Plant Systematics and Evolution

, Volume 305, Issue 7, pp 503–520 | Cite as

Phylogeography, classification and conservation of pink zieria (Zieria veronicea; Rutaceae): influence of changes in climate, geology and sea level in south-eastern Australia

  • Will C. Neal
  • Elizabeth A. James
  • Michael J. BaylyEmail author
Original Article


We assessed genetic variation in the Australian shrub Zieria veronicea across its current distribution and used environmental niche modelling to predict its distribution at the Last Glacial Maximum (LGM). The species range, from Kangaroo Island in South Australia to northern Tasmania, includes substantial overland and marine disjunctions of up to ~ 500 km. By inferring historical patterns of connectivity and genetic differentiation from DNA sequences and AFLP data, we aimed to provide new insight into the history of the species-rich sclerophyll vegetation in south-eastern Australia. Genetic differentiation of populations was not correlated with the size of geographic disjunctions. The deepest genetic divergence was between populations on Kangaroo Island and the adjacent mainland, separated by a strait only 13 km wide. Populations in western Victoria and Tasmania, separated by the 300 km of Bass Strait, showed the lowest genetic differentiation. This pattern is consistent with dispersal of Z. veronicea into Tasmania, across the Bassian Plain, possibly as recently as the LGM, in line with inferred distribution at that time. Genetic patterns, soil ages and niche models support Quaternary colonisation of the lower Murray Basin, potentially from eastern South Australia. The history of a large (500 km) disjunction between populations in western and eastern Victoria is unclear; historical connectivity of populations through suitable habitats is assumed, but the timing and location of connections are not clear. Genetic data support the current recognition of two subspecies and their treatment as distinct entities under conservation legislation.


AFLP Australian biogeography Environmental niche modelling Murray Basin Tasmania Taxonomy 



For assistance with fieldwork or provision of specimens, we thank Ruby Wilson, Todd McLay, Duncan Fraser and Rose Barrett. Plant collecting permits were provided by the former Department of Sustainability and Environment (Victoria), the Department of Primary Industries, Parks, Water and Environment (Tasmania) and the Department for Environment, Water and Natural Resources (South Australia). This work was partly supported by an Early Career Researcher grant to MJB from The University of Melbourne and a David H. Ashton Scholarship to WCN from The University of Melbourne Botany Foundation.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

606_2019_1589_MOESM1_ESM.pdf (55 kb)
Supplementary material 1 (PDF 54 kb)


