Comparative dating of Acacia: combining fossils and multiple phylogenies to infer ages of clades with poor fossil records
Joseph T. Miller A E , Daniel J. Murphy B , Simon Y. W. Ho C , David J. Cantrill B and David Seigler D
+ Author Affiliations
- Author Affiliations
A Centre for Australian National Biodiversity Research, CSIRO Plant Industry, GPO Box 1600 Canberra, ACT 2601, Australia.
B Royal Botanic Gardens Melbourne, Birdwood Avenue, South Yarra, Vic. 3141, Australia.
C School of Biological Sciences, Edgeworth David Building, University of Sydney, Sydney, NSW 2006, Australia.
D Department of Plant Biology, University of Illinois, Urbana, IL 61801, USA.
E Corresponding author. Email: joe.miller@csiro.au
Australian Journal of Botany 61(6) 436-445 https://doi.org/10.1071/BT13149
Submitted: 4 June 2013 Accepted: 20 July 2013 Published: 23 September 2013
Abstract
The ubiquitous and highly diverse element Australian Acacia makes an ideal candidate for investigating a range of questions about the evolution of the flora of continental Australia. In the past, such efforts have been hampered by a lack of well-supported phylogenies and by the relatively poor macrofossil record, which probably reflects the depositional environment in which Acacia species are predominantly found. However, the broader subfamily Mimosoideae offers several reliably age-constrained fossils that can be used as calibrations in divergence-dating analyses of DNA sequence data. In addition, the microfossil pollen record of Acacia is relatively rich and provides a good age constraint for the entire Acacia clade. By using multiple reliable fossil constraints, we applied a combination of primary calibration points to produce a comprehensive study of divergence dates in Acacia s.s. and related mimosoid legumes. Previous dating studies included very limited samples of the diversity of Australian Acacia and experienced difficulties in identifying appropriate age calibrations for the lineage, leading to considerable variation in their results. We used novel calibration schemes and multiple nuclear and chloroplast DNA sequence markers to produce the first estimates of divergence dates for major lineages within the Australian Acacia s.s. clade and for related lineages across the Mimosoideae subfamily. We estimate average crown divergence dates for Vachellia at 13–17 Ma, Senegalia at 31.0–33.4 Ma and Acacia s.s. at 21.0–23.9 Ma. The timing of radiations within these lineages is consistent with the hypothesis that Miocene aridification in Africa, the Americas and Australia was a driver for the diversificationss of lineages in Acacia s.l.
Additional keywords: Australia, divergence dating, legumes, Mimosoideae, Senegalia, Vachellia.
References
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 | 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 |
Brown GK, Ariati SR, Murphy DJ, Miller JTH, Ladiges PY (2006) Bipinnate acacias (Acacia subg. Phyllodineae sect. Botrycephalae) of eastern Australia are polyphyletic based on DNA sequence data. Australian Systematic Botany 19, 315–326.
| Bipinnate acacias (Acacia subg. Phyllodineae sect. Botrycephalae) of eastern Australia are polyphyletic based on DNA sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XoslGlt7o%3D&md5=cc203df0f5d53f5964f7468c4dbedcffCAS |
Brown GK, Murphy DJ, Miller JT, Ladiges PY (2008) Acacia s.s. and its relationship among tropical legumes, Tribe Ingeae (Leguminosae: Mimosoideae). Systematic Botany 33, 739–751.
| Acacia s.s. and its relationship among tropical legumes, Tribe Ingeae (Leguminosae: Mimosoideae).Crossref | GoogleScholarGoogle Scholar |
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 biogeographical tracks. Cladistics 27, 380–390.
| Relationships of the Australo-Malesian genus Paraserianthes (Mimosoideae: Leguminosae) identifies the sister group of Acacia sensu stricto and two biogeographical tracks.Crossref | GoogleScholarGoogle Scholar |
Bruneau A, Mercure M, Lewis GP, Herendeen PS (2008) Phylogenetic patterns and diversification in caesalpinioid legumes. Botany 86, 697–718.
| Phylogenetic patterns and diversification in caesalpinioid legumes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsFegurw%3D&md5=ad9f3dc30f94108ae598563bde40d2faCAS |
Burnham RJ, Johnson KR (2004) South American paleobotany and the origins of neotropical rainforests. Philosophical Transactions of the Royal Society of London Series B 359, 1595–1610.
Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MAJ, Cooper S, Donnellan SC, Keogh JS, Leys R, Melville J, Murphy DJ, Porch N, Wyrwoll K-H (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 | 1:STN:280:DC%2BD1cjhvFGruw%3D%3D&md5=b2c8561f20ea2518196b38b557e28e8bCAS | 18761619PubMed |
Caccavari MA, Barreda V (2000) A new calymmate mimosoid polyad from the Miocene of Argentina. Review of Palaeobotany and Palynology 109, 197–203.
| A new calymmate mimosoid polyad from the Miocene of Argentina.Crossref | GoogleScholarGoogle Scholar |
Cookson IC (1954) The Cainozoic occurrence of Acacia in Australia. Australian Journal of Botany 2, 52–59.
| The Cainozoic occurrence of Acacia in Australia.Crossref | GoogleScholarGoogle Scholar |
Crepet WL, Taylor DW (1986) Primitive mimosoid flowers from the Paleocene–Eocene and their systematic and evolutionary implications. American Journal of Botany 73, 548–563.
dos Reis M, Yang Z (2011) Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times. Molecular Biology and Evolution 28, 2161–2172.
| Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsFWitrs%3D&md5=2b5d8dd04c61a15b04b2bc465ecc6f60CAS | 21310946PubMed |
Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88
| Relaxed phylogenetics and dating with confidence.Crossref | GoogleScholarGoogle Scholar | 16683862PubMed |
Gandolfo MA, Nixon KC, Crepet WL (2008) Selection of fossils for calibration of molecular dating models. Annals of the Missouri Botanical Garden 95, 34–42.
| Selection of fossils for calibration of molecular dating models.Crossref | GoogleScholarGoogle Scholar |
Gómez-Acevedo S, Rico-Arce L, Delgado-Salinas A, Magallon 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 |
Guinet P (1981) Mimosoideae: the characters of their pollen grains. In ‘Advances in legume systematics part 2’. (Eds RM Polhill and PH Raven) pp. 835–855. (Kew Botanic Gardens: Kew)
Herendeen PS, Jacobs BF (2000) Fossil legumes from the Middle Eocene (46.0 Ma) Mahenge flora of Singida, Tanzania. American Journal of Botany 87, 1358–1366.
| Fossil legumes from the Middle Eocene (46.0 Ma) Mahenge flora of Singida, Tanzania.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngt12mug%3D%3D&md5=e80cafefee99ce63db64644edb8728e0CAS | 10991905PubMed |
Ho SYW, Phillips MJ (2009) Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Systematic Biology 58, 367–380.
| Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times.Crossref | GoogleScholarGoogle Scholar |
Jordan GJ (1997) Evidence of Pleistocene plant extinction and diversity from Regatta Point, western Tasmania, Australia. Botanical Journal of the Linnean Society 123, 45–71.
| Evidence of Pleistocene plant extinction and diversity from Regatta Point, western Tasmania, Australia.Crossref | GoogleScholarGoogle Scholar |
Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
| PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=1796bd8593596be288ce89b717ba00d3CAS | 22319168PubMed |
Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Systematic Biology 54, 575–594.
| Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary.Crossref | GoogleScholarGoogle Scholar | 16085576PubMed |
Lewis GP, Schrire B, Mackinder B, Lock M (2005) ‘Legumes of the world.’ (Royal Botanic Gardens: Kew)
Luckow M, Miller JT, Murphy DJ, Livshultz T (2003) A phylogenetic analysis of the Mimosoideae (Leguminosae) based on chloroplast DNA sequence data. In ‘Advances in legume systematics, part 10’. (Eds BB Klitgaard and A Bruneau) pp. 197–220. (Royal Botanic Gardens: Kew)
Macphail MK, Hill RS (2001) Palaeobotany of Acacia and related Mimosaceae. In ‘Flora of Australia. Volume 11A: Mimosaceae, Acacia part 1’. (Ed. Australian Biological Resource Study) pp. 13–29. (CSIRO Publishing: Melbourne)
Maslin BR (2001) ‘Flora of Australia vol. 11A. Mimosaceae, Acacia Part 1.’ (Ed. Australian Biological Resource Study) (CSIRO Publishing: Melbourne)
Miller JT, Bayer RJ (2000) Molecular phylogenetics of Acacia (Fabaceae: Mimosoideae) based on chloroplast TrnK/MatK and nuclear histone H3-D sequences. In ‘Advances in legume systematics 9’. (Eds PS Herendeen and A Bruneau) pp. 181–200. (Royal Botanic Gardens: Kew)
Miller JT, Bayer RJ (2003) Molecular phylogenetics of Acacia subgenera Acacia and Aculeiferum (Fabaceae: Mimosoideae), based on the chloroplast matK coding sequence and flanking trnK intron spacer regions. Australian Systematic Botany 16, 27–33.
