bs_bs_banner Botanical Journal of the Linnean Society, 2013, 171, 61–79. With 3 figures Temporal and spatial origin of Gesneriaceae in the New World inferred from plastid DNA sequences MATHIEU PERRET1*, ALAIN CHAUTEMS1, ANDRÉA ONOFRE DE ARAUJO2 and NICOLAS SALAMIN3,4 1Conservatoire et Jardin botaniques de la Ville de Genève, Ch. de l’Impératrice 1, CH-1292 Chambésy, Switzerland 2Centro de Ciências Naturais e Humanas, Universidade Federal do ABC, Rua Santa Adélia, 166, Bairro Bangu, Santo André, Brazil 3Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland 4Swiss Institute of Bioinformatics, Quartier Sorge, CH-1015 Lausanne, Switzerland Received 15 December 2011; revised 3 July 2012; accepted for publication 18 August 2012 Gesneriaceae are represented in the New World (NW) by a major clade (c. 1000 species) currently recognized as subfamily Gesnerioideae. Radiation of this group occurred in all biomes of tropical America and was accompanied by extensive phenotypic and ecological diversification. Here we performed phylogenetic analyses using DNA sequences from three plastid loci to reconstruct the evolutionary history of Gesnerioideae and to investigate its relationship with other lineages of Gesneriaceae and Lamiales. Our molecular data confirm the inclusion of the South Pacific Coronanthereae and the Old World (OW) monotypic genus Titanotrichum in Gesnerioideae and the sister-group relationship of this subfamily to the rest of the OW Gesneriaceae. Calceolariaceae and the NW genera Peltanthera and Sanango appeared successively sister to Gesneriaceae, whereas Cubitanthus, which has been previously assigned to Gesneriaceae, is shown to be related to Linderniaceae. Based on molecular dating and biogeographical reconstruction analyses, we suggest that ancestors of Gesneriaceae originated in South America during the Late Cretaceous. Distribution of Gesneriaceae in the Palaeotropics and Australasia was inferred as resulting from two independent long-distance dispersals during the Eocene and Oligocene, respectively. In a short time span starting at 34 Mya, ancestors of Gesnerioideae colonized several Neotropical regions including the tropical Andes, Brazilian Atlantic forest, cerrado, Central America and the West Indies. Subsequent diversification within these areas occurred largely in situ and was particularly extensive in the mountainous systems of the Andes, Central America and the Brazilian Atlantic forest. Only two radiations account for 90% of the diversity of Gesneriaceae in the Brazilian Atlantic forest, whereas half of the species richness in the northern Andes and Central America originated during the last 10 Myr from a single radiation. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 61–79. ADDITIONAL KEYWORDS: Andes – Australasia – Brazilian Atlantic forest – dispersal – historical biogeography – Lamiales – molecular dating – Neotropics – phylogeny – radiation. INTRODUCTION actions (Wiehler, 1983; Weber, 2004; Weber & Skog, 2007 onwards). Gesneriaceae are particularly abun- Gesneriaceae (150–160 genera, c. 3200 species) are a dant at mid-elevation in the mountain forests where clade of perennial herbs, shrubs or small trees that they grow as epiphytes or on rock outcrops. Gesne- display an outstanding morphological diversity riaceae are comparatively less frequent in the low- related to the colonization of a wide range of habitats lands where they predominantly occur on slopes, and the evolution of specialized plant–animal inter- riverbanks and moist rocks in rainforest. Flowers of Gesneriaceae are highly diversified, reflecting adap- *Corresponding author. E-mail: [email protected] tation to a wide range of pollinators including birds, © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 61–79 61 62 M. PERRET ET AL. bats and several types of bees (Sanmartin-Gajardo & hemisphere route described for plants (Morley, 2003; Sazima, 2004, 2005; Marten-Rodriguez, Almarales- Sanmartín & Ronquist, 2004; Renner, 2005). Castro & Fenster, 2009; Sanmartin-Gajardo & Discriminating between these hypotheses requires Vianna, 2010). Fruits can be either dry and dehiscent a robust time-calibrated phylogenetic framework. with seeds dispersed by wind or rain drops, or fleshy Such a result however is difficult to obtain for Ges- with seed dispersal relying mainly on animals such as neriaceae due to the lack of known fossils attributed birds or ants (Kleinfeldt, 1978; Wiehler, 1983; David- to this family. In such a case, the extension of the son, 1988; Smith, 2001). This extensive morphological phylogenetic analyses to a broader taxonomic context diversification coupled with high levels of convergence coupled with the use of relaxed molecular clock complicated the