  1. Armstrong JA (1991) Studies on pollination and systematics in the Australian Rutaceae. PhD thesis, University of New South Wales, SydneyGoogle Scholar
  2. Armstrong JA (2002) The genus Zieria (Rutaceae): a systematic and evolutionary study. Austral Syst Bot 15:277–463CrossRefGoogle Scholar
  3. AVH (2018) The Australasian Virtual Herbarium, Council of Heads of Australasian Herbaria.
  4. Barrett RA, Bayly MJ, Duretto MF, Forster PI, Ladiges PY, Cantrill DJ (2015) A chloroplast phylogeny of Zieria (Rutaceae) in Australia and New Caledonia shows widespread incongruence with species-level taxonomy. Austral Syst Bot 27:427–449CrossRefGoogle Scholar
  5. Barrett RA, Bayly MJ, Duretto MF, Forster PI, Ladiges PY, Cantrill DJ (2018) Phylogenetic analysis of Zieria (Rutaceae) in Australia and New Caledonia based on nuclear ribosomal DNA reveals species polyphyly, divergent paralogues and incongruence with chloroplast DNA. Austral Syst Bot 31:16–47CrossRefGoogle Scholar
  6. Bayly MJ, Holmes GD, Forster PI, Cantrill DJ, Ladiges PY (2013) Major clades of Australian Rutoideae (Rutaceae) based on rbcL and atpB sequences. PLoS ONE 8:e72493. CrossRefPubMedCentralGoogle Scholar
  7. Bayly MJ, Duretto MF, Holmes GD, Forster PI, Cantrill DC, Ladiges PY (2015) Transfer of the New Caledonian genus Boronella to Boronia (Rutaceae) based on analyses of cpDNA and nrDNA. Austral Syst Bot 28:111–123CrossRefGoogle Scholar
  8. Boardman R (1986) The history and evolution of South Australia’s forests and woodlands. In: Wallace HR (ed) The ecology of the forests and woodlands of South Australia. Government Printer, Adelaide, pp 16–31Google Scholar
  9. Bowler JM (1980) Quaternary chronology and palaeohydrology in the evolution of mallee landscapes. In: Storrier RR, Stannard MM (eds) Aeolian landscapes in the semi-arid zone of southeastern Australia. Riverina Society of Soil Science, Wagga Wagga, pp 17–36Google Scholar
  10. Bowler JM, Kotsonis A, Lawrence CR (2006) Environmental evolution of the mallee region, western Murray Basin. Proc Roy Soc Victoria 118:161–210Google Scholar
  11. Broadhurst L, Breed M, Lowe A, Bragg J, Catullo R, Coates DJ et al (2017) Genetic diversity and structure of the Australian flora. Divers Distrib 23:41–52CrossRefGoogle Scholar
  12. Byrne M (2008) Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quatern Sci Rev 27:2576–2585CrossRefGoogle Scholar
  13. 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 KH (2008) Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Molec Ecol 17:4398–4417CrossRefGoogle Scholar
  14. Coates DJ, Byrne M, Moritz C (2018) Genetic diversity and conservation unit: dealing with the species-population continuum in the age of genomics. Front Ecol Evol 6:165CrossRefGoogle Scholar
  15. Cupper ML (2005) Last glacial to Holocene evolution of semi-arid rangelands in southeastern Australia. Holocene 15:541–553CrossRefGoogle Scholar
  16. DPIPWE (2012) Zieria veronicea subsp. veronicea. Department of Primary Industries, Parks, Water and Environment, HobartGoogle Scholar
  17. French PA, Brown GK, Bayly MJ (2016) Incongruent patterns of nuclear and chloroplast variation in Correa (Rutaceae): introgression and biogeography in south-eastern Australia. Pl Syst Evol 302:447–468CrossRefGoogle Scholar
  18. Galbraith J (1962) Pink Zieria in Gippsland. Vic Nat 79:175Google Scholar
  19. George AS, Duretto MF, Forster PI (2013) Zieria. Fl Aust 26:282–336Google Scholar
  20. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  21. Hope GS (1978) The late Pleistocene and Holocene vegetational history of Hunter Island, north-western Tasmania. Austral J Bot 26:493–514CrossRefGoogle Scholar
  22. Hope GS (1994) Quaternary vegetation. In: Hill RS (ed) History of the Australian vegetation: cretaceous to recent. Cambridge University Press, Cambridge, pp 368–389Google Scholar
  23. Jackson HD, Steane DA, Potts BM, Vaillancourt RE (1999) Chloroplast DNA evidence for reticulate evolution in Eucalyptus (Myrtaceae). Molec Ecol 8:739–751CrossRefGoogle Scholar
