Abstract
Parasite populations do not necessarily conform to expected patterns of genetic diversity and structure. Parasitic plants may be more vulnerable to the negative consequences of landscape fragmentation because of their specialized life history strategies and dependence on host plants, which are themselves susceptible to genetic erosion and reduced fitness following habitat change. We used AFLP genetic markers to investigate the effects of habitat fragmentation on genetic diversity and structure within and among populations of hemiparasitic Viscum album. Comparing populations from two landscapes differing in the amount of forest fragmentation allowed us to directly quantify habitat fragmentation effects. Populations from both landscapes exhibited significant isolation-by-distance and sex ratios biased towards females. The less severely fragmented landscape had larger and less isolated populations, resulting in lower levels of population genetic structure (F ST = 0.05 vs. 0.09) and inbreeding (F IS = 0.13 vs. 0.27). Genetic differentiation between host-tree subpopulations was also higher in the more fragmented landscape. We found no significant differences in within-population gene diversity, percentage of polymorphic loci, or molecular variance between the two regions, nor did we find relationships between genetic diversity measures and germination success. Our results indicate that increasing habitat fragmentation negatively affects population genetic structure and levels of inbreeding in V. album, with the degree of isolation among populations exerting a stronger influence than forest patch size.
Similar content being viewed by others
References
Barney CW, Hawksworth FG, Geils BW (1998) Hosts of Viscum album. Eur J For Path 28:187–208
Barrett LG, Thrall PH, Burdon JJ, Linde CC (2008) Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends Ecol Evol 23:678–685
Bialozyt R, Ziegenhagen B, Petit RJ (2006) Contrasting effects of long-distance seed dispersal on genetic diversity during range expansion. J Evol Biol 19:12–20
Bickford CP, Kolb TE, Geils BW (2005) Host physiological condition regulates parasitic plant performance: Arceuthobium vaginatum subsp. cryptopodum on Pinus ponderosa. Oecologia 146:179–189
Bonin A, Bellemain E, Eidesen B, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273
Botanga CJ, Timko MP (2005) Genetic structure and analysis of host and nonhost interactions of Striga gesnerioides (witchweed) from central Florida. Phytopathology 95:1166–1173
Cardoso SRS, Eloy NB, Provan J, Cardoso MA, Ferreira PCG (2000) Genetic differentiation of Euterpe edulis Mart. Populations estimated by AFLP analysis. Mol Ecol 9:1753–1760
Dasmahapatra KK, Lacy RC, Amos W (2008) Estimating levels of inbreeding using AFLP markers. Heredity 100:286–295
Davies DM, Graves JD (1998) Interactions between arbuscular mycorrhizal fungi and the hemiparasitic angiosperm Rhinanthus minor during co-infection of a host. New Phyt 139:555–563
de Vega C, Berjano R, Arista M, Ortiz PL, Talavera S, Stuessy TF (2008) Genetic races associated with the genera and sections of host species in the holoparasitic plant Cytinus (Cytinaceae) in the western Mediterranean basin. New Phtyol 178:875–887
Ellstrand N, Elam D (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242
Gagne G, Roeckel-Drevet P, Grezes-Besset B, Shindrova P, Ivanov P, Grand-Ravel C, Vear F, Tourvieille de Labrouhe D, Charmet G, Nicolas P (1998) Study of the variability and evolution of Orobanche Cumana populations infesting sunflower in different European countries. Theor Appl Genet 96:1216–1222
García-Franco JG, Souza V, Eguiarte LE, Rico-Gray V (1998) Genetic variation, genetic structure and effective population size in the tropical holoparasite endophyte Bdallophyton bambusarum (Rafflesiaceae). Pl Syst Evol 210:271–288
Glazner JT, Devlin B, Ellstrand NC (1988) Biochemical and morphological evidence for host race evolution in desert mistletoe, Phorandendron californicum (Viscaceae). Pl Syst Evol 161:13–21
Holt RD, Lawton JH, Polis GA, Martinez ND (1999) Trophic rank and the species-area relationship. Ecology 80:1495–1504
Holzapfel S, Favill MZ, Gemmill CEC (2002) Genetic variation of the endangered holoparasite Dactylanthus taylorii (Balanophoraceae) in New Zealand. J Biogeog 29:663–676
Honnay O, Jacquemyn H (2007) Susceptibility of common and rare species to habitat fragmentation. Conserv Biol 21:823–831
Honnay O, Adriaens D, Coart E, Jacquemyn H, Roldan-Ruiz I (2007) Genetic diversity within and between remnant populations of the endangered calcareous grassland plant Globularia bisnagarica L. Conserv Genet 8:293–303
Jacquemyn H, Honnay O, Galbusera P, Roldán-Ruiz I (2004) Genetic structure of the forest herb Primula elatior in a changing landscape. Mol Ecol 13:211–219
Jerome CA, Ford BA (2002a) The discovery of three genetic races of the dwarf mistletoe Arceuthobium americanum (Viscaceae) provides insight into the evolution of parasitic angiosperms. Mol Ecol 11:387–405
Jerome CA, Ford BA (2002b) Comparative population structure and genetic diversity of Arceuthobium americanum (Viscaceae) and it Pinus host species: insight into host-parasite evolution in parasitic angiosperms. Mol Ecol 11:407–420
