Molecular phylogenetics of Artabotrys (Annonaceae) : evaluating hypotheses of correlated evolution, historical biogeograhy and pollination system evolution

Abstract

Although Artabotrys is one of the most species-rich genera in the early divergent angiosperm family Annonaceae, with ca. 105 species of lianas distributed throughout the Palaeotropics, the genus has received relatively little research attention. The limited phylogenetic resolution and taxon sampling attained in previous studies have significantly constrained biogeographical and evolutionary inferences. The phylogeny of Artabotrys was reconstructed in the present study based on 53 Artabotrys species (ca. 51% of species diversity), and four chloroplast (matK, ndhF, psbA-trnH and trnL-F) and 10 nuclear (AP3, At2g32520, GI, HMGS, LFY, MAG1, ncpGS, NIA, PHYA and RPB2) DNA regions, using maximum likelihood, maximum parsimony and Bayesian analyses. The results indicate that Artabotrys is unequivocally monophyletic, with a species-rich main Artabotrys clade (MAC) comprising distinct African and Asian sister clades, and an early divergent grade (EDG) comprising two African species. Molecular divergence time estimation using a relaxed clock model and ancestral area and habitat reconstructions were performed to elucidate spatio-temporal diversification patterns. An ancestral range in Africa was inferred, with a single dispersal event to Asia. The most plausible explanation for the palaeotropical intercontinental disjunction involves overland migration across Arabia in the Miocene, prior to subsequent climate deterioration. The Late Miocene colonisation of Madagascar postdates the period conducive to rafting of vegetation mats from Africa to Madagascar. Dispersal across Wallace’s line occurred twice from the Late Miocene, when marine gaps diminished following convergence of the Sunda and Sahul shelves. Climatic niche conservatism is an underlying pattern in Artabotrys, with local niche shifts occurring rather recently. Considerable variation in habitat and fruit and seed morphology in Artabotrys renders the genus ideal for evaluating correlated evolution between seed functional traits (seed size and physical defence) and various ecological correlates (climatic variables and dispersal-related traits). The relationships between functional traits and ecological correlates were examined using phylogenetic regression based on 43 Artabotrys species. The hypothesis that testa thickness and seed volume evolved towards distinct optima in lineages with different dispersal-related traits and precipitation regime was furthermore tested using model-fitting approaches. The two distinct trait optima inferred may correspond with two seed dispersal modes in Artabotrys: lineages with smooth testa and thin pericarp have evolved a thinner testa and smaller seeds, potentially reflecting dispersal by birds and primates with seed-spitting and seed-swallowing habits, whereas lineages with other combinations of testa texture and pericarp thickness have evolved a thicker testa and larger seeds, potentially reflecting dispersal by primates with more destructive mastication behaviour. Comparative field studies on floral phenology and pollination ecology were undertaken in two exemplar species, viz. A. blumei from the MAC and A. brachypetalus from the EDG. The aberrant floral morphology of A. brachypetalus—in which all petals lack any distinction between blade and claw, and inner petals lack a projecting rim at the junction of the inner petal claw and blade—is associated with a generalist pollination system and the absence of a pollinator trapping mechanism. The firmly enclosed floral chamber is likely to be apomorphic for the MAC and associated with circadian pollinator trapping.