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

From the desert it came: evolution of the Australian paper daisy genus Leucochrysum (Asteraceae, Gnaphalieae)

Alexander N. Schmidt-Lebuhn A C and Kiarrah J. Smith B
+ Author Affiliations
- Author Affiliations

A CSIRO, Australian National Herbarium, GPO Box 1600, Canberra, ACT 2601, Australia.

B 1238 Bells Line of Road, Kurrajong Heights, NSW 2758, Australia.

C Correspondending author. Email: alexander.s-l@csiro.au

Australian Systematic Botany 29(3) 176-184 https://doi.org/10.1071/SB16012
Submitted: 1 April 2016  Accepted: 17 June 2016   Published: 29 November 2016

Abstract

Present patterns of diversity in the Australian flora have been shaped by increasing seasonality since the Eocene, and by pronounced aridification in the past 3 million years. Arid-zone plants are commonly hypothesised to be the products of radiations of ancestrally temperate or coastal lineages, as in the case of the everlasting paper daisy tribe Gnaphalieae (Asteraceae). However, these inferences are often based on higher-level phylogenies, whereas evolutionary processes in the Australian Gnaphalieae have rarely been studied at the species level. Here, we reconstructed the phylogeny and biogeographic history of the small, but ecologically diverse, paper daisy genus Leucochrysum, to examine recent habitat shifts and character changes, at the same time exploring the feasibility of using amplicon sequencing of low-copy nuclear gene regions to resolve phylogenetic relationships in Australian Gnaphalieae. On the balance of evidence, outgroup comparison and ancestral-area reconstruction support an ancestral range in the arid zone with subsequent diversification towards the south-east, demonstrating a complex evolutionary history with a re-colonisation of temperate areas. Low amplification success rates suggest that methods other than amplicon sequencing of currently available primers will be more promising for molecular phylogenetic work at a larger scale.

Additional keywords: historical biogeography, hoary sunray.


References

Andrew RL, Ostevik KL, Ebert DP, Rieseberg LH (2012) Adaptation with gene flow across the landscape in a dune sunflower. Molecular Ecology 21, 2078–2091.
Adaptation with gene flow across the landscape in a dune sunflower.CrossRef |

Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539–552.
Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative.CrossRef |

Bayer RJ, Greber DG, Bagnall NH (2002) Phylogeny of Australian Gnaphalieae (Asteraceae) based on chloroplast and nuclear sequences, the trnL intron, trnL/trnF intergenic spacer, matK, and ETS. Systematic Botany 27, 801–814.

Bergh NG, Linder PH (2009) Cape diversification and repeated out-of-southern-Africa dispersal in paper daisies (Asteraceae–Gnaphalieae). Molecular Phylogenetics and Evolution 51, 5–18.
Cape diversification and repeated out-of-southern-Africa dispersal in paper daisies (Asteraceae–Gnaphalieae).CrossRef |

Blankenberg D, Gordon A, Kuster GV, Coraor N, Taylor J, Nekrutenko A (2010) Manipulation of FASTQ data with Galaxy. Bioinformatics 26, 1783–1785.
Manipulation of FASTQ data with Galaxy.CrossRef | 1:CAS:528:DC%2BC3cXotleqsL0%3D&md5=0d563902e01e05f4124849d179652dd9CAS |

Burbidge N (1960) The phytogeography of the Australian region. Australian Journal of Botany 8, 75–211.
The phytogeography of the Australian region.CrossRef |

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 | 1:STN:280:DC%2BD1cjhvFGruw%3D%3D&md5=2b12a4d7a8eca8300a43b294a15af11dCAS |

Chapman MA, Chang J, Weisman D, Kesseli RV, Burke JM (2007) Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae). Theoretical and Applied Genetics 115, 747–755.
Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae).CrossRef | 1:CAS:528:DC%2BD2sXhtVKru7%2FJ&md5=7e64946d272b1835a8b030f695d412d5CAS |

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 |

Crisp M, Cook L, Steane D (2004) Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences 359, 1551–1571.
Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities?CrossRef |

Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.
jModelTest 2: more models, new heuristics and parallel computing.CrossRef | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=05295880fd404aca6e6c641989659034CAS |

Dennis RJ, Walsh NG (2010) A revision of the Leucochrysum albicans (Asteraceae: Gnaphalieae) complex. Muelleria 28, 122–135.

Department of the Environment (2008) Outback Australia: the rangelands. Available at https://www.environment.gov.au/land/rangelands [Verified 20 May 2016]

Fritsche F, Kaltz O (2000) Is the Prunella (Lamiaceae) hybrid zone structured by an environmental gradient? Evidence from a reciprocaltransplant experiment. American Journal of Botany 87, 995–1003.
Is the Prunella (Lamiaceae) hybrid zone structured by an environmental gradient? Evidence from a reciprocaltransplant experiment.CrossRef | 1:STN:280:DC%2BC3Mngt12hsg%3D%3D&md5=8a409965d50c3e20f4850c46e5f3c72dCAS |

González-Orozco CE, Ebach MC, Laffan S, Thornhill AH, Knerr NJ, Schmidt-Lebuhn AN, Cargill CC, Clements M, Nagalingum NS, Mishler BD, Miller JT (2014) Quantifying phytogeographical regions of Australia using geospatial turnover in species composition. PLoS One 9, e92558
Quantifying phytogeographical regions of Australia using geospatial turnover in species composition.CrossRef |

Goodwin PB (1996) Selection and trialing of eastern Australian native plants as bedding plants. Horticultural Research and Development Corporation, NY009. Available at http://www.ngia.com.au/Story?Action=View&Story_id=1737 [Verified 2 January 2014]

Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.
SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building.CrossRef | 1:CAS:528:DC%2BC3cXntlGgtw%3D%3D&md5=486e7bb27cbcbb5feea80ce748df48c8CAS |

Gow JL, Peichel CL, Taylor EB (2007) Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. Journal of Evolutionary Biology 20, 2173–2180.
Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks.CrossRef | 1:STN:280:DC%2BD2snjtFaitg%3D%3D&md5=a4720a672e264582ff2b635163262c6dCAS |

Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.CrossRef | 1:CAS:528:DC%2BC3cXks1Kms7s%3D&md5=0efd51eba9a2cd9a0e5b3907d50b71feCAS |

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.

Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27, 570–580.
Bayesian inference of species trees from multilocus data.CrossRef | 1:CAS:528:DC%2BC3cXitlart7s%3D&md5=69ba1f6af2e98711a5f06f4f3613c9d2CAS |

Hill RS (1994) ‘History of the Australian Vegetation: Cretaceous to Recent.’ (Cambridge University Press, Cambridge, UK)

Knowles LL, Carstens BC (2007) Delimiting species without monophyletic gene trees. Systematic Biology 56, 887–895.
Delimiting species without monophyletic gene trees.CrossRef |

Landis MJ, Matzke NJ, Moore BR, Huelsenbeck JP (2013) Bayesian analysis of biogeography when the number of areas is large. Systematic Biology 62, 789–804.
Bayesian analysis of biogeography when the number of areas is large.CrossRef |

Maddison WP (1997) Gene trees in species trees. Systematic Biology 46, 523–536.
Gene trees in species trees.CrossRef |

Matzke NJ (2013) Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Frontiers of Biogeography 5, 242–248.

Matzke NJ (2014) Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Systematic Biology 63, 951–970.
Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades.CrossRef |

McGowran B, Holdgate GR, Li Q, Gallagher SJ (2004) Cenozoic stratigraphic succession in southeastern Australia. Australian Journal of Earth Sciences 51, 459–496.
Cenozoic stratigraphic succession in southeastern Australia.CrossRef |

McLoughlin S (2001) The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Australian Journal of Botany 49, 271–300.
The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism.CrossRef |

Mirarab S, Warnow T (2015) ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, i44–i52.
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes.CrossRef | 1:CAS:528:DC%2BC28Xht1Cit7vF&md5=4da9f532dd9efd132d2b35a0fe5ef09cCAS |

Nakhleh L (2013) Computational approaches to species phylogeny inference and gene tree reconciliation. Trends in Ecology & Evolution 28, 719–728.
Computational approaches to species phylogeny inference and gene tree reconciliation.CrossRef |

Nie Z-L, Funk VA, Meng Y, Deng T, Sun H, Wen J (2016) Recent assembly of the global herbaceous flora: evidence from the paper daisies (Asteraceae: Gnaphalieae). New Phytologist 209, 1795–1806.
Recent assembly of the global herbaceous flora: evidence from the paper daisies (Asteraceae: Gnaphalieae).CrossRef | 1:CAS:528:DC%2BC28Xit12mtrg%3D&md5=4557f910cfefad4e2f5e6d5a5d8277d5CAS |

Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Molecular Biology and Evolution 5, 568–583.

Ree RH, Smith SA (2008) Maximum Likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57, 4–14.
Maximum Likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis.CrossRef |

Ronquist F (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology 46, 195–203.
Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography.CrossRef |

Schmidt-Lebuhn AN, Constable L (2013) Phylogenetic relationships of the Australasian shrubby everlastings Ozothamnus and Cassinia (Asteraceae: Asteroideae: Gnaphalieae). Cladistics 29, 574–588.
Phylogenetic relationships of the Australasian shrubby everlastings Ozothamnus and Cassinia (Asteraceae: Asteroideae: Gnaphalieae).CrossRef |

Schmidt-Lebuhn AN, Bruhl JJ, Telford IRH, Wilson PG (2015) Phylogenetic relationships of Coronidium, Xerochrysum and several neglected Australian species of ‘Helichrysum’ (Asteraceae: Gnaphalieae). Taxon 64, 96–109.
Phylogenetic relationships of Coronidium, Xerochrysum and several neglected Australian species of ‘Helichrysum’ (Asteraceae: Gnaphalieae).CrossRef |

Sinclair SJ (2011) National recovery plan for the hoary sunray Leucochrysum albicans var. tricolor. (Victorian Government Department of Sustainability and Environment: Melbourne) Available at https://www.environment.gov.au/system/files/resources/9d3c877f-78e6-4ca0-906b-6567e205251e/files/leucochrysum-albicans.pdf [Verified 18 July 2016]

Szöllősi GJ, Tannier E, Daubin V, Boussau B (2015) The inference of gene trees with species trees. Systematic Biology 64, e42–e62.
The inference of gene trees with species trees.CrossRef |

Walsh NG (2015) Elevation of rank for Leucochrysum albicans var. tricolor (Asteraceae: Gnaphalieae). Muelleria 34, 11–13.

Washington HG, Wray RA (2011) The geoheritage and geomorphology of the sandstone pagodas of the north-western blue mountains region (NSW). Proceedings of the Linnean Society of New South Wales 132, 131–143.

Weber XA, Schmidt-Lebuhn AN (2015) Generic boundaries of Leucochrysum and Waitzia (Asteraceae: Gnaphalieae). Australian Systematic Botany 28, 203–218.
Generic boundaries of Leucochrysum and Waitzia (Asteraceae: Gnaphalieae).CrossRef |



Supplementary MaterialSupplementary Material (292 KB) Export Citation Cited By (1)

View Altmetrics