Australian Systematic Botany Australian Systematic Botany Society
Taxonomy, biogeography and evolution of plants
RESEARCH ARTICLE

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

Gillian K. Brown A B , Daniel J. Murphy B C , James Kidman A and Pauline Y. Ladiges A
+ Author Affiliations
- Author Affiliations

A School of Botany, The University of Melbourne, Vic. 3010, Australia.

B National Herbarium of Victoria, Royal Botanic Gardens Melbourne, Vic. 3141, Australia.

C Corresponding author. Email: daniel.murphy@rbg.vic.gov.au

Australian Systematic Botany 25(6) 390-403 https://doi.org/10.1071/SB12027
Submitted: 15 August 2012  Accepted: 29 October 2012   Published: 14 December 2012

Abstract

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 (Réunion 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.


References

Adamski DJ, Dudley NS, Morden CW, Borthakur D (2012) Genetic differentiation and diversity of Acacia koa populations in the Hawaiian islands. Plant Species Biology 27, 181–190.
Genetic differentiation and diversity of Acacia koa populations in the Hawaiian islands.CrossRef | open url image1

Ares A, Fownes JH, Sun W (2000) Genetic differentiation of intrinsic water-use efficiency in the Hawaiian native Acacia koa. International Journal of Plant Sciences 161, 909–915.
Genetic differentiation of intrinsic water-use efficiency in the Hawaiian native Acacia koa.CrossRef | open url image1

Ariati SR, Murphy DJ, Udovicic F, Ladiges PY (2006) Molecular phylogeny of three groups of acacias (Acacia subgenus Phyllodineae) in arid Australia based on the internal and external transcribed spacer regions of nrDNA. Systematics and Biodiversity 4, 417–426.
Molecular phylogeny of three groups of acacias (Acacia subgenus Phyllodineae) in arid Australia based on the internal and external transcribed spacer regions of nrDNA.CrossRef | open url image1

Atchison E (1948) Studies in the Leguminosae 2. Cytogeography of Acacia (Tourn.) L. American Journal of Botany 35, 651–655.
Studies in the Leguminosae 2. Cytogeography of Acacia (Tourn.) L.CrossRef | open url image1

Athens JS, Dega MF, Ward JV (2004) Austronesian colonization of the Mariana islands: the paleoenvironmental evidence. Indo-Pacific Prehistory Association Bulletin 24, 21–30.

Baker PJ, Robinson AP, Ewel JJ (2008) Sudden and sustained response of Acacia koa crop trees to crown release in stagnant stands. Canadian Journal of Forest Research 38, 656–666.
Sudden and sustained response of Acacia koa crop trees to crown release in stagnant stands.CrossRef | 1:CAS:528:DC%2BD1cXmtVOnt70%3D&md5=35d8e8f7cff5127ec6227baa8af13355CAS | open url image1

Baldwin BG, Markos S (1998) Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae). Molecular Phylogenetics and Evolution 10, 449–463.
Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae).CrossRef | 1:CAS:528:DyaK1MXhtlKmtb4%3D&md5=a248a743ecae3551e18f56c946932433CAS | open url image1

Bell EA, Evans CS (1978) Biochemical evidence of a former link between Australia and the Mascarene Islands. Nature 273, 295–296.
Biochemical evidence of a former link between Australia and the Mascarene Islands.CrossRef | open url image1

Bowman DMJS, Braby MF, Brown GK, Brown J, Cook LG, Crisp MD, Ford F, Haberle SG, Hughes J, Isagi Y, Joseph L, Ladiges PY, McBride J, Nelson G (2010) Biogeography of the monsoon tropics: Australia’s last biological frontier. Journal of Biogeography 37, 201–216.
Biogeography of the monsoon tropics: Australia’s last biological frontier.CrossRef | open url image1

Brown GK, Murphy DJ, Ladiges PY (2011) Relationships of the Australo-Malesian genus Paraserianthes (Mimosoideae: Leguminosae) identifies the sister group of Acacia sensu stricto and two biogeograhical tracts. Cladistics 27, 380–390.
Relationships of the Australo-Malesian genus Paraserianthes (Mimosoideae: Leguminosae) identifies the sister group of Acacia sensu stricto and two biogeograhical tracts.CrossRef | open url image1

Carlquist S (1965) ‘Island Life: a Natural History of the Islands of the World.’ (American Museum of Natural History, Natural History Press: Garden City, NY)

Coulaud J, Brown SC, Siljak-Yakovlev S (1995) First cytogenetic investigation in populations of Acacia heterophylla, endemic from La-Réunion Island, with reference to A. melanoxylon. Annals of Botany 75, 95–100.
First cytogenetic investigation in populations of Acacia heterophylla, endemic from La-Réunion Island, with reference to A. melanoxylon.CrossRef | 1:STN:280:DC%2BC3M7jt1ygtA%3D%3D&md5=44c84f757459e5f9bd5f21b8460bfd59CAS | open url image1

