Contrasting levels of connectivity and localised persistence characterise the latitudinal distribution of a wind-dispersed rainforest canopy tree

Abstract

Contrasting signals of genetic divergence due to historic and contemporary gene flow were inferred for Coachwood, Ceratopetalum apetalum (Cunoniaceae), a wind-dispersed canopy tree endemic to eastern Australian warm temperate rainforest. Analysis of nine nuclear microsatellites across 22 localities revealed two clusters between northern and southern regions and with vicariance centred on the wide Hunter River Valley. Within populations diversity was high indicating a relatively high level of pollen dispersal among populations. Genetic variation was correlated to differences in regional biogeography and ecology corresponding to IBRA regions, primary factors being soil type and rainfall. Eleven haplotypes were identified by chloroplast microsatellite analysis from the same 22 localities. A lack of chloroplast diversity within sites demonstrates limited gene flow via seed dispersal. Network representation indicated regional sharing of haplotypes indicative of multiple Pleistocene refugia as well as deep divergences between regional elements of present populations. Chloroplast differentiation between sites in the upper and lower sections of the northern population is reflective of historic vicariance at the Clarence River Corridor. There was no simple vicariance explanation for the distribution of the divergent southern chlorotype, but its distribution may be explained by the effects of drift from a larger initial gene pool. Both the Hunter and Clarence River Valleys represent significant dry breaks within the species range, consistent with this species being rainfall dependent rather than cold-adapted.

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References

  1. Adam P (1992) Australian rainforests. Oxford University Press, Oxford

    Google Scholar 

  2. Angelone S, Hilfiker K, Holderegger R, Bergamini A, Hoebee SE (2007) Regional population dynamics define the local genetic structure in Sorbus torminalis. Mol Ecol 16:1291–1301

    CAS  PubMed  Article  Google Scholar 

  3. Barnes RW, Hill RS (1999) Ceratopetalum fruits from Australian Cainozoic sediments and their significance for petal evolution in the genus. Aust Syst Bot 12:635–645

    Article  Google Scholar 

  4. Baur GN (1957) Nature and distribution of rainforests in New South Wales. Aust J Bot 5:190–233

    Article  Google Scholar 

  5. Black MP, Mooney SD, Martin HA (2006) A>43000-year vegetation and fire history from Lake Baraba, New South Wales, Australia. Quat Sci Rev 25:3003–3016

    Article  Google Scholar 

  6. Bond WJ, Midgley JJ (2001) Ecology of sprouting in woody plants: the persistence niche. Trends Ecol Evol 16:45–51

    PubMed  Article  Google Scholar 

  7. Bowman DMJS (2000) Australian rainforests—Islands of green in a land of fire. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  8. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557

    PubMed  Article  Google Scholar 

  9. Di Virgilio G, Laffan SW, Ebach MC (2012) Fine-scale quantification of floral and faunal breaks and their geographic correlates, with an example from south-eastern Australia. J Biogeogr 39:1862–1876

    Article  Google Scholar 

  10. Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant-populations. Hered 72:250–259

    Article  Google Scholar 

  11. Evanno G, Roegnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Article  Google Scholar 

  12. Floyd AG (1990) Australian rainforests in New South Wales. Surrey Beatty, Sydney

    Google Scholar 

  13. Ford J (1987) Minor isolates and minor geographical barriers in avian speciation in continental Australia. EMU 87:90–102

    Article  Google Scholar 

  14. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  15. Heslewood MM, Porter C, Avino M, Rossetto M (2009) Isolation and characterization of nuclear microsatellite loci from Ceratopetalum apetalum (Cunoniaceae). Mol Ecol Resour 9:566–568

    PubMed  Article  Google Scholar 

  16. Heuertz M, Fineschi S, Anzidei M et al (2004) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Mol Ecol 13:3437–3452

    CAS  PubMed  Article  Google Scholar 

  17. Heuertz M, Carnevale S, Fineschi S et al (2006) Chloroplast DNA phylogeography of European ashes, Fraxinus sp (Oleaceae): roles of hybridization and life history traits. Mol Ecol 15:2131–2140

    CAS  PubMed  Article  Google Scholar 

  18. Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc B 359:183–195

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. Hilbert DW, Graham A, Hopkins MS (2007) Glacial and interglacial refugia within a long-term rainforest refugium: the wet tropics bioregion of NE Queensland, Australia. Palaeogeogr Palaeoclim Palaeoecol 251:104–118

