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Radiation of Southern African Daisies: Biogeographic Inferences for Subtribe Arctotidinae (Asteraceae, Arctotideae)

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Radiation of Southern African Daisies: Biogeographic Inferences for Subtribe Arctotidinae (Asteraceae, Arctotideae) Molecular Phylogenetics and Evolution 49 (2008) 1–16 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Radiation of southern African daisies: Biogeographic inferences for subtribe Arctotidinae (Asteraceae, Arctotideae) Robert J. McKenzie *, Nigel P. Barker Molecular Ecology and Systematics Group, Department of Botany, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa article info abstract Article history: The majority of the approximately 80–90 species in subtribe Arctotidinae occur in southern Africa with Received 18 April 2007 the centre of diversity in the winter-rainfall region. Three species are restricted to afromontane eastern Revised 29 June 2008 Africa and three species are endemic to Australia. To investigate biogeographic and phylogenetic relation- Accepted 9 July 2008 ships within Arctotidinae, sequence data from four cpDNA regions (psbA-trnH, trnT-trnL and trnL-trnF Available online 18 July 2008 spacers and trnL intron) and the ITS nrDNA region for 59 Arctotidinae species were analyzed with parsi- mony and Bayesian-inference approaches. Eight well-supported major lineages were resolved. The earli- Keywords: est-diverging extant lineages are afromontane or inhabit mesic habitats, whereas almost all sampled taxa Arctotideae from the winter-rainfall and semi-arid areas have diverged more recently. Molecular dating estimated Arctotidineae Asteraceae that the major clades diverged during the Miocene and Pliocene, which is coincident with the trend of Biogeography increasing rainfall seasonality, aridification and vegetation changes in southwestern Africa. Trans-oceanic Cape floral region dispersal to Australia was estimated to have occurred during the Pliocene. Compositae Ó 2008 Elsevier Inc. All rights reserved. Dispersal–vicariance analysis Molecular phylogeny Molecular dating 1. Introduction ular (McKenzie et al., 2006a) and morphological (Karis 2006) phy- logenetic investigations. However, the sampling in previous Southern Africa is an important centre of floristic biodiversity. studies was not comprehensive and here we present the first Approximately 24,000 species of vascular plants are recorded from well-sampled phylogenetic and biogeographic investigation of the region, of which approximately 80% are endemic to southern the predominantly southern African subtribe Arctotidinae to help Africa (Cowling and Hilton-Taylor, 1997). Almost 10% of this plant to fill this gap in our knowledge. diversity is contributed by the Asteraceae (the daisy family), with Arctotideae is a small tribe containing about 215 species in 17 approximately 250 genera and 2250 species recorded from the re- genera with an almost exclusively African distribution (Karis, gion (Koekemoer, 1996). Over 80% of these species are endemic to 2007). Two subtribes are recognized with some authors placing southern Africa (Cowling and Hilton-Taylor, 1997). The family has other lineages in the tribe (for a brief review of the taxonomy radiated in all of the recognized southern African biomes and is one and relationships of the tribe, see Funk et al., 2004). The subtribe of the more species-rich families in most, if not all, of these biomes. Arctotidinae contains approximately 80–90 species currently clas- The diversity and endemism of Asteraceae in southern Africa is sified into five genera (Karis, 2007). One species, Haplocarpha scap- focused in eight putative centres (Koekemoer, 1996). These centres osa, has a wide distribution in montane and temperate are generally consistent with centres of endemism indicated by the southeastern Africa (e.g. Hilliard, 1977; Pope, 1992). Three species southern African flora as a whole (e.g. see van Wyk and Smith, are indigenous to the high-altitude East African mountains (Mesfin 2001). Despite being a major component of the flora, the evolution Tadesse, 2004) and three species are endemic to Australia (Holland and biogeography of southern African Asteraceae is poorly investi- and Funk, 2006). The remaining species occur in southern Africa, gated and well-resolved phylogenetic reconstructions are required with the centre of diversity in the Cape and Succulent Karoo Cen- to elucidate the origins and radiation of the Asteraceae lineages in tres of Floristic Endemism (see van Wyk and Smith, 2001). Both the region (Galley and Linder, 2006). The only major southern Afri- areas occur in the winter-rainfall zone (Cowling, 1992; Dean and can lineage of Asteraceae that has been investigated to any extent Milton, 1999; see Fig. 1) and are combined into a ‘Greater Capensis’ is the tribe Arctotideae, which has been the subject of both molec- floristic region by some workers (Born et al., 2007). Because more than 50% of the species occur in the Cape Floristic Region (CFR), the * Corresponding author. Fax: +27 46 6229550. Arctotidinae, and especially Arctotis s.str., might represent a true E-mail address: [email protected] (R.J. McKenzie). ‘Cape clade’ sensu Linder (2003, 2005). 