ORIGINAL RESEARCH ARTICLE published: 28 November 2014 doi: 10.3389/fgene.2014.00409 To move or to evolve: contrasting patterns of intercontinental connectivity and climatic niche evolution in “Terebinthaceae” (Anacardiaceae and Burseraceae) Andrea Weeks 1*, Felipe Zapata 2, Susan K. Pell 3, Douglas C. Daly 4, John D. Mitchell 4 and Paul V. A. Fine 5 1 Department of Biology and Ted R. Bradley Herbarium, George Mason University, Fairfax, VA, USA 2 Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA 3 United States Botanical Garden, Washington, DC, USA 4 Institute of Systematic Botany, The New York Botanical Garden, Bronx, NY, USA 5 Department of Integrative Biology and Jepson and University Herbaria, University of California, Berkeley, CA, USA Edited by: Many angiosperm families are distributed pantropically, yet for any given continent Toby Pennington, Royal Botanic little is known about which lineages are ancient residents or recent arrivals. Here Garden Edinburgh, UK we use a comprehensive sampling of the pantropical sister pair Anacardiaceae and Reviewed by: Burseraceae to assess the relative importance of continental vicariance, long-distance Matthew T. Lavin, Montana State University, USA dispersal and niche-conservatism in generating its distinctive pattern of diversity over Wolf L. Eiserhardt, Royal Botanic time. Each family has approximately the same number of species and identical stem Gardens, Kew, UK age, yet Anacardiaceae display a broader range of fruit morphologies and dispersal *Correspondence: strategies and include species that can withstand freezing temperatures, whereas Andrea Weeks, Department of Burseraceae do not. We found that nuclear and chloroplast data yielded a highly supported Biology, George Mason University, 4400 University Drive, 3E1, Fairfax, phylogenetic reconstruction that supports current taxonomic concepts and time-calibrated VA 22030, USA biogeographic reconstructions that are broadly congruent with the fossil record. We e-mail: [email protected] conclude that the most recent common ancestor of these families was widespread and likely distributed in the Northern Hemisphere during the Cretaceous and that vicariance between Eastern and Western Hemispheres coincided with the initial divergence of the families. The tempo of diversification of the families is strikingly different. Anacardiaceae steadily accumulated lineages starting in the Late Cretaceous–Paleocene while the majority of Burseraceae diversification occurred in the Miocene. Multiple dispersal- and vicariance-based intercontinental colonization events are inferred for both families throughout the past 100 million years. However, Anacardiaceae have shifted climatic niches frequently during this time, while Burseraceae have experienced very few shifts between dry and wet climates and only in the tropics. Thus, we conclude that both Anacardiaceae and Burseraceae move easily but that Anacardiaceae have adapted more often, either due to more varied selective pressures or greater intrinsic lability. Keywords: biogeography, biome shifts, continental vicariance, diversification, long-distance dispersal, phylogenetic niche conservatism INTRODUCTION Moreover, the timing and directionality of such dispersal events A richer understanding of factors underlying the origin of the is often unknown, although recent studies have found that many diverse tropical flora depends on aggregating global biogeo- tropical radiations appear to have coincided with climatic and graphic, taxonomic and phylogenetic information from multiple geographic events, such as Oligocene–Miocene cooling and dry- plant clades. Although much progress has been made recon- ing in both the Americas and Africa, the connection of North structing the tempo and genealogical patterns of angiosperm and South America, and the Andean uplift (Bouchenak-Khelladi evolution in the past two decades, most of the major plant lin- et al., 2010; Hoorn et al., 2010; De-Nova et al., 2012; Hughes et al., eages lack the comprehensive global sampling and taxonomic 2013). studies necessary to address basic questions regarding the timing Recent studies have highlighted the importance of phyloge- of radiations, geographic origins, and dispersal histories. Many netic niche conservatism in understanding large-scale patterns of angiosperm families are common to tropical forests around the plant biogeography and evolution (Wiens and Donoghue, 2004; world, yet very little is known about which lineages are ancient Donoghue, 2008). The hypothesis is that because adaptation to and have experienced multiple vicariance events, and which new climatic zones requires a complex array of morphological lineages have experienced more recent long-distance dispersal. and physiological innovations, as