Skip to main content

Advertisement

SpringerLink
Log in

Effects of outcrossing in fragmented populations of the primarily selfing forest herb Geum urbanum

  • Research Article
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

In fragmented landscapes, small populations may be subjected to inbreeding or genetic drift. Gene flow is expected to alleviate the burden of deleterious mutations in such populations. The beneficial effects of outcrossing may, however, depend on life history characteristics such as the species’ breeding system. Frequent selfing is expected to purge (sub)lethal alleles and mitigate inbreeding depression, at least if the load of mildly deleterious mutations has not accumulated through genetic drift in populations with a small effective size. Gene-inflow from distant source populations can cause outbreeding depression due to genomic incompatibilities. We tested these predictions using highly fragmented populations of the self-compatible forest herb Geum urbanum. Assessment of mating system parameters using microsatellite markers inferred high selfing rates (92.5%), confirming the predominantly self-fertilizing character of the study species. We conducted experimental pollinations with self and outcross pollen collected from populations at different distances from the target populations. There were no significant signs of inbreeding depression, even in very small target populations. Except for a minor negative effect on the germination rate for the long-distance crosses, we found no effects of outbreeding on fitness estimates.

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

  • Arens P, Durka W, Wernke-Lenting JH, Smulders MJM (2004) Isolation and characterisation of microsatellite loci in Geum urbanum (Rosaceae) and their transferability within the genus Geum. Mol Ecol Notes 4:209–212

    Article  CAS  Google Scholar 

  • Ayroles JF, Hughes KA, Rowe KC, Reedy MM, Rodriquez-zas SL, Drnevich JM, Caceres CE, Paige KN (2009) A genomewide assessment of inbreeding depression: gene number, function, and mode of action. Conserv Biol 23:920–930

    Article  PubMed  Google Scholar 

  • Barrett SCH, Kohn J (1991) The genetic and evolutionary consequences of small population size in plant: implications for conservation. In: Falk D, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, Oxford, pp 3–30

    Google Scholar 

  • Bossuyt B (2007) Genetic rescue in an isolated metapopulation of a naturally fragmented plant species, Parnassia palustris. Conserv Biol 21:832–841

    Article  PubMed  Google Scholar 

  • Busch JW (2006) Heterosis in an isolated, effectively small, and self-fertilizing population of the flowering plant Leavenworthia alabamica. Evolution 60:184–191

    PubMed  Google Scholar 

  • Byers D, Waller DM (1999) Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst 30:479–513

    Article  Google Scholar 

  • Charlesworth D, Wright SI (2001) Breeding systems and genome evolution. Curr Opin Genet Dev 11:685–690

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B, Charlesworth D, Morgan MT (1990) Genetic loads and estimates of mutation rates in highly inbred plant populations. Nature 347:380–382

    Article  Google Scholar 

  • Charlesworth D, Morgan MT, Charlesworth B (1993) Mutation accumulation in finite outbreeding and inbreeding populations. Genet Res 61:39–56

    Article  Google Scholar 

  • Crnokrak P, Barrett SCH (2002) Purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358

    PubMed  Google Scholar 

  • David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487

    Article  CAS  PubMed  Google Scholar 

  • Dolgin ES, Charlesworth B, Baird SE, Cutter AD (2007) Inbreeding and outbreeding deperssion in Caenorhabditis nematodes. Evolution 61:1339–1352

    Article  PubMed  Google Scholar 

  • Dudash MR, Fenster CB (2000) Inbreeding and outbreeding depression in small populations. In: Young G, Clarke GM (eds) Genetics, demography and viability of fragmented populations. Cambridge University Press, Cambridge, pp 35–53

    Chapter  Google Scholar 

  • Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 57:1757–1768

    Article  Google Scholar 

  • Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475

    Article  PubMed  Google Scholar 

  • Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242

    Article  Google Scholar 

  • Fenster CB, Galloway LF (2000) Inbreeding and outbreeding depression in natural populations of Chamaechrista fasciculate (Fabaceae). Conserv Biol 14:1406–1412

    Article  Google Scholar 

  • Fischer M, Matthies D (1997) Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae). Am J Bot 84:1685–1692

    Article  Google Scholar 

  • Glémin S (2004) How are deleterious mutations purged? Drift versus non-random mating. Evolution 57:2678–2687

    Google Scholar 

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

  • Grime JP, Mason G, Curtis AV, Rodman J, Band SR, Mowforth MAG, Neal AM, Shaw S (1981) A comparative study of germination characteristics in a local flora. J Ecol 69:1017–1059

    Article  Google Scholar 

  • Grindeland JM (2008) Inbreeding depression and outbreeding depression in Digitalis purpurea: optimal outcrossing distance in a tetraploid. J Evol Biol 21:716–726

    Article  CAS  PubMed  Google Scholar 

  • Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc B-Biol Sci 351:1291–1298

    Article  Google Scholar 

  • Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155

    Article  Google Scholar 

  • Ingvarsson PK (2001) Restoration of genetic variation lost—the genetic rescue hypothesis. Trends Ecol Evol 16:62–63

