africa, displaying numerous 1957; Rohwer, 1996; Wallander and Albert, 2000; Green, similarities in morphological and biochemical traits with 2004). Within this family, Olea and ten other (extant) genera section Olea (Harborne and Green, 1980; Green, 2002). Key constitute the subtribe Oleinae within the tribe Oleeae morphological characters discriminating these two sections (Wallander and Albert, 2000). Thirty-three species and nine are the inflorescence position (axillary in section Olea vs. subspecies of evergreen shrubs and trees have been circum- terminal and sometimes axillary in section Ligustroides), the scribed in Olea based on morphological characters (Green, density of peltate scales (densely covered abaxial leaf 2002). In addition, these taxa are classified in three subgenera, surface in section Olea vs. leaves with no or scattered scales Olea, Paniculatae and Tetrapilus, the first of which has two in section Ligustroides) and the structure of the calyx tube sections (Olea and Ligustroides). Section Olea is formed (+ membranous in section Olea vs. + coriaceous in section exclusively by the olive complex (Olea europaea), in which Ligustroides; Green, 2002). Subgenus Paniculatae includes six subspecies are recognized (Vargas et al., 2001; Green, only one taxon (Olea paniculata) distributed from Pakistan 2002). This subgenus is distributed from South Africa to to New Caledonia. This species is characterized by leaf China, across the Saharan mountains, Macaronesia and the domatia in the axils of the midrib and primary veins (Green, Mediterranean basin. O. europaea is also found outside of 2002). Lastly, subgenus Tetrapilus contains 23 species from its native range as a result of human-mediated dispersal; it south-eastern Asia. Limited flower shape variability is found has been repeatedly introduced in the New World and has in this subgenus, whereas variable vegetative and reproductive become naturalized and has invaded numerous areas in traits are observed (e.g. leaf morphology, hermaphrodite vs. dioecious species; Green, 2002). Key characters defining sub- * For correspondence. E-mail [email protected] †These authors contributed equally to this work. genus Tetrapilus are a corolla tube longer than corolla lobes ‡Present address: Department of Biology, Duke University, Box 90338, and the absence of peltate scales. Durham, NC 27708, USA. # The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 144 Besnard et al. — Phylogenetics and dating of the genus Olea Olea taxa are found in a wide range of habitats. Most species test for polyphyly and to infer the origin and centres of diver- are distributed in subtropical and tropical areas where they can sification of the genus Olea. Moreover, the use of palaeobota- be important vegetation components (Green, 2002). Some taxa nical data in phylogenetic analyses helps in dating major in both sections of subgenus Olea occur in arid environments, lineage divergence times and then in identifying differentiation although representatives can also be found in other habitats. events (e.g. Magallo´n and Sanderson, 2001). The olive complex (section Olea) is present in open forests of Contrasting between plastid and nuclear analyses is useful in the Mediterranean and subtropical regions of the Old World, interpreting the biogeographical history of taxa and the evolution from Macaronesian cloud forests (subspp. cerasiformis and of phenotypic traits (e.g. Maurin et al., 2007; Wang et al.,2007; guanchica) to extremely arid Saharan mountains (subsp. laper- Figueroa et al., 2008). Incongruence between classifications rinei). Members of section Ligustroides occur in various habi- based on both genomes can reveal evolutionary events such as tats in subtropical and equatorial Africa (Green and Kupicha, reticulation or incomplete lineage sorting (Linder and 1979; Green, 2002), such as dry brush on coastal dunes (e.g. Rieseberg, 2004). However, if methodologies to generate O. exasperata and O. woodiana), scrub vegetation among quart- plastid DNA sequences are generally simple in plants, the phylo- zite crags (O. chimanimani), upland forests with low rainfall genetic use of nuclear markers can be more challenging (A´ lvarez (e.g. O. capensis subsp. macrocarpa) and altitudinally transi- and Wendel, 2003). The internal transcribed spacers (ITS) of tional and humid upland forests (e.g. O. schliebenii and nrDNA have been useful in resolving phylogenetic relationships O. welwitschii). Stomata protected by dense abaxial peltate in three genera of Oleaceae (Fraxinus: Jeandroz et al., 1997; scales (a trait considered to be linked to dry habitats; Bongi Wallander, 2008; Ligustrum and Syringa:Liet al., 2002), et al., 1987) are only found in section Olea (Green, 2002). In although some limitations of such markers have been encountered contrast, other traits associated with arid environments, such in the analysis of angiosperm phylogenies (Baldwin et al.,1995; as the presence of a thick cuticle and lanceolate leaves, are A´ lvarez and Wendel, 2003; Nieto Feliner and Rossello´, 2007). found in both sections (Green, 2002). Subgenus Paniculatae Typically, ITS sequences are subject to concerted evolution, is present in coastal scrub and rain forests (Kiew, 1979). display a rapid rate of evolution compared with most plastid Lastly, subgenus Tetrapilus is found in a variety of habitats loci, and can be readily amplified and sequenced even from (Kiew, 1979; Chang et al., 1996; Green, 2002), from xeric sand- poorly preserved material (Mort et al., 2007). However, technical stone in open rocky country (e.g. O. dentata) to dense and moist difficulties have been encountered when sequencing ITS regions lowland tropical forests (e.g. O. guangxiensis and O. rosea). in the olive complex due to the presence of numerous pseudo- Some attempts have been made to determine the affinities genes (Besnard et al., 2007c). As a consequence, this set of and phylogenetic relationships between Olea species and markers has to be used cautiously and with improved techniques related genera of Oleaceae using biochemical and molecular to isolate functional ITS sequences from nrDNA units (see Nieto data (e.g. Harborne and Green, 1980; Angiolillo et al., 1999; Feliner and Rossello´, 2007). Wallander and Albert, 2000; Vargas and Kadereit, 2001; In the present study, we used maternally inherited (plastid Baldoni
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