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

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.

[1]  N. Burbidge The phytogeography of the Australian region. , 1960 .

[2]  R. Hill History of the Australian vegetation : cretaceous to recent , 2017 .

[3]  C. Peichel,et al.  Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks , 2007, Journal of evolutionary biology.

[4]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[5]  D. Steane,et al.  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? , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  V. Funk,et al.  Recent assembly of the global herbaceous flora: evidence from the paper daisies (Asteraceae: Gnaphalieae). , 2016, The New phytologist.

[7]  O. Kaltz,et al.  Is the Prunella (Lamiaceae) hybrid zone structured by an environmental gradient? Evidence from a reciprocaltransplant experiment. , 2000, American journal of botany.

[8]  H. Linder,et al.  Cape diversification and repeated out-of-southern-Africa dispersal in paper daisies (Asteraceae-Gnaphalieae). , 2009, Molecular phylogenetics and evolution.

[9]  D. Greber,et al.  Phylogeny of Australian Gnaphalieae (Asteraceae) Based on Chloroplast and Nuclear Sequences, the trnL Intron, trnL/trnF Intergenic Spacer, matK, and ETS , 2009 .

[10]  Michael J. Landis,et al.  Bayesian analysis of biogeography when the number of areas is large. , 2013, Systematic biology.

[11]  Bin Ma,et al.  From Gene Trees to Species Trees , 2000, SIAM J. Comput..

[12]  Ramón Doallo,et al.  CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics , 2012, Nature Methods.

[13]  Fredrik Ronquist,et al.  Dispersal-Vicariance Analysis: A New Approach to the Quantification of Historical Biogeography , 1997 .

[14]  N. Matzke,et al.  Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades. , 2014, Systematic biology.

[15]  A. Schmidt‐Lebuhn,et al.  Phylogenetic relationships of the Australasian shrubby everlastings Ozothamnus and Cassinia (Asteraceae: Asteroideae: Gnaphalieae) , 2013, Cladistics : the international journal of the Willi Hennig Society.

[16]  W. Maddison Gene Trees in Species Trees , 1997 .

[17]  A. Schmidt‐Lebuhn,et al.  Generic boundaries of Leucochrysum and Waitzia (Asteraceae: Gnaphalieae) , 2015, Australian Systematic Botany.

[18]  N. Matzke Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing , 2013 .

[19]  Bryan C. Carstens,et al.  Delimiting species without monophyletic gene trees. , 2007, Systematic biology.

[20]  L. Rieseberg,et al.  Adaptation with gene flow across the landscape in a dune sunflower , 2012, Molecular ecology.

[21]  R. Wray,et al.  The geoheritage and geomorphology of the sandstone pagodas of the North-western Blue Mountains Region (NSW) , 2011 .

[22]  O. Gascuel,et al.  SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. , 2010, Molecular biology and evolution.

[23]  Anton Nekrutenko,et al.  Manipulation of FASTQ data with Galaxy , 2010, Bioinform..

[24]  S. Gallagher,et al.  Cenozoic stratigraphic succession in southeastern Australia , 2004 .

[25]  M. Kearney,et al.  Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota , 2008, Molecular ecology.

[26]  A. Drummond,et al.  Bayesian Inference of Species Trees from Multilocus Data , 2009, Molecular biology and evolution.

[27]  M. Crisp,et al.  How Was the Australian Flora Assembled Over the Last 65 Million Years? A Molecular Phylogenetic Perspective , 2013 .

[28]  L. Nakhleh,et al.  Computational approaches to species phylogeny inference and gene tree reconciliation. , 2013, Trends in ecology & evolution.

[29]  O. Gascuel,et al.  Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. , 2006, Systematic biology.

[30]  M. Chapman,et al.  Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae) , 2007, Theoretical and Applied Genetics.

[31]  S. McLoughlin The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism , 2001 .

[32]  M. Nei,et al.  Relationships between gene trees and species trees. , 1988, Molecular biology and evolution.

[33]  N. Walsh,et al.  Elevation of rank for Leucochrysum albicans var. tricolor (Asteraceae: Gnaphalieae) , 2015 .

[34]  Tandy J. Warnow,et al.  ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes , 2015, Bioinform..

[35]  É. Tannier,et al.  The Inference of Gene Trees with Species Trees , 2013, Systematic biology.

[36]  Richard H. Ree,et al.  Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. , 2008, Systematic biology.

[37]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[38]  B. Mishler,et al.  Quantifying Phytogeographical Regions of Australia Using Geospatial Turnover in Species Composition , 2014, PloS one.