Phylogenetic connections of phyllodinous species of Acacia outside Australia are explained by geological history and human-mediated dispersal

Acacia sensu stricto is found predominantly in Australia; however, there are 18 phyllodinous taxa that occur naturally outside Australia, north from New Guinea to Indonesia, Taiwan, the Philippines, south-western Pacific (New Caledonia to Samoa), northern Pacific (Hawaii) and Indian Ocean (Mascarene Islands). Our aim was to determine the phylogenetic position of these species within Acacia, to infer their biogeographic history. To an existing molecular dataset of 109 taxa of Acacia, we added 51 new accessions sequenced for the ITS and ETS regions of nuclear rDNA, including samples from 15 extra-Australian taxa. Data were analysed using both maximum parsimony and Bayesian methods. The phylogenetic positions of the extra-Australian taxa sampled revealed four geographic connections. Connection A, i.e. northern Australia-South-east Asia-south-western Pacific, is shown by an early diverging clade in section Plurinerves, which relates A. confusa from Taiwan and the Philippines (possibly Fiji) to A. simplex from Fiji and Samoa. That clade is related to A. simsii from southern New Guinea and northern Australia and other northern Australian species. Two related clades in section Juliflorae show a repeated connection (B), i.e. northern Australia-southern New Guinea-south-western Pacific. One of these is the 'A. auriculiformis clade', which includes A. spirorbis subsp. spirorbis from New Caledonia and the Loyalty Islands as sister to the Queensland species A. auriculiformis; related taxa include A. mangium, A. leptocarpa and A. spirorbis subsp. solandri. The 'A. aulacocarpa clade' includes A. aulacocarpa, A. peregrinalis endemic to New Guinea, A. crassicarpa from New Guinea and Australia, and other Australian species. Acacia spirorbis (syn. A. solandri subsp. kajewskii) from Vanuatu (Melanesia) is related to these two clades but its exact position is equivocal. The third biogeographic connection (C) is Australia-Timor-Flores, represented independently by the widespread taxon A. oraria (section Plurinerves) found on Flores and Timor and in north-eastern Queensland, and the Wetar island endemic A. wetarensis (Juliflorae). The fourth biogeographic connection (D), i.e. Hawaii-Mascarene-eastern Australia, reveals an extreme disjunct distribution, consisting of the Hawaiian koa (A. koa, A. koaia and A. kaoaiensis), sister to the Mascarene (Reunion Island) species A. heterophylla; this clade is sister to the eastern Australian A. melanoxylon and A. implexa (all section Plurinerves), and sequence divergence between taxa is very low. Historical range expansion of acacias is inferred to have occurred several times from an Australian-southern New Guinean source. Dispersal would have been possible as the Australian land mass approached South-east Asia, and during times when sea levels were low, from the Late Miocene or Early Pliocene. The close genetic relationship of species separated by vast distances, from the Indian Ocean to the Pacific, is best explained by dispersal by Austronesians, early Homo sapiens migrants from Asia.