Skip to main content

Advertisement

SpringerLink
Log in

Divergent levels of genetic variation and ploidy among populations of the rare shrub, Grevillea repens (Proteaceae)

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Rare plant species are often restricted to small and/or isolated populations that can have reduced reproductive output and adaptive potential, resulting in an increased probability of extinction. Nevertheless, evolutionary changes might occur in such populations that increase their likelihood of persisting. In Australia, many threatened species from the ecologically important genus Grevillea (Proteaceae) are found in disjunct populations and these often display varied modes of reproduction from sexual to exclusively clonal. Here we use microsatellite markers to show that isolated populations across the entire range of G. repens have developed diverse patterns of genetic variation. The largest population has a relatively low level of genetic variation, one small population displays inbreeding, two populations show evidence of clonal reproduction and two contain both triploids and diploids. The global estimate of F ST was moderately high (0.272) suggesting limited gene flow between populations and historical isolation. These findings indicate that the genetically distinct G. repens populations exhibit very different patterns of genetic variation and we propose that the development of clonality and polyploidy in small or isolated populations may allow persistence but also reduces the effective size of the sexual population. Grevillea repens populations from its eastern and western/western central centres of distribution should be viewed as separate units for conservation management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbott RJ, Ireland HE, Rogers HJ (2007) Population decline despite high genetic diversity in the new allopolyploid species Senecio cambrensis (Asteraceae). Mol Ecol 16:1023–1033. doi:10.1111/j.1365-294X.2007.03169.x

    Article  PubMed  CAS  Google Scholar 

  • Auld TD, Denham AJ (1999) The role of ants and mammals in dispersal and post-dispersal seed predation of the shrubs Grevillea (Proteaceae). Plant Ecol 144:201–213. doi:10.1023/A:1009817132378

    Article  Google Scholar 

  • Barrett SCH, Kohn JR (1991) Genetic and evolutionary consequences of small population size in plants: Implications for conservation. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 3–30

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L et al (2004) GENETIX 4.03, logiciel sous Windows pour la génétique des populations. Laboratoire Génome et Populations, Intereactions, CNRS UMR 5000. Université de Montpellier II, Montpellier, France

    Google Scholar 

  • Beyer HL (2004) Hawth’s analysis tools for ArcGIS. Available at http://www.spatialecology.com/htools

  • Briggs JD, Leigh JH (1996) Rare or threatened Australian plants. CSIRO Publishing, Collingwood

    Google Scholar 

  • Burne HM, Yates CJ, Ladd PG (2003) Comparative population structure and reproductive biology of the critically endangered shrub Grevillea althoferorum and two closely related more common congeners. Biol Conserv 114:53–65. doi:10.1016/S0006-3207(02)00420-2

    Article  Google Scholar 

  • Busch JW (2005) The evolution of self-compatibility in geographically peripheral populations of Leavenworthia alabamica (Brassicaceae). Am J Bot 92:1503–1512. doi:10.3732/ajb.92.9.1503

    Article  Google Scholar 

  • Byers DL, Meagher TR (1992) Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68:353–359

    Google Scholar 

  • Caddy HAR, Gross CL (2006) Population structure and fecundity in the putative sterile shrub, Grevillea rhizomatosa Olde & Marriott (Proteaceae). Proc Linn Soc N S W 127:11–18

    Google Scholar 

  • Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM et al (2000) Considering evolutionary processes in conservation biology: an alternative to ‘evolutionarily significant units’. Trends Ecol Evol 15:290–295. doi:10.1016/S0169-5347(00)01876-0

    Article  PubMed  Google Scholar 

  • Dorken ME, Neville KJ, Eckert CG (2004) Evolutionary vestigialization of sex in a clonal plant: selection versus neutral mutation in geographically peripheral populations. Proc R Soc Biol Sci Ser B 271:2375–2380. doi:10.1098/rspb.2004.2875

    Article  Google Scholar 

  • Eckert CG (2002) The loss of sex in clonal plants. Evol Ecol 15:501–520. doi:10.1023/A:1016005519651

    Article  Google Scholar 

  • England PR, Ayre DJ, Whelan RJ (1999) Microsatellites in the Australian shrub Grevillea macleayana (Proteaceae). Mol Ecol Notes 8:689–690