Cowan R, Maslin BR (2001) ‘Flora of Australia. Vol. 11B.’ (ABRS/CSIRO Publishing: Melbourne)

Daehler CC, Yorkston M, Sun W, Dudley N (1999) Genetic variation in morphology and growth characters of Acacia koa in the Hawaiian Islands. International Journal of Plant Sciences 160, 767–773.
Genetic variation in morphology and growth characters of Acacia koa in the Hawaiian Islands.CrossRef | open url image1

De Boer AJ (1995) Islands and cicadas adrift in the West Pacific. Biogeographic patterns related to plate tectonics. Tijdschrift voor Entomologie 138, 169–244.

Diamond JM (2000) Taiwan’s gift to the world. Nature 403, 709–710.
Taiwan’s gift to the world.CrossRef | 1:CAS:528:DC%2BD3cXhsVSqsbs%3D&md5=d112005b5ab3d0bcb518afd14fb4acfdCAS | open url image1

Du Puy D, Labat JN, Rabevohitra R, Villiers J-F (2002) ‘The Leguminosae of Madagascar.’ (Royal Botanic Gardens, Kew: London)

Duffels JP, Ewart A (1988) The cicadas of the Fiji, Samoa and Tonga Islands, their taxonomy and biogeography (Homoptera, cicadoidea). Entomonograph 10, 1–108.

Gray RD, Jordan FM (2000) Language trees support the express-train sequence of Austronesian expansion. Nature 405, 1052–1055.
Language trees support the express-train sequence of Austronesian expansion.CrossRef | 1:CAS:528:DC%2BD3cXkvFKks7c%3D&md5=f11e13e88ef063b80cdfbd8f48add83cCAS | open url image1

Hall R (1998) The plate tectonics of Cenozoic Southeast Asia and the distribution of land and sea. In ‘Biogeography and geological evolution of South-east Asia’. (Eds R Hall, JD Holloway) pp. 99–131. (Backhuys Publishers: Leiden, the Netherlands)

Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.

Hall R (2001) Cenozoic reconstructions of SE Asia and the SW Pacific: changing patterns of land and sea. In ‘Faunal and Floral Migrations and Evolution in SE Asia–Australasia’. (Eds I Metcalfe, JMB Smith, M Morwood, I Davidson) pp. 35–56. (AA Balkema Publishers: Lisse)

Hall R (2009) Southeast Asias’s changing palaeogeograhy. Blumea 54, 148–161.
Southeast Asias’s changing palaeogeograhy.CrossRef | open url image1

Harrington RA, Fownes JH, Meinzer FC, Scowcroft PG (1995) Forest growth along a rainfall gradient in Hawaii: Acacia koa stand structure, productivity, foliar nutrients, and water- and nutrient-use efficiencies. Oecologia 102, 277–284.
Forest growth along a rainfall gradient in Hawaii: Acacia koa stand structure, productivity, foliar nutrients, and water- and nutrient-use efficiencies.CrossRef | open url image1

Hołyńska M, Stoch F (2012) Mesocyclops (Crustacea, Copepoda, Cyclopidae) in the South Pacific islands. Zoologischer Anzeiger 251, 237–252.
Mesocyclops (Crustacea, Copepoda, Cyclopidae) in the South Pacific islands.CrossRef | open url image1

Hope G, Kershaw AP, van der Kaars S, Xiangjun S, Liew P-M, Heusser LE, Takahara H, McGlone M, Miyoshi N, Moss PT (2004) History of vegetation and habitat change in the Austral–Asian region. Quaternary International 118–119, 103–126.
History of vegetation and habitat change in the Austral–Asian region.CrossRef | open url image1

Käss E, Wink M (1997) Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1+2 regions of rDNA. Plant Systematics and Evolution 208, 139–167.
Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1+2 regions of rDNA.CrossRef | open url image1

Kean J (1991) Aboriginal–Acacia relationships in central Australia. Records of the South Australian Museum 24, 111–124.

