Molecular phylogenetics reveal multiple tertiary vicariance origins of the African rain forest trees

Abstract

Background: Tropical rain forests are the most diverse terrestrial ecosystems on the planet. How this diversity evolved remains largely unexplained. In Africa, rain forests are situated in two geographically isolated regions: the West-Central Guineo-Congolian region and the coastal and montane regions of East Africa. These regions have strong floristic affinities with each other, suggesting a former connection via an Eocene pan-African rain forest. High levels of endemism observed in both regions have been hypothesized to be the result of either 1) a single break-up followed by a long isolation or 2) multiple fragmentation and reconnection since the Oligocene. To test these hypotheses the evolutionary history of endemic taxa within a rain forest restricted African lineage of the plant family Annonaceae was studied. Molecular phylogenies and divergence dates were estimated using a Bayesian relaxed uncorrelated molecular clock assumption accounting for both calibration and phylogenetic uncertainties.

Results: Our results provide strong evidence that East African endemic lineages of Annonaceae have multiple origins dated to significantly different times spanning the Oligocene and Miocene epochs. Moreover, these successive origins (c. 33, 16 and 8 million years--Myr) coincide with known periods of aridification and geological activity in Africa that would have recurrently isolated the Guineo-Congolian rain forest from the East African one. All East African taxa were found to have diversified prior to Pleistocene times.

Conclusion: Molecular phylogenetic dating analyses of this large pan-African clade of Annonaceae unravels an interesting pattern of diversification for rain forest restricted trees co-occurring in West/Central and East African rain forests. Our results suggest that repeated reconnections between the West/Central and East African rain forest blocks allowed for biotic exchange while the break-ups induced speciation via vicariance, enhancing the levels of endemicity. These results provide an explanation for present day distribution patterns and origins of endemicity for African rain forest trees. Moreover, given the pre-Pleistocene origins of all the studied endemic East African genera and species, these results also offer important insights for setting conservation priorities in these highly diversified but threatened ecosystems.

Figure 1

Alternative hypotheses of African rain forest origins. (A) Distribution of lowland rain forest in Africa (black) overlaid by altitudinal range (increasing altitude with darker grey). Red lines highlight the Guineo-Congolian region; the blue line highlights the East African region. (B) Phylogenetic tree expected from a single break-up scenario. (C) Phylogenetic tree expected from multiple break-ups at significantly different times scenario. Open circles indicate West-Central/East splits.

Figure 2

Estimated divergence times within African Annonaceae. Maximum clade credibility chronograms, with nodes represented by their mean ages estimated under a relaxed lognormal uncorrelated molecular clock assumption. East African endemic taxa are indicated in blue, West and Central African taxa in red, taxa endemic to Madagascar in black. Solid circles indicate nodes used for calibration of the trees. Open circles indicate nodes for which divergence dates were estimated. Thick branches lead to nodes with more than 0.95 posterior probability support. Geological Epochs, shaded bars: Paleo., Paleocene; Oligo., Oligocene; Pli., Pliocene; Pleis., Pleistocene. (A) Genus-level chronogram showing phylogenetic relationships within the African clade. (B) Species-level chronogram of the two sister genera Isolona and Monodora. (C) posterior distributions of the estimated ages. The 95% highest posterior density (HPD) intervals are indicated with black bars and given between brackets after the mean. These distributions were used to accept or reject significant congruence of node ages.