Abstract
European calcareous grasslands have decreased dramatically in area and number during the last two centuries. As a result, many populations of calcareous grassland species are confined to small and isolated fragments, where their long-term survival is to some extent uncertain. Recently, several restoration projects have been initiated to enlarge the current grassland area in order to maintain the exceptionally high species richness. However, from a genetic point of view, the success of these restoration measures is not necessarily guaranteed, as strong historical decreases in population size and limited gene flow may have led to low genetic diversity through genetic bottlenecks and drift. In this study, we investigated genetic diversity and structure of 16 populations of the calcareous grassland specialist Cirsium acaule in a severely fragmented landscape in south-western Belgium. The overall distribution of this species in the study area was significantly and positively related to patch area, suggesting that small patches do not allow survival of this species. Both allelic richness and genetic diversity were significantly and positively related to population size. Estimation of observed and expected gene diversity provided evidence for population bottlenecks in the history of not less than 31% of all sampled populations. Reconstruction of the historical land use showed that patch area decline in populations that went through a recent bottleneck was significantly larger than that in populations that showed no evidence of a bottleneck. Assignment analyses showed low migration rates, suggesting that replenishment of lost alleles through gene flow is highly unlikely. Overall, our results indicate that in the absence of gene flow strong decreases in calcareous grassland area may have long-lasting effects on genetic diversity of plant populations and may hamper the success of restoration projects that simply aim at restoring initial habitat conditions or enlarging population fragments, as indicated by the fact that none of the recently restored areas has been occupied by C. acaule.
Similar content being viewed by others
References
Adriaens D (2008) Spatio-temporal patterns of calcareous grassland fragmentation and consequences for plant species and communities. PhD dissertation, Catholic University Leuven
Adriaens D, Honnay O, Hermy M (2006) No evidence of a plant extinction debt in highly fragmented calcareous grasslands in Belgium. Biol Cons 133:212–224. doi:10.1016/jbiocon200606006
Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol l17:5177–5188. doi:10.1111/j1365-294X200803971x
Brown JH, Kodrick-Brown A (1977) Turnover rates in insular biogeography effect of migration on extinction. Ecology 58:445–449
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Verlag, New York
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Couvet D (2002) Deleterious effects of restricted gene flow in fragmented populations. Cons Biol 16:369–376
Cozzolino S, Noce ME, Musacchio A, Widmer A (2003) Variation at a chloroplast minisatellite locus reveals the signature of habitat fragmentation and genetic bottlenecks in the rare orchid Anacamptis palustris (Orchidaceae). Am J Bot 90:1681–1687
De Vere N, Jongejans E, Plowman A, Williams E (2009) Population size and habitat quality affect genetic diversity and fitness in the clonal herb Cirsium dissectum. Oecologia 159:59–68. doi:10.1007/s00442-008-1203-y
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Nat Ac Sci USA 91:3166–3170
Ellstrand RM, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Syst 24:217–242
Fischer SF, Poschlod P, Beinlich B (1996) Experimental studies on the dispersal of plants and animals on sheep in calcareous grasslands. J Appl Ecol 33:1206–1222
Goudet J (1995) FSTAT (Version 12): a computer program to calculate F-statistics. J Her 86:485–486
Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford UK
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
Honnay O, Jacquemyn H (2007) Susceptibility of rare and common plant species to the genetic consequences of habitat fragmentation. Cons Biol 21:824–831
Honnay O, Coart E, Butaye J, Adriaens D, Van Glabeke S, Roldán-Ruiz I (2006) Low impact of present and historical landscape configuration on the genetics of fragmented Anthyllis vulneraria populations. Biol Cons 127:411–419. doi:10.1016/j.biocon.2005.09.006
Honnay O, Adriaens D, Coart E, Jacquemyn H, Roldán-Ruiz I (2007) Genetic diversity within and between remnant populations of the endangered calcareous grassland plant Globularia bisnagarica L. Cons Gen 8:293–303. doi:10.1007/s10592-006-9169-y
Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the genetic distribution of genetic variability. Evolution 53:1898–1914
Jacquemyn H, Brys R, Hermy M (2003) Short-term effects of different management regimes on the response of calcareous grassland vegetation to increased nitrogen. Biol Cons 111:137–147
Jump AS, Dawson DA, James CM, Woodward FI, Burke T (2002) Isolation of polymorphic microsatellites in the stemless thistle (Cirsium acaule) and their utility in other Cirsium species. Mol Ecol Notes 2:589–592
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Keymer RJ, Leach SJ (1990) Calcareous grassland—a limited resource in Britain. In: Hillier SW, Walton DHW, Wells DA (eds) Calcareous grasslands: ecology and management. Bluntisham Books, Bluntisham, UK, pp 11–17
Kull T, Zobel M (1991) High species richness in an Estonian wooded meadow. J Veg Sci 2:711–714
Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460
Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size fitness and genetic variation? J Ecol 94:942–952. doi:10.1111/j.1365-2745.2006.01150.x
Mccoy ED, Mushinsky HR (2007) Estimates of minimum patch size depend on the method of estimation and the condition of the habitat. Ecology 6:1401–1407
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Ouborg NJ, Piquot Y, van Groenendael JM (1999) Population genetics, molecular markers and the study of dispersal in plants. J Ecol 87:551–568
Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65. doi:10.1046/j.1365-294X.2003.02008.x
Pigott CD (1968) Biological flora of the British Isles: Cirsium acaulon (L) scop. J Ecol 56:597–612
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
Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software program for genetic assignment and first-generation migrant detection. J Hered 95:536–539. doi:10.1093/jhered/esh074
Poschlod P, Wallis-DeVries MF (2002) The historical and socio-economic perspective of calcareous grasslands–lessons from the distant and recent past. Biol Cons 104:361–376
Poschlod P, Kiefer S, Trankle U, Fischer S, Bonn S (1998) Plant species richness in calcareous grasslands as affected by dispersability in space and time. Appl Veg Sci 1:75–90
Raymond M, Rousset F (1995) GENEPOP version 12 population genetics software for exact tests and ecumenism. J Hered 86:248–249
Schaal BA, Leverich WJ (1996) Molecular variation in isolated plant populations. Plant Spec Biol 11:33–40
Sork VL, Smouse PE (2006) Genetic analysis of landscape connectivity in tree populations. Landscape Ecol 21:821–836. doi:10.1007/s10980-005-5415-9
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Willems JH (2001) Problems approaches and results in restoration of Dutch calcareous grassland during the last 30 years. Restor Ecol 9:147–154
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
Acknowledgments
This research was funded by the Flemish Fund for Scientific Research (FWO—Flanders). We would like to thank Nadja Balis, Katrien Vandepitte, Tim De Meyer and Sabine Van Glabbeke for DNA extraction, microsatellite analysis and simulation. One anonymous reviewer and the Associate Editor provided useful comments on a previous version of this ms. Dries Adriaens kindly supplied a map of the study area.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jacquemyn, H., Roldán-Ruiz, I. & Honnay, O. Evidence for demographic bottlenecks and limited gene flow leading to low genetic diversity in a rare thistle. Conserv Genet 11, 1979–1987 (2010). https://doi.org/10.1007/s10592-010-0089-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-010-0089-5