Systematics and phylogenetics of goniothalamus (annonaceae) : a study of putative rapid, recent evolutionary radiation in a species-rich palaeotropical genus

Abstract

Goniothalamus is one of the largest genera in the pantropical angiosperm family Annonaceae. It includes c. 130 species of trees, distributed in tropical lowland and submontane forests in tropical Asia, Australia and Melanesia. Previous studies have indicated that Goniothalamus shows a significantly higher diversification rate in comparison to closely related taxa and that its species diversity is the result of a relatively recent radiation. The phylogenetic framework necessary for testing this hypothesis, including the investigation of potential intrinsic and environmental correlates of this putative radiation, and additional biogeographical and evolutionary studies, has not previously been available.

Data from nine chloroplast DNA markers (11,214 aligned characters) and 67 ingroup accessions (c. 50% of the species diversity) of Goniothalamus are used for parsimony, maximum likelihood and Bayesian phylogenetic reconstructions. The results confirm the monophyly of Goniothalamus, indicate several strongly supported major subclades, and show that most previously described infrageneric taxa are para- or polyphyletic.

Morphological character evolution in Goniothalamus is investigated using ancestral character state reconstructions and phylogenetic analysis of variance. The evolutionary patterns of 19 morphological characters for which a significant phylogenetic signal was identified are discussed in relation to function. Character correlations indicate two main fruit types: small monocarps (average diameter c. 1 cm) with glabrous seeds borne on young growth, which are hypothesized to be predominantly bird-dispersed, and larger (average diameter 1.5 cm) monocarps with hairy seeds borne on older twigs, the trunk or close to the ground, hypothesized to be predominantly mammal dispersed. Synapomorphies of several subclades of the Goniothalamus phylogeny are identified based on the ancestral character reconstructions of 11 categorical characters.

Molecular dating is performed using two fossil calibrations, an uncorrelated rates relaxed molecular clock model, and the most comprehensive Annonaceae dataset to date (738 ingroup and 5 outgroup accessions, nine chloroplast markers), with the aim of investigating the historical biogeography of Goniothalamus. Mean divergence time estimates indicate a Goniothalamus crown group age of 23 Ma. Biogeographical analyses infer an ancestral area in western Southeast Asia, two dispersal events from western Southeast Asia to India, and multiple dispersal events from western Southeast Asia eastwards to the Philippines, New Guinea and Australia in the early to late Miocene. Diversification analyses corroborate previous studies which indicated that early Annonaceae diversification was characterized by a low net diversification rate and high relative extinction rate. The results of the present study, however, also indicate that the diversification rate peaked between 9.9 and 0.8 Ma, associated with a low relative extinction rate. Temporally coinciding environmental (tectonic and climatic) factors which may underlie this diversification peak are discussed. In contrast to previous studies, the results do not suggest that the species diversity in Goniothalamus is the result of a rapid, recent radiation. Significant rate shifts are not indicated when using methods that accommodate incomplete taxon sampling. Previously inferred rate shifts are probably artefacts because of inadequate taxon sampling. Significantly high diversification rates are identified in the present study in several small to medium-sized Asian genera such as Polyalthia s.str. and Monoon.