BS 55 479 Origins and biogeographic patterns in Ericaceae: New insights from recent phylogenetic analyses Kathleen A. Kron and James L. Luteyn Kron, KA. & Luteyn, J.L. 2005. Origins and biogeographic patterns in Ericaceae: New insights from recent phylogenetic analyses. Biol. Skr. 55: 479-500. ISSN 0366-3612. ISBN 87-7304-304-4. Ericaceae are a diverse group of woody plants that span the temperate and tropical regions of the world. Previous workers have suggested that Ericaceae originated in Gondwana, but recent phy­ logenetic studies do not support this idea. The theory of a Gondwanan origin for the group was based on the concentration of species richness in the Andes, southern Africa, and the southwest Pacific islands (most of which are thought to be of Gondwanan origin). The Andean diversity is comprised primarily of Vaccinieae with more than 800 species occurring in northern South America, Central America, and the Antilles. In the Cape Region of South Africa the genus Erica is highly diverse with over 600 species currently recognized. In the southwest Pacific islands, Vac­ cinieae and Rhodoreae are very diverse with over 290 species of Rhododendron (sect. Vireya) and approximately 500 species of Vaccinieae (I)imorphanthera, Paphia, Vaccinium). Recent phyloge­ netic studies have also shown that the Styphelioideae (formerly Epacridaceae) are included within Ericaceae, thus adding a fourth extremely diverse group (approximately 520 species) in areas considered Gondwanan in origin. Phylogenetic studies of the family on a global scale, how­ ever, have indicated that these highly diverse “Gondwanan” groups are actually derived from within Ericaceae. Both Fitch parsimony character optimization (using MacClade 4.0) and disper- sal-vicariance analysis (DIVA) indicate that Ericaceae is Laurasian in origin. Thus, previous sug­ gestions that Ericaceae are Gondwanan in origin are not supported. Separate analysis of geo­ graphic areas and phylogenetic relationships among the diverse South American Vaccinieae using dispersal-vicariance analysis (DIVA) indicate that dispersal has likely played a major role in the diversification of the Andean clade of Vaccinieae into Central America and the lower eleva­ tions in northern South America. Results of the analysis indicate an Andean origin for this group, which comprises most of the ericaceous species diversity described from South America. This analysis also indicates that in taxa such as Cavendishia and Satyria s.s., the Central American species are the result of relatively recent dispersal from a South American (i.e., Andean) ancestor. Kathleen A. Kron, Department of Biology, Wake Forest University, Winston-Salem, North Carolina, 27109- 7325, U.S.A. E-mail: [email protected] James L. Luteyn, New York Botanical Garden, Bronx, New York, 10458-5126, U.S.A. E-mail: jluteyn@nybg. org 480 BS 55 Introduction regions of the world. These concentrations of diversity occur in four major clades within Eri­ Ecologically and economically important, the caceae: Vaccinieae, Rhodoreae, Ericeae, and Ericaceae are a diverse group of woody plants Styphelioideae (Appendix 1). Vaccinieae are that can be found in a variety of habitats most diverse in the montane tropics of South throughout much of the temperate and tropi­ America and Asia. Although generic limits cal regions of the world (Appendix 1). They within Vaccinieae are poorly understood, phy­ are usually found in acid soils and are associ­ logenetic studies have shown that of the five ated with mycorrhizal fungi. In the tropics, Eri­ major clades identified in a molecular system­ caceae are most diverse in mid- to high-eleva­ atic study of the group (Kron et al. 2002b), tion montane cloud forests (Luteyn 2002), those with the largest number of species are which are also some of the most threatened tropical and occur in Gondwanan regions (e.g., ecosystems in the world (Knapp 2002). The South America, New Guinea). In the Rhodor­ most recent classification of the family (Kron et eae, Rhododendron section Vireya is the most al. 2002a) recognizes eight subfamilies and 20 species rich group within Rhododendron. Vireyas tribes. The distribution of these groups is gen­ are tropical and most diverse in New Guinea. erally cosmopolitan in scale, with concentra­ Africa, another Gondwanan region, also has tions of species diversity in the tropics, the large and morphologically diverse Erica Himalayas, Australia, and the Cape Region of (Ericeae) and one of the highest concentra­ South Africa (Fig. 1, Appendix 1). tions of species in a single genus in the world in The most recent global treatment of Eri­ the Cape Region. Lastly, Styphelioideae, which caceae biogeography is by Raven and Axelrod contain approximately 450 species are most (1974) who presented a general overview of diverse in Australia. This group was formerly the biogeography of angiosperms and sug­ thought to be distinct from Ericaceae, but gested that Ericaceae (not including Styphe- recent phylogenetic studies using molecular lioideae, then a separate family, Epacridaceae) and morphological data have shown that the likely originated