| Molecular phylogenetics of Acacia subgenera Acacia and Aculeiferum (Fabaceae: Mimosoideae), based on the chloroplast matK coding sequence and flanking trnK intron spacer regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1yru7o%3D&md5=1f9a9770133839b55c23787ea0237428CAS |
Miller JT, Burd M (2013) Australia’s Acacia: unrecognized convergent evolution. In ‘Invasion biology and ecosystem theory; insights from a continent in transformation’. (Eds H Prins and I Gordon) In press. (Cambridge University Press: Cambridge)
Miller JT, Seigler D (2012) Evolutionary and taxonomic relationships of Acacia s.l. (Leguminosae: Mimosoideae). Australian Systematic Botany 25, 217–224.
| Evolutionary and taxonomic relationships of Acacia s.l. (Leguminosae: Mimosoideae).Crossref | GoogleScholarGoogle Scholar |
Miller JT, Andrew R, Bayer RJ (2003a) 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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksFSlurs%3D&md5=82f3dcd776fd72b9a706c67828fd06f6CAS |
Miller JT, Grimes JW, Murphy DJ, Bayer RJ, Ladiges PY (2003b) A phylogenetic analysis of the Acacieae and Ingeae (Mimosoideae: Fabaceae) based on trnK, matK, psbA-trnH, and trnL/trnF sequence data. Systematic Botany 28, 558–566.
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 | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1yru78%3D&md5=6d6a5374317dedc1083924989902b49cCAS |
Murphy DJ, Brown GK, Miller JT, Ladiges PY (2010) Molecular phylogeny of Acacia Mill. (Mimosoideae: Leguminosae): evidence for major clades and informal classification. Taxon 59, 7–19.
Porch N, Jordan GJ, Price DM, Barnes RW, Macphail MK, Pemberton M (2009) Last interglacial climates of south-eastern Australia: plant and beetle-based reconstructions from Yarra Creek, King Island, Tasmania. Quaternary Science Reviews 28, 3197–3210.
| Last interglacial climates of south-eastern Australia: plant and beetle-based reconstructions from Yarra Creek, King Island, Tasmania.Crossref | GoogleScholarGoogle Scholar |
Rambaut A, Drummond A (2007) ‘Tracer.’ (Oxford University Press: Oxford)
Sauquet H, Ho SYW, Gandolfo MA, Jordan GJ, Wilf P, Cantrill DJ, Bayly MJ, Bromham L, Brown GK, Carpenter RJ, Lee DM, Murphy DJ, Sniderman JMK, Udovicic F (2012) Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales). Systematic Biology 61, 289–313.
| Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales).Crossref | GoogleScholarGoogle Scholar | 22201158PubMed |
Simon MF, Grether R, de Queiroz LP, Skema C, Pennington RT, Hughes CE (2009) Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proceedings of the National Academy of Sciences of the United States of America 106, 20 359–20 364.
| Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFSqtQ%3D%3D&md5=5f9e2fa4529062b0a8c5ecc628fa2dfaCAS |
Sniderman JMK, Jordan GJ, Cowling RM (2013) Fossil evidence for a hyperdiverse sclerophyll flora under a non-Mediterranean-type climate. Proceedings of the National Academy of Sciences of the United States of America 110, 3423–3428.
| Fossil evidence for a hyperdiverse sclerophyll flora under a non-Mediterranean-type climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkvFyntro%3D&md5=9f81498b6464dac258a7fa85828564b3CAS |
Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution 39, 306–314.
