Introduction

Species richness is unevenly distributed in time (Simpson, 1953), space (Willis, 1922) and across the Tree of Life (Vargas & Zardoya, 2014). An understanding of the processes underlying current patterns in species richness and distribution therefore constitutes a major scientific challenge. The Andean mountains of South America contain c. 15% of the world's plant species, in only 1% of the world's land surface, resulting in the most species‐rich biodiversity hotspot worldwide (Myers et al., 2000). A large proportion of this diversity is found in high‐altitude grasslands, and is suggested to have resulted from recent rapid speciation events (Hughes & Eastwood, 2006; Hughes & Atchison, 2015). By contrast, Andean seasonally dry forests experienced much slower diversification and have older origins (Pennington et al., 2010), suggesting contrasted macroevolutionary histories within the Andean biodiversity hotspot (Valencia et al., 1994; Pennington et al., 2010; ter Steege et al., 2013).

In a seminal paper, Gentry (1982) postulated that mountain uplift was a major trigger of Andean mega‐diversity, although he posited that this might have occurred indirectly via biotic interactions. A pivotal result of Gentry's floristic analyses was the discovery of two patterns of plant distribution in the Neotropics: ‘Amazonian‐centred’ and ‘Andean‐centred’ taxa. Amazonian‐centred taxa consist mostly of canopy trees and lianas, whereas Andean‐centred taxa are almost exclusively epiphytes and shrubs (Gentry, 1982). The latter occur mostly in the Northern Andes, with secondary centres in the Brazilian coastal mountains and Central America, together accounting for c. 33% of all Neotropical plants (Gentry, 1982), and thus largely contributing to the world's most species‐rich biodiversity hotspot, the tropical Andes (Myers et al., 2000).

Contrasting with the dominant views at the time, Gentry (1982) hypothesized that the Andean‐centred flora resulted from ‘recent, very dynamic speciation’, a hypothesis that we test here. Gentry & Dodson (1987) further suggested that the high diversity of epiphytes in the Northern Andes and southern South America could have resulted from the finer niche partitioning in these forests, allowing for high alpha diversity, the high microsite differentiation of mountain areas, fostering high beta diversity, and explosive speciation driven by genetic founder effects because of the environmental dynamicity, implying frequent relocation.

Orchids are one of the most characteristic and diverse components of the Andean flora (Gentry & Dodson, 1987; Krömer & Gradstein, 2003; Richter et al., 2009; Parra‐Sánchez et al., 2016). They often make up 30–50% of the total epiphytic species number reported along the Northern Andes (Kreft et al., 2004; Küper et al., 2004), and epiphytic orchids account for 69% of all vascular epiphytes world‐wide (Zotz & Winkler, 2013). Neotropical epiphytic orchids are generally characterized by narrowly restricted populations with small numbers of individuals (Tremblay & Ackerman, 2001; Jost, 2004; Crain & Tremblay, 2012; Pandey et al., 2013). Despite the ecological importance and prominence of epiphytic orchids (and of epiphyte diversity overall) in the Andean flora, their origin and diversification have not been explicitly studied because of the difficulties in generating densely sampled and strongly supported phylogenies.

We address these issues by studying the evolutionary history of the two largest Neotropical orchid clades, namely Cymbidieae and Pleurothallidinae. The Cymbidieae comprise over 3700 species, 90% of which occur in the Neotropics (the remaining species occur in tropical Africa and Australasia). Cymbidieae comprise 12 subtribes, four of which are the most speciose and include Andean‐dwelling subclades (i.e. Maxillariinae, Oncidiinae, Stanhopeinae and Zygopetalinae; Pridgeon et al., 2009). Pleurothallidinae comprise 44 genera and 5100 exclusively Neotropical species (Karremans, 2016) distributed mostly in the highlands of the Northern Andes and Central America. Together, they are the most representative elements of the Andean orchid flora (Pérez‐Escobar et al., 2009; Pridgeon et al., 2009; Kolanowska, 2014) and make up most of their species richness. In addition, these lineages have evolved a rich array of pollination syndromes and mating systems (including protandry, unisexuality, cleistogamy; Gerlach & Schill, 1991; Borba et al., 2011; Pérez‐Escobar et al., 2016a) that have long fascinated botanists and naturalists (Lindley, 1843; Darwin, 1877). This is particularly true for Cymbidieae, in which up to seven pollination syndromes have been recorded (van der Cingel, 2001; Pridgeon et al., 2009), ranging from species exclusively pollinated by male euglossine bees (Ramírez et al., 2011) to those pollinated only by oil bees. Data on the pollination ecology of Pleurothallidinae are very scarce, but scattered reports across the clade suggest that they are mostly pollinated by a vast array of dipteran lineages (Blanco & Barboza, 2005; Pupulin et al., 2012).

Rapid Andean orogeny could have promoted orchid species richness by creating ecological opportunities, such as increasing the landscape, mediating local climate change, creating novel habitats and forming insular environments that affected migrations and allopatric speciation through isolation (Gentry & Dodson, 1987; Hoorn et al., 2013). This effect should have been most accentuated over the last 10 million yr (Ma), during which c. 60% of the current elevation of the Andes was achieved (Gregory‐Wodzicki, 2000). Diversification studies of Andean‐centred clades have provided evidence for rapid diversification that temporally matches the Andean surface uplift, for instance in the plant genera Lupinus, Espeletia, Halenia and Heliotropium, and in the families Campanulaceae and Annonaceae (von Hagen & Kadereit, 2003; Bell & Donoghue, 2005; Donoghue & Winkworth, 2005; Hughes & Eastwood, 2006; Pirie et al., 2006; Antonelli et al., 2009b; Luebert et al., 2011; Drummond et al., 2012; Madriñán et al., 2013; Lagomarsino et al., 2016; Diazgranados & Barber, 2017). Taken together, these studies suggest that rapid Andean uplift yielded new niches that fostered both adaptive and non‐adaptive radiations (Nevado et al., 2016). Other Andean groups, such as hummingbirds, diversified mostly before Andean uplift (McGuire et al., 2014) or after it had attained most of its current height (Smith et al., 2014).

We address the impact of the Andean uplift on the diversity and distribution of orchids by inferring the dynamics of speciation, extinction and migration, whilst simultaneously incorporating surface uplift of the two largest Andean Neotropical orchid clades Cymbidieae and Pleurothallidinae. We rely on model‐based inference methods in historical biogeography, ancestral area and character estimation approaches, and a series of diversification analyses to investigate the following questions. From which geographical area(s) do Andean orchids mostly originate? Is there evidence for the Andes acting as a dispersal barrier for epiphytic lowland taxa? Did the Andean uplift enhance orchid diversification and, if so, was this effect evident on all species from the Andean region or just those from the highest elevations? Is Andean diversity derived from pre‐adapted (i.e. high elevation) lineages or rather descendants of lowland migrants (either local or from other areas)? In addition, we use the limited available data to evaluate whether shifts in pollination syndromes are associated with changes in diversification rates.

Our results support Gentry's prediction (Gentry, 1982) that Andean‐centred groups have resulted from recent rapid speciation, suggesting that Andean orogeny provided opportunities for rapid orchid species diversification in the world's premier plant biodiversity hotspot. Such diversity is derived from lowland lineages but, more rarely, from migrants already pre‐adapted to cool environments, a more frequent situation documented from other mountain environments (Merckx et al., 2015).