    CAS  Google Scholar 

  • England PR, Usher AV, Whelan RJ et al (2002) Microsatellite diversity and genetic structure of fragmented populations of the rare, fire-dependent shrub Grevillea macleayana. Mol Ecol 11:967–977. doi:10.1046/j.1365-294X.2002.01500.x

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Fausto JA Jr, Eckhart VM, Geber MA (2001) Reproductive assurance and the evolutionary ecology of self-pollination in Clarkia xantiana (Onagraceae). Am J Bot 88:1794–1800. doi:10.2307/3558355

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. University of Cambridge, Cambridge

    Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    PubMed  CAS  Google Scholar 

  • Gaston KJ, Kunin WE (1997) Rare-common differences: an overview. In: Kunin WE, Gaston KJ (eds) The biology of rarity: causes and consequences of rare-common differences. Chapman & Hall, London, pp 12–29

    Google Scholar 

  • Gill MA, Bradstock RA, Williams JE (2002) Fire regimes and biodiversity: legacy and vision. In: Bradstock RA et al (eds) Flammable Australia: the fire regimes and biodiversity of a continent. Cambridge University Press, Cambridge

    Google Scholar 

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

    Google Scholar 

  • Gross CL, Caddy HAR (2006) Are differences in breeding mechanisms and fertility among populations contributing to rarity in Grevillea rhizomatosa (Proteaceae)? Am J Bot 93:1791–1799. doi:10.3732/ajb.93.12.1791

    Article  Google Scholar 

  • Harper JL (1981) The meanings of rarity. In: Synge H (ed) The biological aspects of rare plant conservation. John Wiley & Sons Ltd, Chichester, pp 205–217

    Google Scholar 

  • Hoebee SE (2002) Conservation genetics of the endangered shrub Grevillea iaspicula McGill. (Proteaceae). PhD Thesis, The Australian National University, Canberra

  • Hoebee SE, Menn C, Rotach P et al (2006) Spatial genetic structure of Sorbus torminalis: the extent of clonal reproduction in natural stands of a rare tree species with a scattered distribution. For Ecol Manag 226:1–8

    Article  Google Scholar 

  • Holsinger KE, Gottlieb LD (1991) Conservation of rare and endangered plants: principles and prospects. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 195–208

    Google Scholar 

  • Husband BC (2004) The role of triploid hybrids in the evolutionary dynamics of mixed-ploidy populations. Biol J Linn Soc 82:537–546. doi:10.1111/j.1095-8312.2004.00339.x

    Article  Google Scholar 

  • Jackson RC (1973) Chromosome evolution in Haplopappus gracilis: a centric transposition race. Evol Int J Org Evol 27:243–256. doi:10.2307/2406964

    Google Scholar 

  • Kapralov MV, Gabrielsen TM, Sarapultsev IE et al (2006) Genetic enrichment of the arctic clonal plant Saxifraga cernua at its southern periphery via the alpine sexual Saxifraga sibirica. Mol Ecol 15:3401–3411. doi:10.1111/j.1365-294X.2006.03024.x

    Article  PubMed  CAS  Google Scholar 

  • Kimpton SK, James EA, Drinnan AN (2002) Reproductive biology and genetic marker diversity in Grevillea infecunda (Proteaceae), a rare plant with no known seed production. Aust Syst Bot 15:485–492. doi:10.1071/SB01029

    Article  Google Scholar 

  • Lamont BB, Barrett GJ (1988) Constraints on seed production and storage in a root-suckering Banksia. J Ecol 76:1069–1082. doi:10.2307/2260634

    Article  Google Scholar 

  • Landergott U, Holderegger R, Kozlowski G et al (2001) Historical bottlenecks decrease genetic diversity in natural populations of Dryopteris cristata. Heredity 87:344–355. doi:10.1046/j.1365-2540.2001.00912.x

    Article  PubMed  CAS  Google Scholar 

  • Llorens TM (2004) Conservation genetics and ecology of two rare Grevillea species. PhD Thesis, University of Wollongong, Wollongong

  • Llorens TM, Ayre DJ, Whelan RJ (2004) Evidence for ancient genetic subdivision among recently fragmented populations of the endangered shrub Grevillea caleyi (Proteaceae). Heredity 92:519–526. doi:10.1038/sj.hdy.6800444

