The tropical Andean plant diversity powerhouse

Regardless of what measures of species richness and endemicity are used, the tropical Andes stand out as a global plant diversity hotspot, possibly the hottest hotspot on the planet. This spectacular diversity of plant species and their altitudinal zonation, as well as the steep and extended environmental gradients found in the equatorial Andes, are graphically portrayed on a single page in Alexander von Humboldt's iconic and richly annotated cross-sectional profile of the Andes (Fig. 1; Humboldt & Bonpland, 1807), first sketched soon after his intrepid ascent of Volcán Chimborazo in Ecuador in 1802. Humboldt was one of the first natural historians to make detailed observations about the locations and climates of plant species, and to suggest the importance of geography and ecology for understanding plant diversity. More than 200 years later, the divergent evolutionary histories of these ecologically distinct but geographically juxtaposed Andean vegetation zones, and of the tropical Andean biodiversity hotspot as a whole, are only now emerging. Based on expanding sets of plant phylogenies, especially for high elevation grassland and lowland seasonally dry tropical forest lineages, it is becoming clear that diversification of lineages characteristic of different Andean biomes have followed very different geotemporal trajectories (Pennington et al., 2010; Särkinen et al., 2012; Luebert & Weigend, 2014), all of them related to the history of Andean uplift, but potentially in rather different ways. In this issue of New Phytologist, Lagomarsino et al. (pp. 1430–1442) present important new data that shed light on the trajectories and likely drivers of plant diversification in the third principal Andean biome, the mid-elevation Andean montane forests, which remain poorly understood. Their study of diversification of a species-rich clade of Andean bellflowers contributes to filling this important gap in our understanding of Andean plant diversification and to establishing a more complete integrative framework of the evolutionary diversification of the tropical Andean diversity hotspot as a whole.

The Andean bellflowers (Fig. 2) studied by Lagomarsino et al. form a clade of c. 600 species of herbs, woody vines, shrubs and small trees, displaying remarkable floral diversity associated with insect-, bat- and hummingbird-pollination syndromes, and fruits adapted to both abiotic and animal seed dispersal. The vast majority of these bellflower species are concentrated in the Andean montane forests which are distributed at mid-elevations in an extended and more or less continuous belt along the eastern flanks of the Andes from Venezuela to Bolivia, sandwiched between the lowland tropical rain forest and the treeline. Lagomarsino et al. generate an impressively sampled time-calibrated phylogeny for this clade, and use this to model speciation and extinction rates and to test a set of hypotheses about possible extrinsic abiotic geohistorical and intrinsic biotic drivers of diversification. They show that the large majority of Andean bellflowers form a species-rich clade with an elevated species diversification rate indicative of a large radiation centred in the montane forests of the Andes that started in the late Miocene or early Pliocene. The handful of recently published phylogenies of other plant groups that include Andean montane forest species – the core Tillansioid clade of Bromeliaceae (Givnish et al., 2014), the mostly Andean Neotropical Vaccinieae (Ericaceae) (Schwery et al., 2015), the Oreinotinus clade of Viburnum (Adoxaceae) (Spriggs et al., 2015) and Andean supersection Tacsonia of Passiflora (Passifloraceae) (Abrahamczyk et al., 2014), show remarkably similar patterns of rapid species diversification in Andean montane forests dating from the late Miocene. Together these studies suggest that rapid late Miocene to Pliocene species radiations have been an important component of evolutionary diversification in these Andean mid-elevation montane forests.

The idea that mountain uplift can trigger diversification and provide ‘key landscapes’ (sensu Givnish, 1997) for generating high species richness is certainly not unique to this study (e.g. Hughes & Eastwood, 2006; Hutter et al., 2013; Merckx et al., 2015; Schwery et al., 2015). It has also been previously suggested that species diversification tracks mountain uplift (Antonelli et al., 2009), but the Lagomarsino et al. study is unique in modelling and testing the rate of mountain uplift as a possible determinant of diversification. Perhaps the most striking finding of the Lagomarsino et al. study is the remarkably close correlation between the trajectories of Andean uplift and species diversification. Their estimates of rates of Andean uplift and rates of bellflower diversification through time show contemporaneous peaks in the late Miocene/early Pliocene, and a signal of paleoelevation-dependent diversification. The Andean montane forests are often referred to as cloud forests because of the persistent cloud cover that shrouds these forests in mist throughout most of the year. It is thought that this humid or perhumid climate regime was established from the late Miocene onwards, when the Andes reached a sufficient elevation to form a barrier for Amazonian moisture. The establishment and expansion of these forests at that time provided a likely trigger for diversification in the Andean montane forest biome including for the Andean bellflower and other plant radiations that originated during that period. This suggests that the coincidence of peak rates of mountain uplift and the onset of the cloud forest climatic regime may be no more than that – a coincidence, and that the impact of mountain uplift on species diversification was much less direct than implied by the striking correlation between rates of mountain uplift and rates of bellflower species diversification.

