Phylogenetic placement and the timing of diversification in Australia’s endemic Vachellia (Caesalpinioideae, Mimosoid Clade, Fabaceae) species
D. F. Comben
A D , G. A. McCulloch A B , G. K. Brown C and G. H. Walter A
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, The University of Queensland, Brisbane, Qld 4072, Australia.
B Department of Zoology, University of Otago, PO Box 56, Dunedin, 9054, New Zealand.
C Queensland Herbarium, Mt Coot Tha Road, Brisbane, Qld 4066, Australia.
D Corresponding author. Email: d.comben@uq.edu.au
Australian Systematic Botany 33(1) 103-109 https://doi.org/10.1071/SB19013
Submitted: 2 February 2019 Accepted: 12 June 2019 Published: 2 January 2020
Abstract
The genus Vachellia Wight & Arn. has a pantropical distribution, with species being distributed through Africa, the Americas, Asia and Australia. The relationships among the lineages from Africa and America are well understood, but the phylogenetic placement and evolutionary origins of the Australian species of Vachellia are not known. We, therefore, sequenced four plastid genes from representatives of each of the nine Australian species of Vachellia, and used Bayesian inference to assess the phylogenetic placement of these lineages, and a relaxed molecular clock to assess the timing of diversification. The Australian species of Vachellia form a well-supported monophyletic clade, with molecular-dating analysis suggesting a single dispersal into Australia 6.5 million years ago (95% range 13.9–2.7 million years ago). Diversification of the Australian clade commenced more recently, c. 3.1 million years ago (95% range 9.2–1.2 million years ago), perhaps driven by the increased aridification of Australia at this time. The closest relatives to the Australian Vachellia were not from the Malesian bioregion, suggesting either a long-distance dispersal from Africa, or two separate migrations through Asia. These results not only improve our understanding of the biogeography of Vachellia species, but also have significant implications for the biological control of invasive Vachellia species in Australia.
References
Bartish IV, Antonelli A, Richardson JE, Swenson U (2011) Vicariance or long-distance dispersal: historical biogeography of the pantropical subfamily Chrysophylloideae (Sapotaceae). Journal of Biogeography 38, 177–190.| Vicariance or long-distance dispersal: historical biogeography of the pantropical subfamily Chrysophylloideae (Sapotaceae).Crossref | GoogleScholarGoogle Scholar |
Baum DA, Small RL, Wendel JF (1998) Biogeography and floral evolution of Baobabs Adansonia, Bombacaceae as inferred from multiple data sets. Systematic Biology 47, 181–207.
| Biogeography and floral evolution of Baobabs Adansonia, Bombacaceae as inferred from multiple data sets.Crossref | GoogleScholarGoogle Scholar | 12064226PubMed |
Bell KL, Rangan H, Fernandes MM, Kull CA, Murphy DJ (2017) Chance long-distance or human-mediated dispersal? How Acacia s.l. farnesiana attained its pan-tropical distribution. Royal Society Open Science 4, 170105
| Chance long-distance or human-mediated dispersal? How Acacia s.l. farnesiana attained its pan-tropical distribution.Crossref | GoogleScholarGoogle Scholar | 28484637PubMed |
Boatwright JS, Maurin O, van der Bank M (2015) Phylogenetic position of Madagascan species of Acacia s.l. and new combinations in Senegalia and Vachellia (Fabaceae, Mimosoideae, Acacieae). Botanical Journal of the Linnean Society 179, 288–294.
| Phylogenetic position of Madagascan species of Acacia s.l. and new combinations in Senegalia and Vachellia (Fabaceae, Mimosoideae, Acacieae).Crossref | GoogleScholarGoogle Scholar |
Bouchenak-Khelladi Y, Maurin O, Hurter J, van der Bank M (2010) The evolutionary history and biogeography of Mimosoideae (Leguminosae): an emphasis on African Acacias. Molecular Phylogenetics and Evolution 57, 495–508.
| The evolutionary history and biogeography of Mimosoideae (Leguminosae): an emphasis on African Acacias.Crossref | GoogleScholarGoogle Scholar | 20696261PubMed |
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis (Bayesian evolutionary analysis with BEAST 2). PLoS Computational Biology 10, e1003537
| BEAST 2: a software platform for Bayesian evolutionary analysis (Bayesian evolutionary analysis with BEAST 2).Crossref | GoogleScholarGoogle Scholar | 24722319PubMed |
Bowman DM, Brown GK, Braby MF, Brown JR, Cook LG, Crisp MD, Ford F, Haberle S, Hughes J, Isagi Y, Joseph L, McBride J, Nelson G, Ladiges PY (2010) Biogeography of the Australian monsoon tropics. Journal of Biogeography 37, 201–216.