assessment of relationships in Ges- methods (Sanderson, 1997, 2002; Drummond et al., neriaceae and caused considerable confusion in the 2006) can help estimate divergence time on nodes early taxonomy of this family (Clark et al., 2012). without fossils. Using this approach across the Current phylogenetic evidence supports the divi- asterids, Bremer, Friis & Bremer (2004) found that sion of Gesneriaceae into two main lineages. The first Gesneriaceae have a crown age of 71 Mya and corresponds to subfamily Didymocarpoideae with c. diverged early in Lamiales. Although this age esti- 1900 species distributed in Africa, Eurasia and the mate supports the hypothesis of a Palaeogene origin Pacific (Weber, 2004; Möller et al., 2009). The second of the family as proposed by Raven & Axelrod (1974), is subfamily Gesnerioideae with > 1000 species all a recent molecular dating of tribe Coronanthereae restricted to the Neotropics with the exception of tribe suggests that the origin of this group could largely Coronanthereae (20 species; e.g. Salinas & Armesto, post-date the separation of southern hemisphere 2012), presenting a disjunct distribution in the tem- landmasses, supporting the role of long-distance dis- perate Andes (Asteranthera Hanst., Mitraria Cav. and persal over Gondwanan vicariance for explaining the Sarmienta Ruiz & Pav.) and Australasia (e.g. Coro- occurrence of Coronanthereae in both South America nanthera C.B.Clarke, Fieldia Cunn. and Rhabdoth- and Australasia (Woo et al., 2011). Despite these amnus Cunn.). The close relationship between breakthroughs, the lack of a global phylogenetic Coronanthereae and Gesnerioideae was first proposed analysis for the family has so far prevented resolution based on shared features in the development of their of the biogeographical origin of Gesneriaceae as a cotyledons (Burtt, 1963). Since then, this relationship whole. has been repeatedly confirmed by molecular data Within the Neotropics, Gesneriaeceae show an (Smith, 1996; Mayer et al., 2003; Möller et al., 2009; Andean-centred distribution with the highest species Woo et al., 2011). At a lower taxonomic level, continu- richness in the northern Andes and Central America, ing efforts to resolve phylogenetic relationships in and secondary centres of diversity in the West Indies Gesneriaceae have contributed to redefine the (Skog, 1976; Marten-Rodriguez et al., 2010) and the boundaries of many genera and tribes (Zimmer et al., Brazilian Atlantic forest (Chautems et al., 2005; 2002; Perret et al., 2003; Roalson et al., 2005b; Clark Perret, Chautems & Spichiger, 2006) (Fig. 1). Accord- et al., 2006, 2012; Möller et al., 2009). However, no ing to Gentry’s (1982) survey, such Andean-centred phylogenetic analysis including all major lineages of taxa may represent one-third of all Neotropical plant Gesneriaceae has yet been performed and there is species and account for the extraordinary biodiversity still no firm consensus on the affinities of taxa such as found in the Neotropics compared with other tropical Cubitanthus Barringer, Peltanthera Benth., Sanango regions. To date, few studies have investigated the Bunting & Duke, Titanotrichum Soler. and Calceolar- genesis of this pattern (Pirie et al., 2006; Antonelli iaceae with Gesneriaceae (Weber, 2004). et al., 2009; Givnish et al., 2011), despite its impor- Several hypotheses exist for the age and place of tance for identifying the biotic or abiotic factors that origin of Gesneriaceae. According to Raven & Axelrod may have shaped the spatial distribution of diversity (1974), Gesneriaceae probably existed when Africa we see today (Antonelli & Sanmartín, 2011). In the and South America were in closer contact, perhaps in NW Gesnerioideae, the hypothesis that the Andes the early Palaeogene (> 65 Mya), whereas the major may correspond to a centre of origin and a major groups of the family differentiated later. Building on source area of dispersals into other Neotropical this hypothesis, Burtt (1998) suggested that Coronan- regions still needs to be tested. Roalson, Skog & thereae could be the relict of a Gondwanan lineage, Zimmer (2008) indicated that ancestors of tribe which further gave rise to both Old World (OW) Gloxinieae, and probably of Gesnerioideae as a whole, Didymocarpoideae and New World (NW) Gesnerio- could be either widespread through Central America ideae. The alternative hypothesis is that the transoce- and western/Andean South America or restricted to anic distribution of Gesneriaceae post-dated the Central America. This study also pointed to an early break-up of Gondwana and resulted from long- colonization of Central America and the Caribbean distance dispersal events following the southern region at least 26 Mya, prior