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.
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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
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
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
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
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
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
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
Byers DL, Meagher TR (1992) Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68:353–359
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
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
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
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
Eckert CG (2002) The loss of sex in clonal plants. Evol Ecol 15:501–520. doi:10.1023/A:1016005519651
England PR, Ayre DJ, Whelan RJ (1999) Microsatellites in the Australian shrub Grevillea macleayana (Proteaceae). Mol Ecol Notes 8:689–690
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
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
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
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. University of Cambridge, Cambridge
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752
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
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
Goudet J (1995) FSTAT version 1.2: a computer program to calculate F statistics. J Hered 86:485–486
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
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
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
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
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
Jackson RC (1973) Chromosome evolution in Haplopappus gracilis: a centric transposition race. Evol Int J Org Evol 27:243–256. doi:10.2307/2406964
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
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
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
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
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
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
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
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
Majer JD, Lamont BB (1985) Removal of seed of Grevillea pteridifolia (Proteaceae) by ants. Aust J Bot 33:611–618. doi:10.1071/BT9850611
Makinson RO (2000) Grevillea, flora of Australia. 17A ABRS/CSIRO Australia, Melbourne
McGillivray DJ, Makinson RO (1993) Grevillea; Proteaceae. A taxonomic revision. Melbourne University Press, Carlton
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
Moritz C (1994) Defining ‘Evolutionarily Significant Units’ for conservation. Trends Ecol Evol 9:373–375. doi:10.1016/0169-5347(94)90057-4
Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254. doi:10.1080/10635150252899752
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
Olde PM, Marriott NR (1994) The Grevillea book, vol 1. Timber Press, Portland, Oregon
Olde PM, Marriott NR (1995) The Grevillea book, vol 3. Timber Press, Portland, Oregon
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
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
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
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
Ramsay HP (1963) Chromosome numbers in the Proteaceae. Aust J Bot 11:1–20. doi:10.1071/BT9630001
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
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
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
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
Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman and Company, New York
Stace HM, Douglas AW, Sampson JF (1998) Did ‘paleo-polyploidy’ really occur in Proteaceae? Aust Syst Bot 11:613–629. doi:10.1071/SB98013
Stebbins GL (1985) Polyploidy, hybridization, and the invasion of new habitats. Ann Mo Bot Gard 72:824–832. doi:10.2307/2399224
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
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
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
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
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
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
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
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
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
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
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
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.
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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
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DOI: https://doi.org/10.1007/s10592-008-9643-9