Has Goniothalamus undergone rapid radiation? Investigating temporal patterns in diversification rates shifts in the early-divergent angiosperm family Annonaceae using comparative phylogenetic methods

Abstract

Previous studies have indicated that Goniothalamus (Annonaceae) has undergone rapid radiation. Three lines of evidence support this hypothesis: (1) Goniothalamus (c. 130 species) is one of the eight largest genera in the family and hence often regarded as evolutionarily ‘successful’; (2) it has been estimated to have diverged relatively recently, with a crown age of 10–4 Ma; and (3) a significant rate shift has been identified along the Goniothalamus stem lineage, a feature not observed in any of the other five largest genera in the family. Goniothalamus is therefore a key genus for studying evolutionary radiation, especially since it belongs to a family previously shown to have a relatively low overall net diversification rate. The current study aims to re-examine the putative radiation of Goniothalamus and to investigate temporal patterns in diversification rates across the Annonaceae. A calibrated molecular phylogeny of the Annonaceae was reconstructed, based on 738 accessions, with novel sequence data for 65 Goniothalamus species (representing c. 50% of species in the genus). Different phylogenetic comparative methods which account for incomplete or non-random sampling, such as modeling evolutionary diversification using stepwise AIC (MEDUSA), and likelihood methods fitting birth-death models to the phylogenetic data, were used to estimate diversification rates and rate shifts, enabling reevaluation of the putative radiation of Goniothalamus. The molecular divergence time estimates reveal a crown age of c. 25 Ma, which is substantially older than in previous studies. The results of the diversification analyses show that Goniothalamus is unlikely to be a rapidly radiating genus as it does not show a significant shift in diversification rate when compared to the background rate, nor does it show a significantly high diversification rate when compared with other genus-level clades. Interestingly, variation of diversification rate through time was detected at the family level. The Annonaceae is shown to possess a low net diversification rate and high relative extinction rate until the late Miocene; this rate peak may have been caused by tectonic and climatic events.