bs_bs_banner Botanical Journal of the Linnean Society, 2013, 171, 80–102. With 6 figures REVIEW ARTICLE Phylogeny and biogeography in Solanaceae, Verbenaceae and Bignoniaceae: a comparison of continental and intercontinental diversification patterns RICHARD G. OLMSTEAD* Department of Biology and Burke Museum, University of Washington, Box 355325, Seattle, WA 98195, USA Received 10 January 2012; revised 31 July 2012; accepted for publication 25 August 2012 Recent molecular phylogenetic studies of Solanales and Lamiales show that Solanaceae, Verbenaceae and Bignoniaceae all diversified in South America. Estimated dates for the stem lineages of all three families imply origins in the Late Cretaceous, at which time South America had separated from the united Gondwanan continent. A comparison of clades in each family shows (1) success in most clades at dispersing to, and diversifying in, North America and/or the Caribbean, (2) a mix of adaptation to novel ecological zones and niche conservation, (3) limited dispersal to continents outside of the western hemisphere, and, where this has occurred, (4) no association between long-distance dispersal and fleshy, animal-dispersed fruits. Shared patterns among the three families contribute to a better understanding of the in situ diversification of the South American flora. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 80–102. ADDITIONAL KEYWORDS: biogeography – long-distance dispersal – Neotropics – South America. INTRODUCTION & Antonelli, 2005; Andersson, 2006; Hughes & East- wood, 2006; Erkens, Maas & Couvreur, 2009; O’Leary South America is one of the great crucibles of plant et al., 2009; Lu-Irving & Olmstead, 2012) than about diversity, with some of the most diverse plant ecosys- patterns of diversification of indigenous groups that tems on earth populated in high proportion by plant originated and have a long history in South America. A groups that originated and diversified in situ (Gentry, few examples are available that seem to fit these 1982; Pennington & Dick, 2004 Pennington et al., criteria, including Gesneriaceae subfamily Gesnerio- 2010; Antonelli & Sanmartin, 2011). That said, ideae (Smith et al., 1997; Zimmer et al., 2002; Weber, perhaps more has been written about the biogeography 2004; Perret et al., 2012), Bromeliaceae (Givnish et al., of immigrants to South America (Renner, Clausing & 2004, 2011), a large clade of Cactaceae (Edwards, Meyer, 2001; Davis et al., 2002; Lavin et al., 2004; Nyffeler & Donoghue, 2005) and Asteraceae (Funk Richardson et al., 2004; Bell & Donoghue, 2005; Lavin, et al., 2005). A well-documented example is Malpighi- Herendeen & Wojciechowski, 2005; Särkinen et al., aceae, which has a circumtropical distribution, but has 2007; McDade, Daniel & Kiel, 2008; Soza & Olmstead, been shown to have diversified initially in South 2010a, b), and groups that have radiated recently in America at least 64 Mya (Davis et al., 2002) and has South America (e.g. Richardson et al., 2001; Andersson colonized the Old World as many as six times. Three other large clades that originated and exhibited their *E-mail: [email protected] early diversification in South America are the subject 80 © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 80–102 SOLANACEAE, VERBENACEAE AND BIGNONIACEAE 81 of this paper: Solanaceae (Olmstead et al., 2008), 20 Mya, even if it did not persist. An earlier connec- Bignoniaceae (Olmstead et al., 2009) and Verbenaceae tion, if confirmed, would require re-evaluation of (Marx et al., 2010). classic explanations for mammal (Simpson, 1980; Clade diversification may entail both the geographi- Marshall et al., 1982) and, more recently, bird (Smith cal spread from a point of origin and adaptation to & Klicka, 2010) distributions, which have been linked novel environments along the way. The processes to the more recent date. involved in successful migration and adaptation Over-water, long-distance dispersal requires a present a continuum from migration and diversifica- vector; wind, rafting via ocean currents and transport tion in closely similar environments, referred to as by birds are the three most commonly postulated ‘niche conservatism’ (Harvey & Pagel, 1991; Wiens & mechanisms (Carlquist, 1967; Renner, 2004; Nathan Donoghue, 2004), or ‘biome conservatism’ when con- et al., 2008; Baldwin & Wagner, 2010). A summary of sidered on a global scale (Crisp et al., 2009), to adap- mechanisms for transport of plants to Hawaii, one of tation to rather different environmental settings, the most remote oceanic island archipelagos, which referred to as ‘niche evolution’ (Wiens & Donoghue, was populated (prior to arrival of the first Polyne- 2004). Niche conservation has been shown to