long as dispersal is possible, www.frontiersin.org November 2014 | Volume 5 | Article 409 | 1 Weeks et al. Biogeography and evolution of “Terebinthaceae” in situ adaptation by the resident flora during periods of global 2011). This disparity is primarily responsible for the recognition cooling or drying may often be less common than immigration of more genera in Anacardiaceae (82) as compared to Burseraceae of other lineages that are pre-adapted to freezing or dry climates. (19), although each family has approximately the same number For example, many Northern American temperate plant lineages of species. However, the geographic range as well as the mor- have colonized the high-elevation South American Andes since phological and ecological diversity of Anacardiaceae considerably overland connections were established between the two conti- eclipses that of Burseraceae, which makes the Terebinthaceae nents (Bell and Donoghue, 2005; Hughes and Eastwood, 2006). lineage a valuable comparative model system for testing the rel- However, South American lineages have also colonized these ative contributions to diversification of climate adaptation and freezing habitats, even from warm tropical lowlands (Donoghue, intercontinental movement. 2008), demonstrating that adaptation to new biomes, as well as The differences between the families raise the question of immigration from other areas, can result in diversification within how sister lineages having identical ages and nearly equivalent regions (Donoghue, 2008; Donoghue and Edwards, 2014). numbers of species could have taken such different evolution- The angiosperm lineages Anacardiaceae and Burseraceae ary trajectories whilst becoming so widespread. Anacardiaceae (Sapindales) represent an excellent study system for investi- comprise a cosmopolitan group, are found at a greater range of gating the biogeographic history of tropical diversification and latitudes and elevations, and a broader range of habitats than the relative importance of movement and climatic adaptation Burseraceae. All Burseraceae, by contrast, are intolerant of frost in angiosperm evolution. Once recognized as the single taxon and are thus limited to lower elevation zones in the African, “Terebinthaceae” (Marchand, 1869) and subsequently shown to American, Asian and Pacific (sub-)tropics. be sister taxa (Fernando et al., 1995; Gadek et al., 1996; Bremer Testing which events may have been correlated with cladogen- et al., 1999; Savolainen et al., 2000a,b; Pell, 2004), these families esis in Terebinthaceae is contingent on reconstructing a densely collectively comprise ca. 1500 lianas, shrubs and trees distributed sampled, time-calibrated phylogeny for the group. Divergence on every continent except Antarctica and are major elements of time estimates are a critical component of testing historical bio- the structure and diversity of temperate, seasonally dry tropical geographic hypotheses for Terebinthaceae because routes of over- forest and tropical wet forest floras (Gentry, 1988; Pennington land range expansion available to Anacardiaceae and Burseraceae et al., 2010)(Figure 1). Anacardiaceae species display a remark- may have been different as global climate fluctuated over geo- able range of fruit morphologies and seed dispersal syndromes logical time. For example, ancestral lineages of frost tolerant not present in Burseraceae (see Daly et al., 2011; Pell et al., Anacardiaceae may have been able to disperse through regions FIGURE 1 | (A) Global distribution of Anacardiaceae and Burseraceae (red Protium, Bursera and Boswellia nuculaniums; 3, Garuga drupe; 4, area is Anacardiaceae only, blue is Burseraceae only, and gray is where Solenocarpus drupe; 5, Spondias, internally operculate drupe; 6, the two families’ distributions overlap), and fossils used to calibrate the Dracontomelon, externally operculate drupe; 7, Loxostylis, drupe subtended phylogenies in this study (1, Oligocene/Late Eocene Cotinus leaf; 2, Middle by wing-like calyx; 8, Anacardium, drupe subtended by fleshy hypocarp; 9, Miocene Loxopterygium fruit; 3, Middle Eocene Anacardium fruit; 4, Campylopetalum, drupe subtended by an accrescent bract; 10, Swintonia, Middle Eocene Bursericarpum aldwickense and Protocommiphora europea drupe subtended by wing-like corolla; 11, Schinopsis, samara.) (illustrations fruits; 5, Middle Eocene Bursera subgenus Elaphrium leaf). (B) Fruit 1–7 and 10–11 from Engler, 1883; 8 from Faguet, 1874/1875; 9 copyright diversity in Anacardiaceae and Burseraceae (1, Triomma pseudocapsule; 2, Bobbi Angell). Frontiers in Genetics | Evolutionary and Population Genetics November 2014 | Volume 5 | Article 409 | 2 Weeks et al. Biogeography and evolution of “Terebinthaceae” located above the frost line during