Origin and global diversification patterns of tropical rain forests: inferences from a complete genus-level phylogeny of palms

Abstract

Background: Understanding how biodiversity is shaped through time is a fundamental question in biology. Even though tropical rain forests (TRF) represent the most diverse terrestrial biomes on the planet, the timing, location and mechanisms of their diversification remain poorly understood. Molecular phylogenies are valuable tools for exploring these issues, but to date most studies have focused only on recent time scales, which minimises their explanatory potential. In order to provide a long-term view of TRF diversification, we constructed the first complete genus-level dated phylogeny of a largely TRF-restricted plant family with a known history dating back to the Cretaceous. Palms (Arecaceae/Palmae) are one of the most characteristic and ecologically important components of TRF worldwide, and represent a model group for the investigation of TRF evolution.

Results: We provide evidence that diversification of extant lineages of palms started during the mid-Cretaceous period about 100 million years ago. Ancestral biome and area reconstructions for the whole family strongly support the hypothesis that palms diversified in a TRF-like environment at northern latitudes. Finally, our results suggest that palms conform to a constant diversification model (the 'museum' model or Yule process), at least until the Neogene, with no evidence for any change in diversification rates even through the Cretaceous/Paleogene mass extinction event.

Conclusions: Because palms are restricted to TRF and assuming biome conservatism over time, our results suggest the presence of a TRF-like biome in the mid-Cretaceous period of Laurasia, consistent with controversial fossil evidence of the earliest TRF. Throughout its history, the TRF biome is thought to have been highly dynamic and to have fluctuated greatly in extent, but it has persisted even during climatically unfavourable periods. This may have allowed old lineages to survive and contribute to the steady accumulation of diversity over time. In contrast to other plant studies, our results suggest that ancient and steady evolutionary processes dating back to the mid-Cretaceous period can contribute, at least in part, to present day species richness in TRF.

Figure 1

Lineage-through-time (LTT) plots for three alternative hypothetical diversification models of tropical rain forest (TRF) evolution. (1) Decrease in diversification rates since origin with early radiation; 'ancient cradle model'; (2) constant diversification rate, 'museum model'; (3) increase in diversification rates since origin with recent radiation; 'recent cradle model'.

Figure 2

Example of an understory lowland tropical rain forest in the Parque National do Amazonia (near Itaituba, Pará state, Brazil) dominated by palms. Foreground Bactris acanthocarpa var. exscapa, upper right corner Attalea sp., middle left Euterpe precatoria, background: Astrocaryum gynacanthum. Photo: TLPC.

Figure 3

Area, tempo and mode of palm diversification. (a) Paleomap representing the distribution of landmasses in the mid-Cretaceous period, dark grey upland land, light grey lowland (100 million years (Ma), adapted from Beerling and Woodward [60]). Laurasia, which is the most likely ancestral area reconstructed for the crown node of palms, is highlighted. (b) Chronogram showing the three different biomes assigned to each genus. Red: tropical rain forest; green: mangrove; blue: not tropical rain forest; grey: ambiguous. Yellow circles indicate fossil calibration points. The vertical black lines highlight the five subfamilies of palms with an illustration (drawings by Marion Ruff Sheehan, L.H. Bailey Hortorium, Cornell University, except top one (Arecoideae), which is reproduced with permission from Springer from Kahn and de Granville [30]. (c) Semilogarithmic mean lineage-through-time (LTT) plot averaged over 1,000 posterior trees from the Bayesian analysis (left axis, triangles) and percentage of missing taxa as a function of time (right axis, grey line). Short dashed line = upper 95% confidence interval; long dashed line = lower 95% confidence interval; filled square = extant number of palms species. Vertical black line indicates threshold up to which the LTT plot is considered reliable even under incomplete taxon sampling. Palm fossil indicates time of earliest known unequivocal fossil for the family (Sabalites fossil leaf image reproduced by permission of the Board of Trustees, National Museums Liverpool, Liverpool, UK).