    Article  PubMed  CAS  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet J-M et al (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247. doi:10.1093/jhered/89.3.238

    Article  PubMed  CAS  Google Scholar 

  • Lynch AJJ, Barnes RW, Cambecèdes J et al (1998) Genetic evidence that Lomatia tasmanica (Proteaceae) is an ancient clone. Aust J Bot 46:25–33. doi:10.1071/BT96120

    Article  Google Scholar 

  • Mahy G, Bruederle LP, Connors B et al (2000) Allozyme evidence for genetic autopolyploidy and high genetic diversity in tetraploid cranberry, Vaccinium oxycoccos (Ericaceae). Am J Bot 87:1882–1889. doi:10.2307/2656840

    Article  PubMed  CAS  Google Scholar 

  • Majer JD, Lamont BB (1985) Removal of seed of Grevillea pteridifolia (Proteaceae) by ants. Aust J Bot 33:611–618. doi:10.1071/BT9850611

    Article  Google Scholar 

  • Makinson RO (2000) Grevillea, flora of Australia. 17A ABRS/CSIRO Australia, Melbourne

    Google Scholar 

  • McGillivray DJ, Makinson RO (1993) Grevillea; Proteaceae. A taxonomic revision. Melbourne University Press, Carlton

    Google Scholar 

  • McKinney ML (1997) How do rare species avoid extinction? A paleontological view. In: Kunin WE, Gaston KJ (eds) The biology of rarity: causes and consequences of rare-common differences. Chapman & Hall, London, pp 110–129

    Google Scholar 

  • Moritz C (1994) Defining ‘Evolutionarily Significant Units’ for conservation. Trends Ecol Evol 9:373–375. doi:10.1016/0169-5347(94)90057-4

    Article  Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254. doi:10.1080/10635150252899752

    Article  PubMed  Google Scholar 

  • Murray BG, Young AG (2001) Widespread chromosome variation in the endangered grassland forb Rutidosis leptorrhynchoides F. Muell. (Asteraceae: Gnaphalieae). Ann Bot (Lond) 87:83–90. doi:10.1006/anbo.2000.1307

    Article  Google Scholar 

  • Olde PM, Marriott NR (1994) The Grevillea book, vol 1. Timber Press, Portland, Oregon

    Google Scholar 

  • Olde PM, Marriott NR (1995) The Grevillea book, vol 3. Timber Press, Portland, Oregon

    Google Scholar 

  • Parks JC, Werth CR (1993) A study of spatial features of clones in a population of bracken fern, Pteridium aqulinum (Dennstaedtiaceae). Am J Bot 80:537–544. doi:10.2307/2445369

    Article  Google Scholar 

  • Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. doi:10.1093/jhered/90.4.502

    Article  Google Scholar 

  • Rabanowitz D (1981) Seven forms of rarity. In: Synge H (ed) The biological aspects of rare plant conservation. John Wiley & Sons Ltd, Chichester, pp 205–217

    Google Scholar 

  • Ramsay HP (1963) Chromosome numbers in the Proteaceae. Aust J Bot 11:1–20. doi:10.1071/BT9630001

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rossetto M, Weaver PK, Dixon KW (1995) Use of RAPD analysis in devising conservation strategies for the rare and endangered Grevillea scapigera (Proteaceae). Mol Ecol 4:321–329. doi:10.1111/j.1365-294X.1995.tb00225.x

    Article  PubMed  CAS  Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10. doi:10.1016/0169-5347(86)90059-5

    Article  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573. doi:10.1038/sj.hdy.6885180

    Article  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman and Company, New York

    Google Scholar 

  • Stace HM, Douglas AW, Sampson JF (1998) Did ‘paleo-polyploidy’ really occur in Proteaceae? Aust Syst Bot 11:613–629. doi:10.1071/SB98013

    Article  Google Scholar 

  • Stebbins GL (1985) Polyploidy, hybridization, and the invasion of new habitats. Ann Mo Bot Gard 72:824–832. doi:10.2307/2399224

    Article  Google Scholar 

  • Thompson JD (1999) Population differentiation in Mediterranean plants: insights into colonization history and the evolution and conservation of endemic species. Heredity 82:229–236. doi:10.1038/sj.hdy.6885040