  24. King RA, Leys R (2014) Molecular evidence for mid-Pleistocene divergence of populations of three freshwater amphipod species (Talitroidea: Chiltoniidae) on Kangaroo Island, South Australia, with a new spring-associated genus and species. Austral J Zool 62:137–156CrossRefGoogle Scholar
  25. Kotsonis A (1999) Tertiary shorelines of the western Murray Basin: weathering, sedimentology and exploration potential. In: Stewart R (ed) Murray basin mineral sands conference, vol 26. Australian Institute of Geoscientists Bulletin, Mildura, pp 57–63Google Scholar
  26. Ladiges PY, Gray AM, Brooker MIH (1981) Pattern of geographic variation, based on seedling morphology, in Eucalyptus ovata Labill. and E. brookerana A.M. Gray and comparisons with some other Eucalyptus species. Austral J Bot 29:593–603CrossRefGoogle Scholar
  27. Lambeck K, Chappell J (2001) Sea level change through the last glacial cycle. Science 292:679–686CrossRefGoogle Scholar
  28. Larcombe MJ, McKinnon GE, Vaillancourt RE (2011) Genetic evidence for the origins of range disjunctions in the Australian dry sclerophyll plant Hardenbergia violacea. J Biogeogr 38:125–136CrossRefGoogle Scholar
  29. Lawrence CR (1966) Cainozoic stratigraphy and structure of the mallee region, Victoria. Proc Roy Soc Victoria 79:517–554Google Scholar
  30. Marginson J, Ladiges PY (1988) Geographical variation in Eucalyptus baxteri s.l. and the recognition of a new species, E. arenacea. Austral Syst Bot 1:151–170CrossRefGoogle Scholar
  31. McIntosh PD, Eberhard R, Slee A, Moss P, Price DM, Donaldson P, Doyle R, Martins J (2012) Late quaternary extraglacial cold-climate deposits in low and mid-altitude Tasmania and their climatic implications. Geomorphology 179:21–39CrossRefGoogle Scholar
  32. Mee JA, Bernatchez L, Reist JD, Rogers SM, Taylor EB (2015) Identifying designatable units for intraspecific conservation prioritization: a hierarchical approach applied to the lake whitefish species complex (Coregonus spp.). Evol Appl 8:423–441CrossRefPubMedCentralGoogle Scholar
  33. Merow C, Smith MJ, Silander JA (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36:1058–1069CrossRefGoogle Scholar
  34. Meudt HM, Clarke AC (2007) Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends Plant Sci 12:106–117CrossRefGoogle Scholar
  35. Millner ML, Rossetto M, Crisp MD, Weston PH (2012) The impact of multiple biogeographic barriers and hybridization on species-level differentiation. Amer J Bot 99:2045–2057CrossRefGoogle Scholar
  36. Moritz C (1994) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9:373–375CrossRefGoogle Scholar
  37. Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254CrossRefGoogle Scholar
  38. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273CrossRefGoogle Scholar
  39. Nelson EC (1981) Phytogeography of southern Australia. In: Keast A (ed) Ecological biogeography of Australia. Dr. W. Junk, The Hague, pp 735–757Google Scholar
  40. Nevill PG, Bossinger G, Ades PK (2010) Phylogeography of the world’s tallest angiosperm, Eucalyptus regnans: evidence for multiple isolated Quaternary refugia. J Biogeogr 37:179–192CrossRefGoogle Scholar
  41. Nevill PG, Despres T, Bayly MJ, Bossinger G, Ades PK (2014) Shared phylogeographic patterns and widespread chloroplast haplotype sharing in Eucalyptus species with different ecological tolerances. Tree Genet and Genomes 10:1079–1092CrossRefGoogle Scholar
  42. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, UppsalaGoogle Scholar
  43. Palsbøll PJ, Berube M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–6CrossRefGoogle Scholar
  44. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molec Ecol Notes 6:288–295CrossRefGoogle Scholar
  45. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedCentralGoogle Scholar
  46. Phillips S, Anderson R, Schapire R (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190:231–259CrossRefGoogle Scholar
  47. Phillips SJ, Dudík M, Schapire RE (2018) Maxent software for modeling species niches and distributions (Version 3.4.1).