Kay QON (1986) Dioecy and pollination in Viscum album. Watsonia 16:232
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Kim SC, Lee C, Santos-Guerra A (2005) Genetic analysis and conservation of the endangered Canary Island woody sow-thistle, Sonchus gandogeri (Asteraceae). J Plant Res 118:147–153
Kruess A, Tscharntke T (2000) Species richness and parasitism in a fragmented landscape: experiments and field studies with insects on Vicia sepium. Oecologia 122:129–137
Kwak MM, Velterop O, van Andel J (1998) Pollen and gene flow in fragmented habitats. Appl Veg Sci 1:37–54
Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive associations between population size, fitness, and genetic variation? J Ecol 94:942–952
Linhart YB, Ellwood LM, Karron JD, Gehring JL (2003) Genetic differentiation in the dwarf mistletoes Arceuthobium vaginatum and Arceuthobium americanum on their principal and secondary hosts. Int J Pl Sci 164:61–69
Mathiasen RL, Nickrent DL, Shaw DC, Watson DM (2008) Mistletoes: pathology, systematics, ecology, and management. Pl Disease 92:988–1006
Mutikainen P, Koskela T (2002) Population structure of a parasitic plant and its perennial host. Heredity 89:318–324
Nybom H, Bartish IV (2000) Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspect Plant Ecol Evol 3(2):93–114
Olivier A, Glaszmann JC, Lanaud C, Leroux GD (1998) Population structure, genetic diversity and host specificity of the parasitic weed Striga hermonthica (Scrophulariaceae) in Sahel. Pl Syst Evol 209:33–45
Parisod C, Bonvin G (2008) Fine-scale genetic structure and marginal processes in an expanding population of Biscutella laevigata L. (Brassicaceae). Heredity 101:536–542
Peakall R, Smouse P (2006) GenAlEx v6.1 genetic Aanalysis in Excel. Australian National University, Canberra
Peters MD, Xiang QY, Thomas DT, Stucky J, Whiteman NK (2009) Genetic analysis of the federally endangered Echinacea laevigata using amplified fragment length polymorphisms (AFLP)—inferences in population genetic structure and mating system. Conserv Genet 10:1–14
Phoenix GK, Press MC (2005) Linking physiological traits to impacts on community structure and function: the role of root hemiparasitic Orobanchaceae (ex-Scrophulariaceae). J Ecol 93:67–78
Piessens K, Adriaens D, Jacquemyn H, Honnay O (2009) Synergistic effects of an extreme weather event and habitat fragmentation on a specialized insect herbivore. Oecologia 159:117–126
Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751
Price PW (1980) Evolutionary biology of parasites. Princeton University Press, Princeton
Roldán-Ruiz I, Dendauw J, Van Bockstaele E, Depickere A, De Loose M (2000) AFLP markers reveal high polymorphic rates in ryegrass (Lolium spp.). Mol Breeding 6:125–134
Salonen V, Setala H, Puustinen S (2000) The interplay between Pinus sylvestris, its root hemiparasite, Melampyrum pratense, and ectomycorrhizal fungi: influences on plant growth and reproduction. Ecoscience 7:195–200
Schmidt K, Jensen K (2000) Genetic structure and AFLP variation of remnant populations in the rare plant Pedicularis palustris (Scrophulariaceae) and its relation to population size and reproductive components. Am J Bot 87:678–689
Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 12:432–440
Steffan-Dewenter I, Tscharntke T (2002) Insect communities and biotic interactions on fragmented calcareous grasslands—a mini review. Biol Conserv 104:275–284
Van Rossum F, Echchgadda G, Szabadi I, Triest L (2002) Commonness and long-term survival in fragmented habitats: Primula elatior as a study case. Conserv Biol 16:1286–1295
Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151
Watson DM (2001) Mistletoe—a keystone resource in forests and woodlands worldwide. Ann Rev Ecol Syst 32:219–2490
Wright S (1951) The genetical structure of populations. Ann Eugenics 15:323–354
Wright S (1969) Evolution and the genetics of populations, vol 2. The theory of gene frequencies. University of Chicago Press, Chicago
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
Zabel J, Tscharntke T (1998) Does fragmentation of Urtica habitats affect phytophagous and predatory insects differentially? Oecologia 116:419–425
Zhivotovsky LA (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8:907–913
Zuber D (2004) Biological flora of Central Europe: Viscum album L. Flora 199:181–203
Zuber D, Widmer A (2009) Phylogeography and host race differentiation in the European mistletoe (Viscum album L.). Mol Ecol 18:1946–1962
Acknowledgements
Thanks to S. Boavida Torrado for help with fieldwork and seed germination experiments, and to N. Mergan, S. van Glabeke, and K. Vandepitte for their patience and assistance with genetic analyses. Comments from two anonymous referees greatly improved this paper. S.S. was partially supported by a fellowship from the Belgian American Educational Foundation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Stanton, S., Honnay, O., Jacquemyn, H. et al. A comparison of the population genetic structure of parasitic Viscum album from two landscapes differing in degree of fragmentation. Plant Syst Evol 281, 161–169 (2009). https://doi.org/10.1007/s00606-009-0198-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-009-0198-0