    Article  PubMed  Google Scholar 

  • Thórsson ÆT, Pálsson S, Sigurgeirsson A et al (2007) Morphological variation among Betula nana (diploid), B. pubescens (tetraploid) and their triploid hybrids in Iceland. Ann Bot (Lond) 99:1183–1193. doi:10.1093/aob/mcm060

    Article  Google Scholar 

  • Vallejo-Marín M, O’Brien HE (2007) Correlated evolution of self-incompatibility and clonal reproduction in Solanum (Solanaceae). New Phytol 173:415–421. doi:10.1111/j.1469-8137.2006.01924.x

    Article  PubMed  Google Scholar 

  • van Kleunen M, Fischer M, Johnson SD (2007) Reproductive assurance through self-fertilization does not vary with population size in the alien invasive plant Datura stramonium. Oikos 116:1400–1412. doi:10.1111/j.0030-1299.2007.16004.x

    Article  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935. doi:10.1046/j.1365-294X.2004.02076.x

    Article  PubMed  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F statistics for the analysis of population structure. Evolution Int J Org Evolution 38:1358–1370. doi:10.2307/2408641

    Google Scholar 

  • Whelan RJ (2002) Managing fire regimes for conservation and property protection: an Australian response. Conserv Biol 16:1659–1661. doi:10.1046/j.1523-1739.2002.02091.x

    Article  Google Scholar 

  • Whelan RJ, Rodgerson L, Dickman CR et al (2002) Critical life cycles of plants and animals: developing a process-based understanding of population changes in fire-prone landscapes. In: Bradstock RA et al (eds) Flammable Australia: the fire regimes and biodiversity of a continent. Cambridge University Press, Cambridge, pp 94–123

    Google Scholar 

  • Wilcock CC, Jennings SB (1999) Partner limitation and restoration of sexual reproduction in the clonal dwarf shrub Linnaea borealis L. (Caprifoliaceae). Protoplasma 208:76–86. doi:10.1007/BF01279077

    Article  Google Scholar 

  • Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458. doi:10.1146/annurev.ecolsys.37.091305.110145

    Article  Google Scholar 

  • Young AG, Brown AHD, Murray BG et al (2000) Genetic erosion, restricted mating and reduced viability in fragmented populations of the endangered grassland herb Rutidosis leptorrhynchoides. In: Young AG, Clarke GM (eds) Genetics demography and viability of fragmented populations. Cambridge University Press, Cambridge, pp 335–359

    Google Scholar 

Download references

Acknowledgements

We thank the staff from Parks Victoria and DSE for collection permits and access to sites, Brian Murray and Claire Marks for assistance with cytological work, nursery staff at RBGM, and Mark Blacket, Paul Mitrovski, Phillip England and Susan Hoebee for advice during the microsatellite study. Thanks to Michael Kearney for mapping assistance, Yvonne Parsons for help during the initial project stages and Mark Blacket, Margaret Byrne and an anonymous reviewer for commenting on the manuscript. This research was funded by the Cybec Foundation, Royal Botanic Gardens Melbourne and the Centre for Environmental Stress and Adaptation Research and undertaken under DSE permits 10003055 and 05/1/09/11/06.

Author information

Authors and Affiliations

  1. Centre for Environmental Stress and Adaptation Research (CESAR) Hoffmann Laboratory, Level 2, Bio21 Institute, University of Melbourne, 30 Flemington Rd, Parkville, VIC, 3010, Australia

    Gareth D. Holmes & Ary A. Hoffmann

  2. Royal Botanic Gardens Melbourne, Private Bag 2000, Birdwood Ave, South Yarra, VIC, 3141, Australia

    Elizabeth A. James

Authors
  1. Gareth D. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elizabeth A. James
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ary A. Hoffmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gareth D. Holmes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holmes, G.D., James, E.A. & Hoffmann, A.A. Divergent levels of genetic variation and ploidy among populations of the rare shrub, Grevillea repens (Proteaceae). Conserv Genet 10, 827–837 (2009). https://doi.org/10.1007/s10592-008-9643-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-008-9643-9

Keywords

Search

Navigation