Despite the fact that links between rates of mountain uplift and species diversification are likely to be complex and indirect, there is no doubt that rates and trajectories of plant diversification in the Andes, whether it is in the high elevation grasslands, low elevation seasonally dry tropical forests, or mid-elevation montane forests, have been fundamentally influenced and determined by the uplift of the Andes. The emerging framework of tropical Andean plant diversification closely tracks the appearance and expansion of these different biomes as their respective altitudinal zones emerged during the uplift of the Andes (Pennington et al., 2010; Särkinen et al., 2012; Luebert & Weigend, 2014). In the low elevation seasonally dry tropical forests of the deeply entrenched inter-Andean valleys we find old, mid-Miocene, slowly diversifying, species-poor but endemic-rich clades (Pennington et al., 2010; Särkinen et al., 2012). Somewhat younger and faster species-rich, late Miocene or early Pliocene radiations characterize the mid-elevation montane forests, as documented by Lagomarsino et al. Finally, the very young, high elevation Andean grassland biome, dubbed by Madriñán et al. (2013), as the world's fastest evolving and coolest biodiversity hotspot, is characterized by numerous species-rich clades that have radiated very rapidly in the Pliocene and Pleistocene (Madriñán et al., 2013; Luebert & Weigend, 2014; Hughes & Atchison, 2015).

One notable exception to this framework is the middle Miocene age and the consequently slow diversification rate estimates for the genus Lysipomia in the Lagomarsino et al. study. Lysipomia, a clade of c. 30 species restricted to the Andean grasslands above 3000 m, has previously been considered a typical recent rapid high-elevation Andean radiation (Madriñán et al., 2013). The most likely explanation for Lagomarsino et al.'s surprisingly old age estimate is that the high substitution rate heterogeneity between Lysipomia (a long-branch clade) and the main centropogonid clade (a short branch clade) has not been fully accounted for in their divergence time analysis. If the age of Lysipomia is over-estimated, there are likely to be important knock-on effects in terms of estimating diversification rates, locating diversification rate shifts and for testing for trait (and especially pollinator) dependent diversification.

Despite these doubts surrounding the age of Lysipomia, there is no doubt that the large Centropogonid clade of Andean bellflowers represents a spectacularly species-rich, late Miocene–Pliocene Andean montane forest radiation. Seehausen (2015) recently proposed a conceptual model of species diversification that might account for exceptionally rapid evolutionary radiations such as those in the Andean cloud forests. He suggested that rapid plant species diversification is likely when phenotypically diverse and versatile populations with access to a diverse assemblage of pollinators invade adaptive landscapes with exceptional spatial and resource heterogeneity. It is striking how closely these conditions are met in the case of the Andean bellflower radiation. Lagomarsino et al. show that there is pollinator partitioning among species, with shifts between insect-, hummingbird- and bat-pollination syndromes during the diversification of the Andean bellflowers. These plants are also phenotypically extremely versatile in growth habit, forming herbs, shrubs, trees and vines. Finally, the steep and extensive multi-dimensional environmental gradients of the tropical Andes spanning > 4000 km north to south and 5000 m of altitude, with their associated extreme physiographic (habitat and topographic) heterogeneity, present exceptional opportunities for rapid diversification of species.

As depicted by Humboldt & Bonpland in their 1807 tableau, in a single transect over the Andes one can traverse from tropical (hyper arid or hyper wet) to temperate montane and tropical alpine habitats, with these radically different vegetation types juxtaposed immediately adjacent to each other over 1000s of kilometres. As pursued by Hutter et al. (2013), these readily quantifiable multi-dimensional environmental gradients present unusual opportunities for teasing apart, quantifying and testing the relative contributions of geography and ecology, of phylogenetic niche conservatism vs niche evolution, of allopatric vs ecological speciation and of adaptive vs non-adaptive radiation, in determining the distribution of diversity and the turnover of clades. In other words, the tropical Andes provide an excellent living laboratory for studying evolutionary diversification and for understanding the historical assembly of one of the world's most exceptional plant diversity hotspots.