Ladiges PY, Cantrill D (2007) New Caledonia-Australian connections: comment on biogeographic patterns and geology. Australian Systematic Botany 20, 383–389.
New Caledonia-Australian connections: comment on biogeographic patterns and geology.CrossRef | open url image1

Ladiges PY, Udovicic F, Nelson G (2003) Australian biogeographical connections and the phylogeny of large genera in the plant family Myrtaceae. Journal of Biogeography 30, 989–998.
Australian biogeographical connections and the phylogeny of large genera in the plant family Myrtaceae.CrossRef | open url image1

Larson G (2007) Phylogeny and ancient DNA of Sus provides insights into Neolithic expansion in inland Southeast Asia and Oceania. Proceedings of the National Academy of Sciences of the United States of America 104, 4834–4839.
Phylogeny and ancient DNA of Sus provides insights into Neolithic expansion in inland Southeast Asia and Oceania.CrossRef | 1:CAS:528:DC%2BD2sXjvFCjtrw%3D&md5=27783b826c7792b89d0018fe83df39cdCAS | open url image1

Lewis GP, Schrire B, Mackinder B, Lock M (2005) ‘Legumes of the World.’ (Royal Botanic Gardens, Kew: London)

Macphail MK, Hill RS (2001) Fossil record of Acacia in Australia: Eocene to Recent. In ‘Flora of Australia. Vol. 11A’. (Eds AE Orchard, AJG Wilson) pp. 13–29. (ABRS/CSIRO Publishing: Melbourne)

Maslin BR (2001a) Introduction to Acacia. In ‘Flora of Australia. Vol. 11A’. (Eds AE Orchard, AJG Wilson) pp. 3–13. (ABRS/CSIRO Publishing: Melbourne)

Maslin BR (2001b) ‘Flora of Australia. Vol. 11B.’ (ABRS/CSIRO Publishing: Melbourne)

Maslin BR (2004) Classification and phylogeny of Acacia. In ‘Evolution of Ecological and Behavioural Diversity: Australian Acacia Thrips as Model Organisms’. (Eds BJ Crespi, DC Morris, LA Mound) pp. 97–112. (ABRS/CSIRO Publishing: Melbourne)

Maslin BR (2008) Generic and subgeneric names in Acacia following retypification of the genus. Muelleria 26, 7–9.

McDonald MW, Maslin BR (2000) Taxonomic revision of the salwoods: Acacia aulacocarpa Cunn. ex Benth. and its allies (Leguminosae: Mimosoideae: section Juliflorae). Australian Systematic Botany 13, 21–78.
Taxonomic revision of the salwoods: Acacia aulacocarpa Cunn. ex Benth. and its allies (Leguminosae: Mimosoideae: section Juliflorae).CrossRef | open url image1

McDonald MW, Maslin BR, Butcher PA (2001) Utilisation of acacias. In ‘Flora of Australia. Vol. 11A’. (Eds AE Orchard, AJG Wilson) pp. 30–40. (ABRS/CSIRO Publishing: Melbourne)

Miller JT, Andrew R, Bayer R (2003) Molecular phylogenetics of the Australian acacias of subg. Phyllodineae (Fabaceae: Mimosoideae) based on the trnK intron. Australian Journal of Botany 51, 167–177.
Molecular phylogenetics of the Australian acacias of subg. Phyllodineae (Fabaceae: Mimosoideae) based on the trnK intron.CrossRef | 1:CAS:528:DC%2BD3sXksFSlurs%3D&md5=64cab82cf0956b1bc4145b1402ba69d0CAS | open url image1

Miller JT, Murphy DJ, Brown GK, Richardson DM, González-Orozco CE (2011) The evolution and phylogenetic placement of invasive Australian Acacia species. Diversity & Distributions 17, 848–860.
The evolution and phylogenetic placement of invasive Australian Acacia species.CrossRef | open url image1

Moran GF, Muona O, Bell JC (1989a) Acacia mangium: a tropical forest tree of low genetic diversity. Evolution 43, 231–235.
Acacia mangium: a tropical forest tree of low genetic diversity.CrossRef | open url image1

Moran GF, Muona O, Bell JC (1989b) Breeding systems and genetic diversity in Acacia auriculiformis and A. crassicarpa. Biotropica 21, 250–256.
Breeding systems and genetic diversity in Acacia auriculiformis and A. crassicarpa.CrossRef | open url image1

Murphy DJ, Miller JT, Bayer RJ, Ladiges PY (2003) Molecular phylogeny of Acacia subgenus Phyllodineae (Mimosoideae: Leguminosae) based on DNA sequences of the internal transcribed spacer region. Australian Systematic Botany 16, 19–26.
Molecular phylogeny of Acacia subgenus Phyllodineae (Mimosoideae: Leguminosae) based on DNA sequences of the internal transcribed spacer region.CrossRef | 1:CAS:528:DC%2BD3sXms1yru78%3D&md5=468123469faf94ab8eb5b4dce3dc1427CAS | open url image1

Murphy DJ, Brown GK, Miller JT, Ladiges PY (2010) Molecular phylogeny of Acacia s.s. (Mimosoideae: Leguminosae) – evidence for major clades and informal classification. Taxon 59, 7–19.