    Article  Google Scholar 

  20. Hill RS, Truswell EM, McLoughlin S, Dettmann ME (1999) The evolution of the Australian flora: fossil evidence. In: Orchard AE (ed) Flora of Australia, vol 1., IntroductionCSIRO Publishing, Melbourne, pp 251–320

    Google Scholar 

  21. Hoogland RD (1960) Studies in the Cunoniaceae. I. The genera Ceratopetalum, Gillbeea, Aistopetalum, and Calycomis. Aust J Bot 8:318–341

    Article  Google Scholar 

  22. Hoogland RD (1981) Studies in the Cunoniaceae III. Additional notes on Ceratopetalum and Acrophyllum. Brunonia 4:213–216

    Article  Google Scholar 

  23. Hopkins MS, Ash J, Graham AW, Head J, Hewett RK (1993) Charcoal evidence of the spatial extent of the Eucalyptus woodland expansions and rainforest contractions in north Queensland during the late Pleistocene. J Biogeogr 20:357–372

    Article  Google Scholar 

  24. Jordano P (2010) Pollen, seeds and genes: the movement ecology of plants. Hered 105:329–330

    CAS  Article  Google Scholar 

  25. Joseph L, Dolman G, Donnellan S et al (2008) Where and when does a ring start and end? Testing the ring-species hypothesis in a species complex of Australian parrots. Proc Trans R Soc B 275:2431–2440

    Article  Google Scholar 

  26. Jost LOU (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    PubMed  Article  Google Scholar 

  27. Kershaw AP, Bretherton SC, van der Kaars S (2007) A complete pollen record of the last 230 ka from Lynch’s Crater, north-eastem Australia. Palaeogeogr Palaeoclim Palaeoecol 251:23–45

    Article  Google Scholar 

  28. Kooyman R, Rossetto M, Cornwell W, Westoby M (2011) Phylogenetic tests of community assembly across regional to continental scales in tropical and subtropical rain forests. Global Ecol Biogeogr 20:707–716

    Article  Google Scholar 

  29. Magri D, Vendramin GG, Comps B et al (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221

    CAS  PubMed  Article  Google Scholar 

  30. McLoughlin S (2001) The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Aust J Bot 49:271–300

    Article  Google Scholar 

  31. Mellick R, Lowe A, Rossetto M (2011) Consequences of long- and short-term fragmentation on the genetic diversity and differentiation of a late successional rainforest conifer. Aust J Bot 59:351–362

    Article  Google Scholar 

  32. Milner ML, Rossetto M, Crisp MD, Weston PH (2012) The impact of multiple biogeographic barriers and hybridization on species-level differentiation. Am J Bot 99:2045–2057

    PubMed  Article  Google Scholar 

  33. Nicholls JA, Austin JJ (2005) Phylogeography of an east Australian wet-forest bird, the satin bowerbird (Ptilonorhynchus violaceus), derived from mtDNA, and its relationship to morphology. Mol Ecol 14:1485–1496

    CAS  PubMed  Article  Google Scholar 

  34. Oddou-Muratorio S, Petit RJ, Le Guerroue B, Guesnet D, Demesure B (2001) Pollen-versus seed-mediated gene flow in a scattered forest tree species. Evolution 55:1123–1135

    CAS  PubMed  Article  Google Scholar 

  35. Pakkad G, Ueno S, Yoshimaru H (2008) Genetic diversity and differentiation of Quercus semiserrata Roxb. in northern Thailand revealed by nuclear and chloroplast microsatellite markers. For Ecol Manag 255:1067–1077

    Article  Google Scholar 

  36. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  37. Petit RJ, Duminil J, Fineschi S et al (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701

    CAS  PubMed  Article  Google Scholar 

  38. Playford J, Bell JC, Moran GF (1993) A major disjunction in genetic diversity over the geographic range of Acacia melanoxylon R.Br. Aust J Bot 41:355–368

    Article  Google Scholar 

  39. Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  42. Rossetto M, Kooyman RM (2005) The tension between dispersal and persistence regulates the current distribution of rare palaeo-endemic rain forest flora: a case study. J Ecol 93:906–917

