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Astereae, Asteraceae) Downloaded from by Guest on 04 September 2019 GISELA SANCHO1*, PETER J bs_bs_banner Botanical Journal of the Linnean Society, 2015, 177, 78–95. With 5 figures Late Cenozoic diversification of the austral genus Lagenophora (Astereae, Asteraceae) Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/1/78/2416348 by guest on 04 September 2019 GISELA SANCHO1*, PETER J. DE LANGE FLS2, MARIANO DONATO3, JOHN BARKLA4 and STEVE J. WAGSTAFF5 1División Plantas Vasculares, Museo de La Plata, FCNYM, UNLP, Paseo del Bosque s.n., La Plata, 1900, Buenos Aires, Argentina 2Ecosystems and Species Unit, Department of Conservation, Private Bag 68908, Newton 1145, Auckland, New Zealand 3ILPLA, Instituto de Limnología Dr. Raúl A. Ringuelet, FCNYM, UNLP and CONICET, 122 and 60, La Plata, 1900, Buenos Aires, Argentina 4Otago Conservancy, Department of Conservation, PO Box 5244, Dunedin 9058, New Zealand 5Allan Herbarium, Landcare Research, PO Box 69040, Lincoln 7640, New Zealand Received 14 March 2014; revised 23 May 2014; accepted for publication 30 August 2014 Lagenophora (Astereae, Asteraceae) has 14 species in New Zealand, Australia, Asia, southern South America, Gough Island and Tristan da Cunha. Phylogenetic relationships in Lagenophora were inferred using nuclear and plastid DNA regions. Reconstruction of spatio-temporal evolution was estimated using parsimony, Bayesian inference and likelihood methods, a Bayesian relaxed molecular clock and ancestral area and habitat reconstruc- tions. Our results support a narrow taxonomic concept of Lagenophora including only a core group of species with one clade diversifying in New Zealand and another in South America. The split between the New Zealand and South American Lagenophora dates from 11.2 Mya [6.1–17.4 95% highest posterior density (HPD)]. The inferred ancestral habitats were openings in beech forest and subalpine tussockland. The biogeographical analyses infer a complex ancestral area for Lagenophora involving New Zealand and southern South America. Thus, the estimated divergence times and biogeographical reconstructions provide circumstantial evidence that Antarctica may have served as a corridor for migration until the expansion of the continental ice during the late Cenozoic. The extant distribution of Lagenophora reflects a complex history that could also have involved direct long-distance dispersal across southern oceans. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 78–95. ADDITIONAL KEYWORDS: Antarctica – austral distributions – divergence times – molecular dating – molecular phylogeny – New Zealand – South America. INTRODUCTION Barreda et al., 2010, 2012). By the Miocene, the family had a cosmopolitan distribution (Scott, With more than 20 000 species and a cosmopolitan Cadman & McMillan, 2006; Barreda et al., 2010; distribution, Asteraceae is probably the largest family Zavada & Lowrey, 2010). Members of the family are of flowering plants. The discovery of a remarkably presently found in virtually all biomes, with the well-preserved fossil from Eocene deposits in Argen- exception of Antarctica (Funk et al., 2005). The fruits tina suggests that the family was part of an ancient of Asteraceae are one-seeded cypselae and many flora that inhabited southern Gondwana before the species have a modified pappus structure adapted for establishment of oceanic barriers to dispersal seed dispersal over great distances. (Bremer & Gustafsson, 1997; Katinas et al., 2007; Notably, only a few genera of Asteraceae occur in Australia, New Zealand and southern South America, *Corresponding author. E-mail: [email protected] occasionally extending to Asia (Allan, 1961; 78 © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 78–95 AUSTRAL DIVERSIFICATION OF LAGENOPHORA 79 Moreira-Muñoz & Muñoz-Schick, 2007; Ezcurra, Table 1. Lagenophora species and their geographical dis- Baccala & Wardle, 2008). One such genus is Lagen- tribution. Abbreviations: AR, Argentina; AS, Asia; AU, ophora Cass. (Astereae). Its austral distribution, Australia; AUI, Auckland Island; CAI, Campbell Island; unusual in Asteraceae, makes this genus a fascinat- CH, Chile; CHI, Chatham Islands; KI, Kermadec Island; ing object of study that could provide valuable new NI, North Island; NZ, New Zealand; SI, South Island; STI, insights into the evolutionary processes that explain Stewart Island; TA, Tasmania; WAU, Western Australia. extant austral distribution patterns. Roman numerals depict regions of Chile The fruit morphology of Lagenophora is also Lagenophora species Distribution unusual (see below) in Asteraceae, and could be key to Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/1/78/2416348 by guest on 04 September 2019 inferring dispersal mechanisms and biogeographical