1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2008.07.007 2 R.J. McKenzie, N.P. Barker / Molecular Phylogenetics and Evolution 49 (2008) 1–16 Fig. 1. A topographical map of southern Africa with the approximate boundaries of different rainfall regimes indicated (based on Chase and Meadows, 2007). Understanding the factors responsible for the unusually high Gondwana, transoceanic dispersal has been important in a diver- levels of floristic richness and endemism in the winter-rainfall re- sity of animals (e.g. Vences et al., 2003; Schwarz et al., 2006) and gion of southern Africa (and the CFR in particular) has attracted plant groups (e.g. Baum et al., 1998; Mummenhoff et al., 2004; considerable interest (for reviews for the CFR, see Linder, 2003, Cook and Crisp, 2005; Linder and Barker, 2005; Barker et al., 2005). Molecular dating has indicated that plant lineages have 2007). Vicariance appears to have been much stronger in animals been recruited into the Cape flora since at least the Cretaceous than plant groups (Sanmartín and Ronquist, 2004). Of particular and the onset of radiations in these lineages is indicated to range significance to the present study, plant taxa with a disjunct south- from the Oligocene to the Pliocene (Linder, 2005), so the extant ern African–Australian distribution, such as the Arctotidinae, are diversity cannot be explained solely by vicariance or explosive spe- rare (Good, 1964; Thorne, 1972; Goldblatt, 1978), and as yet few ciation in response to one or more concurrent triggers. Further- of these taxa have been investigated in a phylogenetic context. more, the southern African flora as a whole is indicated to have A previous molecular phylogenetic study of Arctotidinae exam- evolved from disparate sources, including descendants of Gondwa- ined sequence variation in five cpDNA regions (ndhF, psbA-trnH, nan ancestors (Goldblatt, 1978; Anderson et al., 1999), temperate rps16, trnS-trnfM, and trnT-trnF) and the ITS nrDNA region for 18 southern African progenitors (Goldblatt, 1978), groups of Eurasian species representing the major morphological variation in the sub- or tropical African origin (e.g. Meerow et al., 2003; Hurka et al., tribe (McKenzie et al., 2006a). Strong incongruence between the 2005; Mummenhoff et al., 2005), and Australasian ancestors (e.g. prevailing taxonomy and evolutionary relationships were indi- Linder et al., 2003). Therefore a thorough understanding of diversi- cated. A clade comprising two Haplocarpha species (H. nervosa fication processes in the southern African flora is likely to be best and H. rueppellii, both formerly segregated in Landtia) from the achieved by a taxon-focused, rather than a broad floristic, approach southern and East African mountain chain was sister to the rest because of the individuality of taxon histories within a flora (Ver- of the subtribe, and the widely distributed H. scaposa was indicated boom et al., 2003). to be an early divergence. The placement of the Australian Cymbon- The above evidence indicates that transcontinental and trans- otus lawsonianus and East African H. schimperi in a well-supported oceanic dispersal has been important in the compilation of the clade along with south-eastern African Arctotis species provided present-day southern African flora. Indeed, there is increasing evi- evidence for dispersal from southern Africa to Australia and migra- dence for the importance of long-distance dispersal in determining tion to East Africa, respectively. However, comprehensive sampling extant plant biogeographic patterns worldwide (e.g. Price and Cla- of extant lineages is required for confident phylogenetic recon- gue, 2002; de Queiroz, 2005). Phylogenetic reconstructions based structions and to allow more accurate biogeographic inferences on molecular data, in combination with molecular calibrations to to be made. The primary objective of the present study was to estimate the date of divergence events, have provided strong evi- reconstruct a species-level phylogenetic hypothesis for a compre- dence that in the Southern Hemisphere, following the breakup of hensive sample of Arctotidinae based on sequence data from four R.J. McKenzie, N.P. Barker / Molecular Phylogenetics and Evolution 49 (2008) 1–16 3 cpDNA regions (the psbA-trnH, trnT-trnL and trnL-trnF intergenic (Bioline, London), 1 ll 0.1 lM solution of each forward and reverse spacers and trnL intron) and the ITS nrDNA region. The specific primer, 0.2 ll BioTaqÒ DNA polymerase (5 U/ll, Bioline,
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