    Article  Google Scholar 

  43. Rossetto M, Gross CL, Jones R, Hunter J (2004a) The impact of clonality on an endangered tree (Elaeocarpus williamsianus) in a fragmented rainforest. Biol Conserv 117:33–39

    Article  Google Scholar 

  44. Rossetto M, Jones R, Hunter J (2004b) Genetic effects of rainforest fragmentation in an early successional tree (Elaeocarpus grandis). Hered 93:610–618

    CAS  Article  Google Scholar 

  45. Rossetto M, Crayn D, Ford A, Ridgeway P, Rymer P (2007) The comparative study of range-wide genetic structure across related, co-distributed rainforest trees reveals contrasting evolutionary histories. Aust J Bot 55:416–424

    Article  Google Scholar 

  46. Rossetto M, Kooyman R, Sherwin W, Jones R (2008) Dispersal limitations, rather than bottlenecks or habitat specificity, can restrict the distribution of rare and endemic rainforest trees. Am J Bot 95:321–329

    PubMed  Article  Google Scholar 

  47. Rossetto M, Crayn D, Ford A, Mellick R, Sommerville K (2009) The influence of environment and life-history traits on the distribution of genes and individuals: a comparative study of 11 rainforest trees. Mol Ecol 18:1422–1438

    CAS  PubMed  Article  Google Scholar 

  48. Rossetto M, Allen C, Thurlby K, Weston P, Milner M (2012) Genetic structure and bio-climatic modeling support allopatric over parapatric speciation along a latitudinal gradient. BMC Evol Biol 12:149

    PubMed Central  PubMed  Article  Google Scholar 

  49. Rousset F (2008) GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    PubMed  Article  Google Scholar 

  50. Rozefelds AC, Barnes RW (2002) The systematic and biogeographical relationships of Ceratopetalum (Cunoniaceae) in Australia and New Guinea. Int J Plant Sci 163:651–673

    Article  Google Scholar 

  51. Schodde R, Mason IJ (1997) Psittacidae. In: WWK Houston, Wells A (eds) Aves (Columbidae to Coraciidae). Zoological Catalogue of Australia Vol. 37.2. CSIRO Publishing, Melbourne, pp 109-218. Taylor KJ, Lowe AJ, Hunter RJ et al (2005) Genetic diversity and regional identity in the Australian remnant Nothofagus moorei. Aust J Bot 53:437–444

    Article  Google Scholar 

  52. Tulau MJ (1999) Acid sulfate soil management priority areas in the Lower Clarence floodplain (Report). Department of Land and Water Conservation, Sydney

    Google Scholar 

  53. van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol Ecol Notes 6:255–256

    Article  Google Scholar 

  54. Webb LJ, Tracey JG (1981) Australian rainforests: patterns and change. In: Keast A (ed) Ecological Biogeography of Australia. W. Junk, The Hague, pp 605–694

    Google Scholar 

  55. Weising K, Gardner RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19

    CAS  PubMed  Article  Google Scholar 

  56. Williams NJ, Harle KJ, Gale SJ, Heijnis H (2006) The vegetation history of the last glacial–interglacial cycle in eastern New South Wales. J Quat Sci 21:735–750

    Article  Google Scholar 

  57. 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 182:519–532

    CAS  PubMed  Article  Google Scholar 

  58. 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). Mol Ecol 19:2949–2963

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

We thank Steve Clarke, Maria Cotter, Robert Kooyman, Hannah McPherson, Louisa Murray, Carolyn Connelly, Marlien van der Merwe, Peter Weston and Michael Whitehead for assisting with fieldwork or supplying specimens. We thank Chris Togher, Chris Allen and Rohan Mellick for assistance with the GIS and the map. The project was funded by the Australian Research Council (DP0665859).

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Correspondence to Margaret M. Heslewood.

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Heslewood, M.M., Lowe, A.J., Crayn, D.M. et al. Contrasting levels of connectivity and localised persistence characterise the latitudinal distribution of a wind-dispersed rainforest canopy tree. Genetica 142, 251–264 (2014). https://doi.org/10.1007/s10709-014-9771-8

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Keywords

  • Cunoniaceae
  • Microsatellites
  • Rainforest refugia
  • Vicariance
  • Wind-dispersed tree