L. barkeri Kirk NZ (SI) patterns in the Southern Hemisphere. Lagenophora L. cuneata Kirk NZ (NI, SI) also has an association with southern beech forest L. gracilis Steetz South-eastern AS, AU (Nothofagaceae), an important component of austral (south-eastern AU, TA), India, floras and the focus of much discussion about South- Java, New Caledonia, New ern Hemisphere biogeography. Guinea, Philippines, Sri Lanka, Sumatra, Timor L. hariotii Franch. AR (Chubut, Neuquén, Río LAGENOPHORA TAXONOMIC HISTORY, DISTRIBUTION Negro, Santa Cruz, Tierra del AND HABITATS Fuego), CH (VII, VIII, IX, X, Lagenophora previously included Australasian, XI, XII, Juan Fernández Hawaiian, Central American and South American Island) species. However, Cabrera (1966) excluded the L. hirsuta Poepp. ex AR (Neuquén, Río Negro), CH Hawaiian species from Lagenophora and placed them Less. (VII, VIII, IX, X, XII) in Keysseria Lauterbach. Cabrera (1966) also L. huegelii Benth. AU (TA, south-eastern AU, described the new section Lagenophora section Pseu- WAU) domyriactis Cabrera to include the Central American L. lanata A.Cunn. NZ (NI) and one Venezuelan species of Lagenophora. Cabrera L. montana Hook.f. AU (south-eastern AU, TA), NZ with Beaman & de Hong (1965) noticed the anoma- (NI, SI) lous morphological characters of the species of this L. nudicaulis (Comm. AR (Neuquén, Río Negro, Tierra section. Later, Velez (1981) and Cuatrecasas (1986) ex Lam.) Dusén del Fuego), CH (VI, VII, VIII, IX, X, XI, XII), Islands: excluded the Central American species and the Ven- Staten (de los Estados), ezuelan species from Lagenophora and placed them in Falklands (Malvinas), Gough, Myriactis Less. This narrowed circumscription of Tristan da Cunha Lagenophora without the Central American, Venezue- L. petiolata Hook.f. NZ (AUI, CAI, CHI, KI, NI, SI, lan and Hawaiian species was followed by different STI) authors (e.g. Nesom, 2001; Brouillet et al., 2009; L. pinnatifida Hook.f. NZ (NI, SI) Sancho & Pruski, 2011) and supported by recent L. pumila (Forst.f.) NZ (CHI, KI, NI, SI, STI) molecular phylogenetic analyses. Indeed, Keysseria Cheesem. and Myriactis proved to be distantly related to Lage- L. stipitata (Labill.) AU (south-eastern AU, TA), NZ nophora [Brouillet et al., 2009; Nakamura et al., 2012, Druce (NI), Papua with Myriactis panamensis (S.F.Blake) Cuatrec. as L. strangulata Colenso NZ (NI, SI) ‘Lagenophora panamensis S.F. Blake’]. Recently, Nakamura et al. (2012), based on internal transcribed spacer (ITS) sequence data, showed a paraphyletic Lagenophora closely related to Solenogyne Cass., diversity in New Zealand (nine species; de Lange & although the authors did not make decisions on the Rolfe, 2010); Australia has four species [two, circumscription of Lagenophora. In addition, this L. montana and L. stipitata, shared with New study did not include the southern South American Zealand]; one of the Australian species extends to Lagenophora spp. [one of which, L. nudicaulis Asia and three species live in southern South (Comm. ex Lam.) Dusén, is the type species of the America, including Juan Fernández and surrounding genus], which are important to completely under- islands, Staten Island (Isla de los Estados) and the stand the phylogenetic relationships and spatio- Falkland Islands (Islas Malvinas) (Fig. 1A, B). One of temporal evolution of this genus. the South American species, L. nudicaulis, also occurs As presently circumscribed, Lagenophora comprises on Gough Island and the islands of Tristan da Cunha. 14 species (Table 1) (Cabrera, 1966; Drury, 1974; Seven of the nine species in New Zealand are Cuatrecasas, 1986; Nesom, 2001) and has most of its endemic. The New Zealand species occupy habitats © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177, 78–95 80 G. SANCHO ET AL. LAGENOPHORA AND DISPERSAL PATTERNS OF A AUSTRAL FLORA Lagenophora spp. are mostly delicate plants, usually rhizomatous, that produce solitary capitula on long, often wiry scapes (Fig. 2E); the pappus, the most common dispersal structure in Asteraceae, is lacking, which is unusual (Fig. 2F). Sanmartín, Wanntorp & Winkworth (2007) suggested that dispersal mecha- Downloaded from https://academic.oup.com/botlinnean/article-abstract/177/1/78/2416348 by guest on 04 September 2019 nisms are important for inferring dispersal patterns Area A (i.e. direct wind or water dispersal) that explain bio- Area B geographical scenarios of trans-Pacific flora. Accord- Area D ing to Sanmartín & Ronquist (2004), the dominant pattern in plants (southern South America (Australia, New Zealand)) is better explained by dispersal than Areaf E Area F by vicariance associated with the breakup of Gond- 2000 km wanaland and subsequent continental drift. For B Asteraceae, the break-up
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