in Gondwana with direct group is sister to the Vaccinioideae (Kron et al. migration from Africa to South America. They 2002a) and therefore derived from within Eri­ considered that long distance dispersal from caceae. North America in the late Miocene had added Recent phylogenetic analyses in Ericaceae to the diversity of Ericaceae in South America, have provided good resolution with strong sta­ which was already established there via the ear­ tistical support of major clades within the fam­ lier African-South American land connection. ily based on both molecular and morphologi­ The Styphelioideae (Epacridaceae) were con­ cal data. With this phylogenetic framework, sidered to be of relatively ancient descent biogeographic patterns may be analyzed with resulting from long distance dispersal between the goal of shedding some light on the origins west Gondwana and Australasia (Raven & Axel­ of the group. Here we investigate the origin rod 1974). Heads (2003) postulated a globally and biogeographic patterns of Ericaceae using widespread complex as ancestral to Ericaceae, dispersal-vicariance analysis (DIVA; Ronquist but his supporting argument was confined to 1997) and Fitch parsimony character optimiza­ descriptions of Malesian ericad distributions. tion using MacClade 4.0 (Maddison & Maddi­ The most species-rich groups within the Eri­ son 2000). In addition, the biogeographic caceae do indeed appear to be concentrated in areas of the Andean clade within the Vac­ what are now considered to be Gondwanan cinieae are analyzed using DIVA. BS 55 481 Enkianthoideae (1/16) Monotropoideae (15/50) Arbutoideae (4/81) Cassiopoideae 1/12) Ericoideae (19/1780) Harrimanelloideae (1/2) Vaccinioideae (45/1593) Fig. 1. World-wide distribution maps for the eight subfamilies of Ericaceae. A, Enkianthoideae. B, Monotropoideae. C, Arb­ utoideae. D, Cassiopoideae. E, Ericoideae. F, Harrimanelloideae. G, Styphelioideae. H, Vaccinioideae. 482 BS 55 Methods morphological (91 characters) data for the Eri­ caceae tree. The sampling of ericalean taxa is In addition to DIVA and Fitch parsimony char­ relatively small, but relationships in the tree acter optimization, there are several other are in general agreement with the recent study approaches to biogeographic analysis (c.g., by Anderberg et al. (2002) that used more COMPONENT; Page 1993,). We chose DIVA genes and many more taxa. For the Andean because it can be used with a single phyloge­ clade analysis we used the most recent molecu­ netic tree, rather than requiring trees from sev­ lar tree based on three chloroplast eral different groups in order to construct area genes/regions (matK, ndhF, rps4) and the cladograms. DIVA does not require any a prior nuclear internal transcribed spacer region, ITS knowledge of geologic history and does not (Powell 8c Kron 2003). All of the trees used for assume areas have a strictly divergent history biogeographic analysis exhibited moderate to (Ronquist 1997). DIVA treats areas as charac­ strong bootstrap support for most clades. Few ters (in a presence/absence format), but mini­ polytomies were present in the Ericales and mizes dispersal and extinction events relative Andean trees, and the Ericaceae tree was fully to vicariance (no cost) events in ancestral state resolved. Because DIVA requires fully resolved (?>., area) reconstruction. Therefore, DIVA trees, the Ericales tree of Kron et al. (2002a) offers the possibility of identifying potential was resolved according to the results of more vicariance events at deep branches in the tree. detailed analyses (Kron et al. 2002a; Kron However, the deepest nodes within the tree are 1997) and the Andean tree was resolved arbi­ also prone to more error (Ronquist 1997), so it trarily. The Ericales tree was modified to is important to evaluate the group of interest at include an additional taxon (i.e., Clethra more than one taxonomic scale. arborea, authors of species names are given in Fitch parsimony character optimization uses Appendices 2-4) in order to better represent areas as character states and these are mapped the geographic distribution of the Clethraceae. onto the tree using MacClade 4.0 (Maddison & The placement of C. arborea sister to C. alnifolia Maddison 2000). This provides a simple way of was based on the analysis of Anderberg et al. viewing the distribution of current taxa relative (2002) which provided better statistical sup­ to the branching patterns in the tree. However, port and resolution for nodes basal to the Eri­ Fitch parsimony optimization allows fewer pos­ caceae. Two widespread species were removed sible ancestral area reconstructions than DIVA from the Andean clade to facilitate the DIVA because only terminals can have more than analysis. one state (i.e., area). In the biogeographic analysis of Ericaceae We investigated the origin of Ericaceae using (both the Ericales tree and the Ericaceae two trees. One tree included Ericaceae and sev­ tree) different scorings of areas for DIVA and eral other members of the Ericales (APG 1998) Fitch parsimony character optimization were and the other tree included more taxa within used.