Tracing the impact of the Andean uplift on Neotropical plant evolution

Abstract

Recent phylogenetic studies have revealed the major role played by the uplift of the Andes in the extraordinary diversification of the Neotropical flora. These studies, however, have typically considered the Andean uplift as a single, time-limited event fostering the evolution of highland elements. This contrasts with geological reconstructions indicating that the uplift occurred in discrete periods from west to east and that it affected different regions at different times. We introduce an approach for integrating Andean tectonics with biogeographic reconstructions of Neotropical plants, using the coffee family (Rubiaceae) as a model group. The distribution of this family spans highland and montane habitats as well as tropical lowlands of Central and South America, thus offering a unique opportunity to study the influence of the Andean uplift on the entire Neotropical flora. Our results suggest that the Rubiaceae originated in the Paleotropics and used the boreotropical connection to reach South America. The biogeographic patterns found corroborate the existence of a long-lasting dispersal barrier between the Northern and Central Andes, the "Western Andean Portal." The uplift of the Eastern Cordillera ended this barrier, allowing dispersal of boreotropical lineages to the South, but gave rise to a huge wetland system ("Lake Pebas") in western Amazonia that prevented in situ speciation and floristic dispersal between the Andes and Amazonia for at least 6 million years. Here, we provide evidence of these events in plants.

Fig. 1.

Combined chronogram and biogeographic analysis of Neotropical Rubiaceae. The tree is the 50% majority-rule consensus (with compatible groups added) from the Bayesian analysis, with branches proportional to absolute ages (in millions of years) calculated from mean branch lengths of 6,000 Bayesian trees. Green bars indicate 95% confidence intervals of node ages estimated from 1,000 trees randomly sampled from the Bayesian stationary distribution. Node charts show the relative probabilities of alternative ancestral distributions obtained by integrating dispersal-vicariance analysis (DIVA) optimizations over the 1,000 Bayesian trees; the first 4 areas with highest probability are colored according to their relative probability in the following order: white > red > blue > gray; any remaining areas (usually frequencies <0.01) are collectively given with black color. Stars indicate calibration points. Red arrows indicate clades with a posterior probability <0.90. Present ranges for each species are given after the species name. Brackets identify subfamilies and tribes: CHI, Chiococceae; CIN, Cinchoneae; GUE, Guettardeae; HAM, Hamelieae; HIL, Hillieae; ISE, Isertieae; NAU, Naucleeae; RON, Rondeletieae. Shaded boxes indicate approximate periods of Andean uplift phases. The biogeographic interpretation of events I–V is summarized in Fig. 2. (Inset) Areas used in the biogeographic analysis. A, Central America, B, West Indies; C, Northern Andes; D, Central Andes; E, Chocó; F, Amazonia; G, The Guiana Shield; H, Southeastern South America; I, Temperate North America; J, Africa; K, Australasia. Topographic map from the National Geophysical Data Center (www.ngdc.noaa.gov).

Fig. 2.

Spatiotemporal evolution of the Neotropical Rubiaceae. (I) Paleocene: Rubiaceae ancestors use the boreotropical route to reach North America from the Paleotropics. (II) Early Eocene: Dispersal into South America, presumably facilitated by occasional island chains. (III) Late Eocene: North Andean and Amazonian lineages become isolated by marine incursions such as the Western Andean Portal (WAP). (IV) Middle Miocene: The gradual uplift of the Eastern Cordillera creates a huge watershed, Lake Pebas (LP). It also closes the WAP, enabling dispersal of plant lineages from the Northern to the Central Andes. (V) The Pebas system drains, promoting land dispersal of several lineages and rapid speciation of terrestrial plants in western Amazonia. Area codings as in Fig. 1. (Maps I–II are based on C. R. Scotese's PALEOMAP project (www.scotese.com); maps III–V modified from refs. and 28).