Systematics and Biogeography of the Afro-Malagasy Fleshy-Fruited Begonia (Begoniaceae)

The ca. 158 African species of Begonia represent 16 sections and occur principally in the tropical rain forests of West and Central Africa, but are also found in the more seasonal forests of East and South Africa. Other species are island endemics found in: the Socotran Archipelago (2 spp.); Madagascar, the Mascarenes and Comores (50 spp.); and the Gulf of Guinea Islands (4 spp.). Afro-Malagasy begonias include 40 species in sections Baccabegonia, Squamibegonia, Tetraphila and Mezierea, that possess fleshy fruits, presumed to be an adaptation to bird or ant dispersal. A phylogeny of African Begonia based on chloroplast trnL intron nucleotide sequences resolved the wingless fleshy-fruited species of African Begonia as monophyletic with the exception of species in section Mezierea. This section is polyphyletic with B. meyeri-johannis and B. oxyloba forming an unresolved clade, and B. salaziensis and B. comorensis more closely related to winged, dry-fruited Malagasy species. All endemic Malagasy and Mascarene species sampled (representing sections Mezierea, Erminea, Quadrilobaria and Nerviplacentaria) form a monophyletic group. Another clade comprises the terrestrial, hydrophytic, predominantly West and Central African, wing-fruited species in sections Scutobegonia, Loasibegonia, Filicibegonia and Cristasemen plus Begonia iucunda. It includes the monotypic section Cristasemen and B. iucunda that are sister to the remaining, more species-rich sections. This result is mirrored by morphological and previous ITS data, and a new section, Chasmophila, is established to accommodate B. iucunda. The predominantly East and South African species in sections Augustia, Rostrobegonia, Sexalaria and Peltaugustia are more closely related to American and Asian species of Begonia than they are to other African species. A comparison of separate analyses based on the chloroplast trnL intron and the nuclear ribosomal internal transcribed spacer (ITS) and 26S regions show congruence in portions of the tree that depict the West and Central African and endemic Malagasy begonias, but are incongruent among the clades that include Asian, American and East and South African species. In the ITS phylogeny Asian and American species form two separate monophyletic clades which collapsed when ambiguously aligned regions in the ITS matrix were eliminated. In the trnL intron phylogeny American and Asian species are interdigitated. These results weaken prior claims that American and Asian species of Begonia are monophyletic. A combined trnL intron, ITS and 26S analysis shows that fleshy fruits are apomorphic within Begonia and evolved at least twice in Africa. An overview of morphological character and character state delimitations in Begonia found that different workers interpret morphology and delimit character states in different ways. Twenty-seven characters were identified for the fleshy-fruited begonias of sections Baccabegonia, Squamibegonia and Tetraphila. When combined with molecular data, morphology resolved nodes that molecular data alone did not. This combined analysis suggests non-monophyly of section Tetraphila, but a re-delimitation of this section is not advised. Section Squamibegonia {B. poculifera, B. ampla, and B. bonus-henricus) is monophyletic with B. baccata (section Baccabegonia) as sister. The best indicators of species relationships within Tetraphila are stigma and style morphology; forked styles with twisted stigmas are plesiomorphic within the section and simple styles with contracted stigmas at their apex are apomorphic. Leaf shape and habit characters also provide valuable synapomorphies. Dates of evolutionary events in African Begonia were estimated assuming an age of two million years for B. salaziensis, equivalent to the age of Reunion, and are congruent with biogeographical hypotheses based on other plant and animal phylogenies and with geological and climatological evidence. A large proportion of the current diversity of Begonia in Africa is of pre-Pleistocene origin, and many of the main lineages probably arose at the end of the Miocene, reflecting the general aridification that converted large parts of central Africa into savanna or rain forest-savanna mosaic. Areas previously identified as Pleistocene rain forest refugia have probably acted as refugia repeatedly since the Miocene. Sao Tome is identified as an important pre- Pleistocene refuge for the genus. Species of relatively recent Pleistocene origin are concentrated in the species-rich sections Tetraphila, Loasibegonia and Scutobegonia. Begonia diversification on Madagascar is postulated to have followed a single dispersal event at ca. 12 Ma, followed by the more recent dispersal of B. oxyloba from the mainland