'Andean-centred' genera in the short-branch clade of Annonaceae: testing biogeographical hypotheses using phylogeny reconstruction and molecular dating

Aim We test biogeographical hypotheses regarding the origin of Andean-centred plant groups by reconstructing phylogeny in the short-branch clade (SBC) of Annonaceae, and estimating the timing of diversifications in four apparently Andean-centred genera: Cremastosperma R.E.Fr., Klarobelia Chatrou, Malmea R.E.Fr. and Mosannona Chatrou. The SBC includes species distributed in both the Old and New World tropics. A number of the Neotropical genera display 'Andean-centred' distribution patterns, with high species richness on both sides of the Andes mountain range. In particular, we test whether these groups could have originated on the South American continent during the time frame of the Andean orogeny [from c. 23 Ma (Miocene) to the present]. Methods Chloroplast DNA sequences were used to reconstruct phylogeny in related Annonaceae taxa plus outgroups, under maximum parsimony and Bayesian inference. The markers rbcL, trnL-trnF and psbA-trnH were sampled for 96 accessions to test the monophyly of each of the genera, and thus whether they might be para- or polyphyletic with respect to related groups distributed across Amazonia. To determine the sister groups of the four genera, the additional markers matK, ndhF, trnT-trnL, trnS-trnG and atpB-rbcL were sampled for 23 of the 96 accessions. Molecular dating techniques (nonparametric rate-smoothing; penalized likelihood; Bayesian inference) were then applied to estimate the age of the crown group of each genus and the age of their sister groups. Results Monophyly was confirmed in Cremastosperma, Malmea and Mosannona. The monotypic genus Pseudephedranthus Aristeg. was found to be nested within Klarobelia, the species of which otherwise formed a monophyletic group, and a South American-centred (SAC) clade was identified. The SAC clade comprises all the SBC genera distributed in South America and generally to a limited extent into Central America, but not those endemic to Africa, Asia and Central America. Age estimations for clades within the SBC were no older than around 60 Myr; those for the crown groups of Cremastosperma, Klarobelia, Malmea and Mosannona fell largely within the last 10-20 Myr. Main conclusions The distribution patterns of Cremastosperma, Klarobelia, Malmea and Mosannona are not the arbitrary result of the definition of para- or polyphyletic groups. We infer the presence of a common ancestor of the four genera in South America, but not by vicariance of an ancestral population on Gondwana. The age estimations, instead, may suggest that the SAC clade originated in South America by dispersal across the Boreotropics. Although the strength of this test was limited by imprecision in the molecular dating results, the ages of crown groups of the four genera suggest that diversifications occurred within the time frame of the orogeny of the Northern Andes.