  48. Radosavljevic A, Anderson RP, Araújo M (2014) Making better Maxent models of species distributions: complexity, overfitting and evaluation. J Biogeogr 41:629–643CrossRefGoogle Scholar
  49. Rambaut A (2002) Sequence alignment editor (version 2.0). Oxford University.
  50. Rambaut A, Drummond AJ (2009) Tracer, version 1.5, MCMC trace analysis package.
  51. Rathbone DA, McKinnon GE, Potts BM, Steane DA, Vaillancourt RE (2007) Microsatellite and cpDNA variation in island and mainland populations of a regionally rare eucalypt, Eucalyptus perriniana (Myrtaceae). Austral J Bot 55:513–520CrossRefGoogle Scholar
  52. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  53. Sgrò CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337CrossRefGoogle Scholar
  54. Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller JT, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Amer J Bot 92:142–166CrossRefGoogle Scholar
  55. Shaw J, Lickey E, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Amer J Bot 94:275–288CrossRefGoogle Scholar
  56. Shepherd L, McLay T (2011) Two micro-scale protocols for the isolation of DNA from polysaccharide-rich plant tissue. J Pl Res 124:311–314CrossRefGoogle Scholar
  57. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381CrossRefGoogle Scholar
  58. Swofford DL (2002) PAUP* 4.0b10: phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
  59. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109CrossRefGoogle Scholar
  60. Thomas I, Enright NJ, Kenyon CE (2001) The Holocene history of mediterranean-type plant communities, Little Desert National Park, Victoria, Australia. Holocene 11:691–697CrossRefGoogle Scholar
  61. Webb JA (1991) Geological history of Victoria. In: Cochrane GW, Quick GW, Spencer-Jones D (eds) Introducing Victorian geology. Geological Society of Australia (Victorian Division), Melbourne, pp 97–168Google Scholar
  62. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfrand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  63. Williams KJ, Ferrier S, Rosauer D, Yeates D, Manion G, Harwood T, Stein J, Faith DP, Laity T, Whalen A (2010) Harnessing continent-wide biodiversity datasets for prioritising national conservation investment. A report prepared for the Department of Sustainability, Environment, Water, Population and Communities. CSIRO Ecosystem Sciences, CanberraGoogle Scholar
  64. Worth JRP, Jordan GJ, McKinnon GE, Vaillancourt RE (2009) The major Australian cool temperate rainforest tree Nothofagus cunninghamii withstood Pleistocene glacial aridity within multiple regions: evidence from the chloroplast. New Phytol 182:519–532CrossRefGoogle Scholar
  65. Worth JRP, Jordan GJ, Marthick JR, McKinnon GE, Vaillancourt RE (2010) Chloroplast evidence for geographic stasis of the Australian bird-dispersed shrub Tasmannia lanceolata (Winteraceae). Molec Ecol 19:2949–2963CrossRefGoogle Scholar
  66. Worth JRP, Marthick JR, Jordan GJ, Vaillancourt RE (2011) Low but structured chloroplast diversity in Atherosperma moschatum (Atherospermataceae) suggests bottlenecks in response to the Pleistocene glacials. Ann Bot (Oxford) 108:1247–1256CrossRefGoogle Scholar
  67. Worth JRP, Williamson GJ, Sakaguchi S, Nevill PG, Jordan GJ (2014) Environmental niche modelling fails to predict Last Glacial Maximum refugia: niche shifts, microrefugia or incorrect palaeoclimate estimates? Glob Ecol Biogeogr 23:1186–1197CrossRefGoogle Scholar
  68. Worth JRP, Holland BR, Beeton NJ, Schönfeld B, Rossetto M, Vaillancourt RE, Jordan GJ (2017) Habitat type and dispersal mode underlie the capacity for plant migration across an intermittent seaway. Ann Bot (Oxford) 120:539–549CrossRefGoogle Scholar
  69. Wright S, Yong CG, Wichman SR, Dawson JW, Gardner RC (2001) Stepping stones to Hawaii: a trans-equatorial dispersal pathway for Metrosideros (Myrtaceae) inferred from nrDNA (ITS + ETS). J Biogeogr 28:769–774CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of BioSciencesThe University of MelbourneParkvilleAustralia
  2. 2.Royal Botanic Gardens VictoriaMelbourneAustralia

Personalised recommendations