be asso- sians) entirely by long-distance dispersed propagules, ciated with recently diversified groups in South indicates that transport by birds can account for c. America (e.g. Inga Mill. – Richardson et al., 2001; 75% of all immigrants, with wind and ocean drift Coursetia DC – Lavin et al., 2003; Lavin, 2006; Vale- accounting for the remainder (Gillespie et al., 2012). rianaceae – Bell & Donoghue, 2005; Lupinus L. – Disjunctions between North and South America have Hughes & Eastwood, 2006; Cinchoneae – Andersson also been attributed mainly to transport by birds & Antonelli, 2005; Calceolaria L. – Andersson, 2006) (Carlquist, 1967; Raven, 1972; Wen & Ickert-Bond, and may be a major determinant in the pattern 2009; Cody et al., 2010). However, Renner (2004) recognized by Gentry (1982) that there is a significant reviewed the putative long-distance dispersed dis- taxonomic division between Andean and Amazonian juncts between tropical Africa and South America and floras. At the other end of this continuum, niche concluded that dispersal by rafting on ocean currents evolution, the adaptive shifts between ecological is likely to have been more common than dispersal by zones, has been important in the adaptation of plants birds or wind. Whereas wind can be an effective into geologically new ecosystems, such as oceanic mechanism for seed dispersal in some species, islands (Carlquist, 1974; Baldwin et al., 1998) and the reviews suggest that it is rarely effective for long- cerrado of South America (Simon et al., 2009), but distance, over-water dispersal (Renner, 2004; Nathan may prove to be a barrier to entry into established et al., 2008; Gillespie et al., 2012). From a local, eco- ecosystems with well-developed floras (Antonelli logical perspective, animal-dispersed fruits/seeds, et al., 2009; Antonelli & Sanmartin, 2011). Under- including fleshy fruits or fruits/seeds with mecha- standing the course of diversification of large clades nisms for sticking to the body of an animal, are and the balance between ecological shifts and diver- considered to be more effective for medium- to long- sification in similar habitats can offer insight into the distance seed dispersal than are fruits/seeds lacking relative importance of these processes. any such mechanism (Nathan et al., 2008), although As reviewed by Pennington & Dick (2004) and in such fruits/seeds may have an alternative dispersal the present volume by Christenhusz & Chase (2012), mechanism, such as hitch-hiking on a rafted sub- explanations for intercontinental disjunctions involv- strate, and modelling long-distance dispersal is ing South American plant groups with distributions fraught with difficulty (Levin et al., 2003). on other continents typically involve either relict South America has a long history of geographical Gondwanan distributions (Gentry, 1982), migration isolation from other continental land masses and has routes involving northern hemisphere continental a biota that reflects that isolation, exemplified most connections (Renner et al., 2001; Davis et al., 2002) or iconically by its mammal fauna (Simpson, 1980). Its over-water, long-distance dispersal (Givnish et al., link to Gondwana was severed about 100 Mya when 2004; Renner, 2004; Särkinen et al., 2007). A continu- South America and Africa separated and began to ous land connection to North America has existed drift apart (Goldblatt, 1993; Burnham & Graham, with certainty only since the closure of the Isthmus of 1999; Morley, 2003), even though east–west running Panama (c. 3 Mya), so, for groups that originated in archipelagos (Walvis Ridge/Rio Grande rise and South America after the split up of Gondwana, except Sierra Leone rise) derived from volcanic hotspots on for very recent migrants to North America, virtually or near the mid-Atlantic ridge may have permitted all emigration required over-water dispersal (Cody stepping stone migration perhaps until c. 70 Mya (e.g. et al., 2010). However, recent evidence (Farris et al., Morley, 2003; Pennington & Dick, 2004), when the 2011; Montes et al., 2012) suggests that there may mid-Atlantic ridge moved off the stationary hotspot have been a continuous land connection as early as c. that formed the Walvis Ridge/Rio Grande rise © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 171, 80–102 82 R. G. OLMSTEAD (O’Connor & Duncan, 1990). After the opportunities sphere, (2) the importance of niche conservatism and for short-distance, over-water migration with Africa adaptive shifts between ecological zones for explain- waned in the Cretaceous and early Tertiary, such ing current distribution patterns, (3) the success of opportunities arose again, this time with North transoceanic, long-distance dispersal to