| Biogeography of the Australian monsoon tropics.Crossref | GoogleScholarGoogle Scholar |
Brown GK, Murphy DJ, Kidman J, Ladiges PY (2012) Phylogenetic connections of phyllodinous species of Acacia outside Australia are explained by geological history and human-mediated dispersal. Australian Systematic Botany 25, 390–403.
| Phylogenetic connections of phyllodinous species of Acacia outside Australia are explained by geological history and human-mediated dispersal.Crossref | GoogleScholarGoogle Scholar |
Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MA, Cooper S, Donnellan SC, Keogh JS, Leys R, Melville J, Murphy DJ, Porch N, Wyrwoll KH (2008) Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17, 4398–4417.
| Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota.Crossref | GoogleScholarGoogle Scholar | 18761619PubMed |
Cook LG, Crisp MD (2005) Not so ancient: the extant crown group of Nothofagus represents a post-Gondwanan radiation. Proceedings of the Royal Society of London – B. Biological Sciences 272, 2535
| Not so ancient: the extant crown group of Nothofagus represents a post-Gondwanan radiation.Crossref | GoogleScholarGoogle Scholar |
Crisp MD, Cook LG (2013) How was the Australian flora assembled over the last 65 million years? A molecular phylogenetic perspective. Annual Review of Ecology Evolution and Systematics 44, 303–324.
| How was the Australian flora assembled over the last 65 million years? A molecular phylogenetic perspective.Crossref | GoogleScholarGoogle Scholar |
Crisp MD, Isagi Y, Kato Y, Cook LG, Bowman DM (2010) Livistona palms in Australia: ancient relics or opportunistic immigrants? Molecular Phylogenetics and Evolution 54, 512–523.
| Livistona palms in Australia: ancient relics or opportunistic immigrants?Crossref | GoogleScholarGoogle Scholar | 19766198PubMed |
Darriba D, Taboada G, Doallo R, Posada D (2012) jModelTest2: more models, new heuristics and parallel computing. Nature Methods 9, 772
| jModelTest2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 22847109PubMed |
Darwin C (1859) ‘On the Origin of Species by Means of Natural Selection, or, the Preservation of Favoured Races in the Struggle for Life.’ (John Murray: London, UK)
de Candolle AP (1820) ‘Essai élémentaire de géographie botanique.’ (FS Laeraule: Strasbourg, France)
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11–15.
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence (relaxed phylogenetics). PLoS Biology 4, e88
| Relaxed phylogenetics and dating with confidence (relaxed phylogenetics).Crossref | GoogleScholarGoogle Scholar | 16683862PubMed |
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 15034147PubMed |
Felsenstein J (1985) Phylogenies and the comparative method. American Naturalist 125, 1–15.
| Phylogenies and the comparative method.Crossref | GoogleScholarGoogle Scholar |
Fujioka T, Chappell J, Honda M, Yatsevich I, Fifield K, Fabel D (2005) Global cooling initiated stony deserts in central Australia 2–4 Ma, dated by cosmogenic 21Ne-10Be. Geology 33, 993–996.
| Global cooling initiated stony deserts in central Australia 2–4 Ma, dated by cosmogenic 21Ne-10Be.Crossref | GoogleScholarGoogle Scholar |
Gill ED (1975) Evolution of Australia’s unique flora and fauna in relation to the plate tectonics theory. Proceedings of the Royal Society of Victoria 87, 215–234.
Gillespie RG, Baldwin BG, Waters JM, Fraser CI, Nikula R, Roderick GK (2012) Long-distance dispersal: a framework for hypothesis testing. Trends in Ecology & Evolution 27, 47–56.
| Long-distance dispersal: a framework for hypothesis testing.Crossref | GoogleScholarGoogle Scholar |
Gómez-Acevedo S, Rico-Arce L, Delgado-Salinas A, Magallón S, Eguiarte LE (2010) Neotropical mutualism between Acacia and Pseudomyrmex: phylogeny and divergence times. Molecular Phylogenetics and Evolution 56, 393–408.
| Neotropical mutualism between Acacia and Pseudomyrmex: phylogeny and divergence times.Crossref | GoogleScholarGoogle Scholar | 20307674PubMed |
Hansford M (2015) Karoo thorn, Vachellia (Acacia) karroo: a state prohibited weed close to eradication. Plant Protection Quarterly 30, 51–58.
