ABSTRACT
BACKGROUND: The Asimina-Disepalum clade (Annonaceae subfam. Annonoideae tribe Annoneae) includes a major Neotropical-Asian biogeographical disjunction. We evaluate whether this disjunction can be explained by the Eocene boreotropics hypothesis, which relies on the existence of extensive boreotropical forests during the Late Palaeocene-Early Eocene thermal maximum (52-50 Ma), followed by disruption of boreotropical vegetation during post-Eocene cooling. Molecular dating using an uncorrelated relaxed molecular clock (UCLD) model with two fossil calibrations, ancestral range estimation, and ecological niche modelling across evolutionary time were performed. Our focus was the geographical origin of Disepalum and general biogeographic patterns within this genus. Comparison of ecological tolerance among extant species and niche reconstructions at ancestral nodes within the clade enabled insights in likely migration routes of lineages, as well as evaluating the role of bioclimatic ecological differentiation in the diversification of Disepalum within Southeast Asia. RESULTS: The inferred vicariance event associated with the Asimina-Disepalum disjunction is estimated to have originated ca. 40 Mya [95% highest posterior density (HPD): 44.3-35.5 Mya]. The Disepalum crown lineage is estimated to have originated ca. 9 Mya (95% HPD: 10.6-7.6), either in western Malesia and continental Southeast Asia, or exclusively in western Malesia. Ecological niche modelling shows that seasonality of temperature and precipitation are major contributors determining the geographical range of species. Ancestral niche modelling furthermore indicates that the ancestor of the Asimina-Disepalum clade likely had bioclimatic preferences close to conditions found in current tropical and subtropical climates across Asia, whereas the ancestors of the Asimina and Disepalum crown groups are projected onto the more subtropical and tropical regions, respectively. CONCLUSIONS: The vicariance event associated with the Neotropical-Asian disjunction within the Asimina-Disepalum clade likely coincided with climatic deterioration at the Eocene-Oligocene boundary. Although detrended component analyses (DCA) indicate that altitude and seasonality of temperature and precipitation have the greatest influence in determining the geographical range of species, isolation due to palaeogeographic and palaeoclimatic events appears to be of greater significance than climate niche differentiation in driving diversification in Disepalum.
Subject(s)
Asimina/classification , Ecosystem , Models, Biological , Phylogeography , Tropical Climate , Asia , Bayes Theorem , Phylogeny , Time FactorsABSTRACT
Taxonomic delimitation of Disepalum (Annonaceae) is contentious, with some researchers favoring a narrow circumscription following segregation of the genus Enicosanthellum. We reconstruct the phylogeny of Disepalum and related taxa based on four chloroplast and two nuclear DNA regions as a framework for clarifying taxonomic delimitation and assessing evolutionary transitions in key morphological characters. Maximum parsimony, maximum likelihood and Bayesian methods resulted in a consistent, well-resolved and strongly supported topology. Disepalum s.l. is monophyletic and strongly supported, with Disepalum s.str. and Enicosanthellum retrieved as sister groups. Although this topology is consistent with both taxonomic delimitations, the distribution of morphological synapomorphies provides greater support for the inclusion of Enicosanthellum within Disepalum s.l. We propose a novel infrageneric classification with two subgenera. Subgen. Disepalum (= Disepalum s.str.) is supported by numerous synapomorphies, including the reduction of the calyx to two sepals and connation of petals. Subgen. Enicosanthellum lacks obvious morphological synapomorphies, but possesses several diagnostic characters (symplesiomorphies), including a trimerous calyx and free petals in two whorls. We evaluate changes in petal morphology in relation to hypotheses of the genetic control of floral development and suggest that the compression of two petal whorls into one and the associated fusion of contiguous petals may be associated with the loss of the pollination chamber, which in turn may be associated with a shift in primary pollinator. We also suggest that the formation of pollen octads may be selectively advantageous when pollinator visits are infrequent, although this would only be applicable if multiple ovules could be fertilized by each octad; since the flowers are apocarpous, this would require an extragynoecial compitum to enable intercarpellary growth of pollen tubes. We furthermore infer that the monocarp fruit stalks are likely to have evolved independently from those in other Annonaceae genera and may facilitate effective dispersal by providing a color contrast within the fruit.