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jain SK (1976) The evolution of inbreeding plants. Annu Rev Ecol Syst 7:469–494

    Article  Google Scholar 

  • Johansen-Morris AD, Latta RG (2006) Fitness consequences of hybridization between ecotypes of Avena barbata: hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution 60:1585–1595

    CAS  PubMed  Google Scholar 

  • Johnston MO, Schoen DJ (1996) Correlated evolution of self-fertilization and inbreeding depression: an experimental study of nine populations of Amsinckia (Boraginaceae). Evolution 50:1478–1491

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  CAS  PubMed  Google Scholar 

  • Lande R, Schemske DW (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40

    Article  Google Scholar 

  • Lande R, Shannon S (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50:434–437

    Article  Google Scholar 

  • Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships plant population size, fitness and genetic variation? J Ecol 94:942–952

    Google Scholar 

  • Littell RC, Stroup WW, Freund RJ (2002) SAS for linear models. SAS Institute, Cary

    Google Scholar 

  • Paland S, Schmid B (2003) Population size and the nature of genetic load in Gentianella germanica. Evolution 57:2242–2251

    PubMed  Google Scholar 

  • Price MV, Waser NM (1979) Pollen dispersal and optimal outcrossing in Delphinium nelsoni. Nature 277:294–297

    Article  Google Scholar 

  • Richards CM (2000) Inbreeding depression and genetic rescue in a plant metapopulation. Am Nat 155:383–394

    Article  PubMed  Google Scholar 

  • Schmidt T, Arens P, Smulders MJM, Billeter R, Liira J, Augenstein I, Durka W (2009) Effects of landscape structure on genetic diversity of Geum urbanum L. populations in agricultural landscapes. Flora 204:549–559

    Google Scholar 

  • Shaffer M (1981) Minimum population size for species conservation. Bioscience 31:131–134

    Article  Google Scholar 

  • Taylor K (1997) Biological flora of the British Isles. Geum urbanum L. J Ecol 85:705–720

    Article  Google Scholar 

  • Vandepitte K, Jacquemyn H, Roldan-Ruiz I, Honnay O (2007) Landscape genetics of the self-compatible forest herb Geum urbanum: effects of habitat age, fragmentation and local environment. Mol Ecol 16:4171–4179

    Article  CAS  PubMed  Google Scholar 

  • Waser NM (1993) Population structure, optimal outbreeding, and assortive mating in angiosperms. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. Theoretical and empirical perspectives. University Press Chicago, Chicago, pp 173–200

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whitlock MC, Ingvarsson PK, Hatfield T (2000) Local drift load and the heterosis of interconnected populations. Heredity 84:452–457

    Article  PubMed  Google Scholar 

  • Willi Y, Fischer M (2005) Genetic rescue in interconnected populations of small and large size of the self-incompatible Ranunculus reptans. Heredity 95:437–443

    Article  CAS  PubMed  Google Scholar 

  • Willi Y, van Buskirk J (2005) Genomic compatibility occurs over a wide range of parental genetic similarity in an outcrossing plant. Proc R Soc B: Biol Sci 272:1333–1338

    Article  Google Scholar 

  • Willi Y, van Buskirk J, Fischer M (2005) A threefold genetic Allee effect: population size affects cross-compatibility, inbreeding depression and drift load in the self-incompatible Ranunculus reptans. Genetics 169:2255–2265

    Article  CAS  PubMed  Google Scholar 

  • Willis JH (1999) The role of genes of large effect on inbreeding depression in Mimulus guttatus. Evolution 53:1678–1691

    Article  CAS  Google Scholar 

  • Wright S (1977) Evolution and the genetics of populations, experimental results and evolutionary deductions, vol 3. University of Chicago Press, Chicago

    Google Scholar 

  • Young A, Boyle T, Brown A (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  Google Scholar 

Download references

Acknowledgments

This research was funded by a grant of the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen). We are grateful to S. Van Glabeke, L. Gevaert, G. Lejeune, K. Mehdikhanlou, N. Mergan, A. Staelens and C. Pardon for excellent assistance in the greenhouse, field or lab, or with the planning of experiments. We thank M. Levenson for language assistance and two anonymous reviewers for useful comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Laboratory of Plant Ecology, Biology Department, Katholieke Universiteit Leuven (KULeuven), Kasteelpark Arenberg 31, 3001, Heverlee, Belgium

    K. Vandepitte, O. Honnay & H. Jacquemyn

  2. Plant Sciences Unit, Growth and Development, Institute for Agricultural and Fisheries Research (ILVO), Caritasstraat 21, 9090, Melle, Belgium

    I. Roldán-Ruiz

Authors
  1. K. Vandepitte
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. Honnay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Jacquemyn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. Roldán-Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Vandepitte.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vandepitte, K., Honnay, O., Jacquemyn, H. et al. Effects of outcrossing in fragmented populations of the primarily selfing forest herb Geum urbanum . Evol Ecol 24, 1353–1364 (2010). https://doi.org/10.1007/s10682-010-9395-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-010-9395-0

Keywords

Search

Navigation