Hodgkinson K, Oxley R (1990) Influence of fire and edaphic factors on germination of the arid zone shrubs Acacia aneura, Cassia nemophila and Dodonaea Viscosa. Australian Journal of Botany 38, 269–279.
| Influence of fire and edaphic factors on germination of the arid zone shrubs Acacia aneura, Cassia nemophila and Dodonaea Viscosa.Crossref | GoogleScholarGoogle Scholar |
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| MRBAYES: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 11524383PubMed |
Julien MH, Sforza R, Bon M, Evans H, Hatcher P (2008) ‘Proceedings of the XII international symposium on biological control of weeds.’ (CABI: La Grande Motte, France)
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |
Kress WJ, Erickson DL, Jones FA, Swenson NG, Perez R, Sanjur O, Bermingham E (2009) Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proceedings of the National Academy of Sciences of the United States of America 106, 18621–18626.
| Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama.Crossref | GoogleScholarGoogle Scholar | 19841276PubMed |
Kuzmina ML, Johnson KL, Barron HR, Hebert PD (2012) Identification of the vascular plants of Churchill, Manitoba, using a DNA barcode library. BMC Ecology 12, 25
| Identification of the vascular plants of Churchill, Manitoba, using a DNA barcode library.Crossref | GoogleScholarGoogle Scholar | 23190419PubMed |
Kyalangalilwa B, Boatwright JS, Daru BH, Maurin O, van der Bank M (2013) Phylogenetic position and revised classification of Acacia s.l. (Fabaceae: Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia. Botanical Journal of the Linnean Society 172, 500–523.
| Phylogenetic position and revised classification of Acacia s.l. (Fabaceae: Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia.Crossref | GoogleScholarGoogle Scholar |
Le Roux JJ, Strasberg D, Rouget M, Morden CW, Koordom M, Richardson DM (2014) Relatedness defies biogeography: the tale of two island endemics (Acacia heterophylla and A. koa). New Phytologist 204, 230–242.
| Relatedness defies biogeography: the tale of two island endemics (Acacia heterophylla and A. koa).Crossref | GoogleScholarGoogle Scholar | 24942529PubMed |
Levin RA, Wagner WL, Hoch PC, Nepokroeff M, Pires JC, Zimmer EA, Sytsma KJ (2003) Family‐level relationships of Onagraceae based on chloroplast rbcL and ndhF data. American Journal of Botany 90, 107–115.
| Family‐level relationships of Onagraceae based on chloroplast rbcL and ndhF data.Crossref | GoogleScholarGoogle Scholar | 21659085PubMed |
Li Y, Dressler S, Zhang D, Renner SS (2009) More Miocene dispersal between Africa and Asia; the case of Bridelia (Phyllanthaceae). Systematic Botany 34, 521–529.
| More Miocene dispersal between Africa and Asia; the case of Bridelia (Phyllanthaceae).Crossref | GoogleScholarGoogle Scholar |
Malcomber ST (2002) Phylogeny of Gaertnera Lam. (Rubiaceae) based on multiple DNA markers: evidence of a rapid radiation in a widespread, morphologically diverse genus. Evolution 56, 42–57.
| Phylogeny of Gaertnera Lam. (Rubiaceae) based on multiple DNA markers: evidence of a rapid radiation in a widespread, morphologically diverse genus.Crossref | GoogleScholarGoogle Scholar | 11913666PubMed |
Maslin B (2008) Generic and subgeneric names in Acacia following retypification of the genus. Muelleria 26, 7–9.
Maslin BR, Miller J, Seigler DS (2003) Overview of the generic status of Acacia (Leguminosae: Mimosoideae). Australian Systematic Botany 16, 1–18.
| Overview of the generic status of Acacia (Leguminosae: Mimosoideae).Crossref | GoogleScholarGoogle Scholar |
Maslin BR, Seigler DS, Ebinger J (2013) New combinations in Senegalia and Vachellia (Leguminosae: Mimosoideae) for Southeast Asia and China. Blumea 58, 39–44.
| New combinations in Senegalia and Vachellia (Leguminosae: Mimosoideae) for Southeast Asia and China.Crossref | GoogleScholarGoogle Scholar |
McEvoy PB (1996) Host specificity and biological pest control. Bioscience 46, 401–405.
| Host specificity and biological pest control.Crossref | GoogleScholarGoogle Scholar |
Miller MF (1995) Acacia seed survival, seed-germination and seedling growth following pod consumption by large herbivores and seed chewing by rodents. African Journal of Ecology 33, 194–210.
| Acacia seed survival, seed-germination and seedling growth following pod consumption by large herbivores and seed chewing by rodents.Crossref | GoogleScholarGoogle Scholar |
Miller JT, Murphy DJ, Ho SYW, Cantrill DJ, Seigler D (2013) Comparative dating of Acacia: combining fossils and multiple phylogenies to infer ages of clades with poor fossil records. Australian Journal of Botany 61, 436–445.
| Comparative dating of Acacia: combining fossils and multiple phylogenies to infer ages of clades with poor fossil records.Crossref | GoogleScholarGoogle Scholar |
Muellner AN, Pannell CM, Coleman A, Chase MW (2008) The origin and evolution of Indomalesian, Australasian and Pacific island biotas: insights from Aglaieae (Meliaceae, Sapindales). Journal of Biogeography 35, 1769–1789.