New TR (1984) ‘A Biology of Acacias. (Oxford University Press: Melbourne)

Pearson HL, Vitousek PM (2001) Stand dynamics, nitrogen accumulation, and symbiotic nitrogen fixation in regenerating stands of Acacia koa. Ecological Applications 11, 1381–1394.
Stand dynamics, nitrogen accumulation, and symbiotic nitrogen fixation in regenerating stands of Acacia koa.CrossRef | open url image1

Pedley L (1975) Revision of the extra-Australian species of Acacia subg. Heterophyllum. Contributions from the Queensland Herbarium 18, 1–24.

Pedley L (1978) A revision of Acacia Mill. in Queensland. Austrobaileya 1, 75–234.

Pedley L (1990) New combinations in Acacia Miller (Leguminosae: Mimosoideae). Austrobaileya 3, 215–216.

Regueiro M, Mirabal S, Lacau H, Caerio JL, Garcia-Bertrand RL, Herrera RJ (2008) Austronesian genetic signature in East African Madagascar and Polynesia. Journal of Human Genetics 53, 106–120.
Austronesian genetic signature in East African Madagascar and Polynesia.CrossRef | 1:STN:280:DC%2BD1c%2FnsFCruw%3D%3D&md5=4fd62198e45ba7daf2741d5afc45bcb8CAS | open url image1

Rock JF (1913) ‘The Indigenous Trees of the Hawaiian Islands.’ pp. 22–35. (E. Herrick Brown: Honolulu, HI)

Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MRBAYES 3: Bayesian phylogenetic inference under mixed models.CrossRef | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=c3efa0cf361d593855ae82b9093dc1d2CAS | open url image1

Soares P, Trejaut JA, Loo J-H, Hill C, Mormina M, Lee C-L, Chen Y-M, Hudjashov G, Forster P, Macauley V, Bulbeck D, Oppenheimer S, Lin M, Richards MB (2008) Climate change and postglacial human dispersals in Southeast Asia. Molecular Biology and Evolution 25, 1209–1218.
Climate change and postglacial human dispersals in Southeast Asia.CrossRef | 1:CAS:528:DC%2BD1cXntlWltLY%3D&md5=ac28dc0ad525f9f0a0c7290b9bfd0bbdCAS | open url image1

Sun Y (1994) Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theoretical and Applied Genetics 89, 26–32.
Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA.CrossRef | 1:CAS:528:DyaK2MXivFWkt7k%3D&md5=5c6de875b92adac672cbe1c47ee02554CAS | open url image1

Swofford DL (2002) ‘PAUP*: Phylogenetic Analysis using Parsimony (*and Other Methods) (version 4.0b.10).’ (Sinauer: Sunderland, MA)

Trejaut JA, Kivisild TJ, Loo H, Lee CL, He CL, Hsu CJ, Lee ZY, Lin M (2005) Traces of archaic mitochondrial lineages persist in austronesian-speaking Formosan populations. PLoS Biology 3, 1362–1372.

Turnbull JW (1984) Six phyllodinous Acacia species for planting in the humid tropical Lowlands. Pesquisa Agropecuaria Brasileira 19, 69–73.

Turnbull JW, Crompton HR, Pinyopusarerk K (Eds) (1998) Recent developments in acacia planting. ACIAR Proceedings number 82, 27–30 October 1997, Hanoi, Vietnam. (Australian Centre for International Agriculture Research: Canberra)

van Welzen PC, Turner H, Hovenkamp P (2003) Historical biogeography of Southeast Asia and the West Pacific, or the generality of unrooted networks as historical biogeographic hypotheses. Journal of Biogeography 30, 181–192.
Historical biogeography of Southeast Asia and the West Pacific, or the generality of unrooted networks as historical biogeographic hypotheses.CrossRef | open url image1

Vassal J (1969) A propos des Acacia heterophylla et koa. Bulletin de la Société D’Histoire Naturelle de Toulouse 105, 443–447.

Wagner WL, Herbst DR, Sohmer SH (1990) ‘Manual of the Flowering Plants of Hawaii.’ (University of Hawaii Press and Bishop Museum Press: Honolulu, HI)

Whitesell CD (1964) Silvical characteristics of koa (Acacia koa Gray). USDA Forest Service, Pacific Southwest Forest and Range Experiment Station, Research Paper PSW-16, pp. 1–11. (Berkley, CA)

Yu H (2007) Physiological comparisons of true leaves and phyllodes in Acacia mangium seedlings. Photosynthetica 45, 312–316.
Physiological comparisons of true leaves and phyllodes in Acacia mangium seedlings.CrossRef | open url image1



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