| The origin and evolution of Indomalesian, Australasian and Pacific island biotas: insights from Aglaieae (Meliaceae, Sapindales).Crossref | GoogleScholarGoogle Scholar |
Nelson G (1978) From Candolle to Croizat: comments on the history of biogeography. Journal of the History of Biology 11, 269–305.
| From Candolle to Croizat: comments on the history of biogeography.Crossref | GoogleScholarGoogle Scholar | 11610435PubMed |
New TR (1984) ‘A Biology of Acacias.’ (Oxford University Press: Oxford, UK)
Newmaster SG, Subramanyam R (2009) Testing plant barcoding in a sister species complex of pantropical Acacia (Mimosoideae, Fabaceae). Molecular Ecology Resources 9, 172–180.
| Testing plant barcoding in a sister species complex of pantropical Acacia (Mimosoideae, Fabaceae).Crossref | GoogleScholarGoogle Scholar |
Orchard AE, Maslin BR (2003) (1584) Proposal to conserve the name Acacia (Leguminosae: Mimosoideae) with a conserved type. Taxon 52, 362–363.
| (1584) Proposal to conserve the name Acacia (Leguminosae: Mimosoideae) with a conserved type.Crossref | GoogleScholarGoogle Scholar |
Palmer B, Lockett C, Dhileepan K (2012) Acacia nilotica subsp. indica (Benth.) Brenan: prickly acacia. In ‘Biological Control of Weeds in Australia’. (Eds M Julien, R McFadyen, J Cullen) pp. 18–28. (CSIRO Publishing: Melbourne, Vic., Australia)
Pascov C, Nevill P, Elliott C, Majer J, Anthony J, Krauss S (2015) The critical role of ants in the extensive dispersal of Acacia seeds revealed by genetic parentage assignment. Oecologia 179, 1123–1134.
| The critical role of ants in the extensive dispersal of Acacia seeds revealed by genetic parentage assignment.Crossref | GoogleScholarGoogle Scholar | 26255273PubMed |
Pedley L (2002) A conspectus of Acacia subg. Acacia in Australia. Austrobaileya 6, 177–186.
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA, Susko E (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
| Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |
Raven PH, Axelrod DI (1972) Plate tectonics and Australasian paleobiogeography. Science 176, 1379–1386.
| Plate tectonics and Australasian paleobiogeography.Crossref | GoogleScholarGoogle Scholar | 17834636PubMed |
Renner SS (2005) Relaxed molecular clocks for dating historical plant dispersal events. Trends in Plant Science 10, 550–558.
| Relaxed molecular clocks for dating historical plant dispersal events.Crossref | GoogleScholarGoogle Scholar | 16226053PubMed |
Ridley A, Hereward J, Daglish G, Raghu S, McCulloch G, Walter G (2016) Flight of Rhyzopertha dominica (Coleoptera: Bostrichidae): a spatio-temporal analysis with pheromone trapping and population genetics. Journal of Economic Entomology 109, 2561–2571.
| Flight of Rhyzopertha dominica (Coleoptera: Bostrichidae): a spatio-temporal analysis with pheromone trapping and population genetics.Crossref | GoogleScholarGoogle Scholar | 27986943PubMed |
Rosen DE (1978) Vicariant patterns and historical explanation in biogeography. Systematic Zoology 27, 159–188.
| Vicariant patterns and historical explanation in biogeography.Crossref | GoogleScholarGoogle Scholar |
Ross JH (1981) An analysis of the African Acacia species: their distribution, possible origins and relationships. Bothalia: African Biodiversity & Conservation 13, 389–413.
| An analysis of the African Acacia species: their distribution, possible origins and relationships.Crossref | GoogleScholarGoogle Scholar |
Sabiiti EN, Wein RW (1987) Fire and Acacia seeds: a hypothesis of colonization success. Journal of Ecology 75, 937–946.
| Fire and Acacia seeds: a hypothesis of colonization success.Crossref | GoogleScholarGoogle Scholar |
Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84, 1120–1136.
| Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae).Crossref | GoogleScholarGoogle Scholar | 21708667PubMed |
Swofford DL (2003) ‘PAUP*. Phylogenetic analysis using parsimony (*and other methods).’ (Sinauer Associates: Sunderland, MA, USA)
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
| Universal primers for amplification of three non-coding regions of chloroplast DNA.Crossref | GoogleScholarGoogle Scholar | 1932684PubMed |
Tate JA, Simpson BB (2003) Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploid species. Systematic Botany 28, 723–737.
Viana DS, Gangoso L, Bouten W, Figuerola J (2016) Overseas seed dispersal by migratory birds. Proceedings of the Royal Society of London – B. Biological Sciences 283, 20152406
| Overseas seed dispersal by migratory birds.Crossref | GoogleScholarGoogle Scholar |
