Skip to main content

Microsatellite analysis in museum samples reveals inbreeding before the regression of Bombus veteranus

Abstract

The worldwide decline of pollinators is an emerging threat and is a matter both for ecological and economic concerns. Population genetics can be used to correlate bumblebee decline with genetic parameters. In order to do so, historical data are needed. We used eight microsatellite loci to genotype pinned museum specimens of the declining bumblebee Bombus veteranus. Bumblebee samples were collected spanning a period of three decades (1895–1923). We detected low genetic diversity and inbreeding in the samples collected during the respective time periods. Inbreeding was also confirmed by the occurrence of sterile diploid males. Based on the data obtained, we speculate that low genetic diversity and inbreeding did not directly result in the collapse of B. veteranus in Belgium. However, inbreeding might still play an indirect role in the decline of bumblebee populations because of the appearance of diploid males and because a low H E might reduce the capacity to react to the drivers of bumblebee decline.

This is a preview of subscription content, access via your institution.

Figure 1.

References

  • Anderson, C.N.K., Ramakrishnan, U., Chan, Y.L., Hadly, E.A. (2005) Serial SimCoal: a population genetic model for data from multiple populations and points in time. Bioinformatics 21, 1733–1734

    PubMed  Article  CAS  Google Scholar 

  • Ashley, M.V., Berger-Wolf, T.Y., Caballero, I.C., Chaovalitwongse, W., Dasgupta, B., et al. (2008) Full siblings reconstruction in wild populations from microsatellite genetic markers. Nova, Hauppauge. Computational Biology: New Research

    Google Scholar 

  • Ashley, M.V., Caballero, I.C., Chaovalitwongse, W., Dasgupta, B., Govindan, P., Sheikh, S.I., Berger-Wolf, T.Y. (2009) KINALYZER, a computer program for reconstructing sibling groups. Mol. Ecol. Resour. 9, 1127–1131

    PubMed  Article  CAS  Google Scholar 

  • Blacquière, T., Smagghe, G., Van Gestel, C.A.M., Mommaerts, V. (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk-assessment. Ecotoxicoly 21, 973–992

    Article  Google Scholar 

  • Callen, D.F., Thompson, A.D., Shen, Y., Phillips, H.A., Richards, R.I., Mulley, J.C., Sutherland, G.R. (1993) Incidence and origin of “null” alleles in the (AC)n microsatellite markers. Am. J. Hum. Genet 52, 922–927

    PubMed  CAS  Google Scholar 

  • Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordes, N., Solter, L.F., Griswold, T.L. (2011) Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. USA 18, 662–667

    Article  Google Scholar 

  • Chapuis, M.-P., Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol 24, 621–631

    PubMed  Article  CAS  Google Scholar 

  • Chapuis, M.-P., Lecoq, M., Michalakis, Y., Loiseau, A., Sword, G.A., Piry, S., Estoup, A. (2008) Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Mol. Ecol 17, 3640–3653

    PubMed  Article  Google Scholar 

  • Chybicki, I.J., Burczyk, J. (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J. Hered 100, 106–113

    PubMed  Article  CAS  Google Scholar 

  • Connop, S., Hill, T., Steer, J., Shaw, P. (2010) The role of dietary breadth in national bumblebee (Bombus) declines: simple correlation? Biol. Conserv 143, 2739–2746

    Article  Google Scholar 

  • Cook, J.M., Crozier, R.H. (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol. Evol 10, 281–286

    PubMed  Article  CAS  Google Scholar 

  • Crawford, N.G. (2010) SMOGD: software for the measurement of genetic diversity. Mol. Ecol. Resour 10, 556–557

    PubMed  Article  Google Scholar 

  • Duchateau, M.J., Hishiba, H., Velthuis, H.H.W. (1994) Diploid males in the bumble bee Bombus terrestris. Entomol. Exp. Appl 71, 263–269

    Article  Google Scholar 

  • El Mousadik, A., Petit, R.J. (1996) Chloroplast DNA phylogeography of the argan tree of Morocco. Mol. Ecol 5, 547–555

    PubMed  Article  CAS  Google Scholar 

  • Estoup, A., Solignac, M., Harry, M., Cornuet, J.-M. (1993) Characterization of (GT)n and (CT)n microsatellites in two insect species Apis mellifera and Bombus terrestris. Nucleic. Acid. Res 21, 1427–1431

    PubMed  Article  CAS  Google Scholar 

  • Excoffier, L., Novembre, J., Schneider, S. (2000) SimCoal: a general coalescent program for simulation of molecular data in interconnected populations with arbitrary demography. J. Hered 91, 506–509

    PubMed  Article  CAS  Google Scholar 

  • Frankham, R. (2005) Genetics and extinction. Biol. Conserv 126, 131–140

    Article  Google Scholar 

  • Garza, J.C., Williamson, E. (2001) Detection of reduction in population size using data from microsatellite DNA. Mol. Ecol 10, 305–318

    PubMed  Article  CAS  Google Scholar 

  • Gerloff, C.U., Schmid-Hempel, P. (2005) Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). Oikos 111, 67–80

    Article  Google Scholar 

  • Goudet, J. (2001) Fstat: a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet, J. (1995): Fstat (version 1.2): a computer program to calculate F-statistics. J. Hered 86, 485–486

    Google Scholar 

  • Goulson, D., Osborne, J.L. (2010) Foraging economics. Bumblebees: behaviour, ecology and conservation (ed. by D. Goulson), p. 96. Oxford University Press, Oxford, UK

    Google Scholar 

  • Goulson, D., Lye, G.C., Darvill, B. (2008) Decline and conservation of bumble bees. Annu. Rev. Entomol 53, 191–208

    PubMed  Article  CAS  Google Scholar 

  • Guinand, B., Scribner, K.T. (2003) Evaluation of methodology for detection of genetic bottlenecks: inferences from temporally replicated lake trout populations. C. R. Biol 326(Supplement 1), 61–67

    Article  Google Scholar 

  • Hines, H.M., Hendrix, S.D. (2005) Bumble bee (Hymenoptera: Apidae) diversity and abundance in tallgrass prairie patches: effects of local and landscape floral resources. Environ. Entomol. 34, 1477–1484

    Article  Google Scholar 

  • Jost, L. (2008) G(ST) and its relatives do not measure differentiation. Mol. Ecol. 17, 4015–4026

    PubMed  Article  Google Scholar 

  • Keller, L.F., Waller, D.M. (2002) Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241

    Article  Google Scholar 

  • Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., et al. (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B. 274, 303–313

    PubMed  Article  Google Scholar 

  • Kremen, C., Williams, N.M., Aizen, M.A., Gemmill-Herren, B., Le Buhn, G., et al. (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol. Lett 10, 299–314

    PubMed  Article  Google Scholar 

  • Lozier, J.D., Cameron, S.A. (2009) Comparative genetic analyses of historical and contemporary collections highlight contrasting demographic histories for the bumblebees Bombus pensylvanicus and B. impatiens in Illinois. Mol. Ecol 18, 1875–1886

    PubMed  Article  Google Scholar 

  • Meeus, I., Brown, M.J.F., de Graaf, D.C., Smagghe, G. (2011) Effects of invasive parasites on bumble bee declines. Conserv. Biol 25, 662–671

    PubMed  Article  Google Scholar 

  • Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590

    PubMed  CAS  Google Scholar 

  • Packer, L., Owen, R. (2001) Population genetic aspects of pollinator decline. Conserv. Ecol 5, 4

    Google Scholar 

  • Pauly, A., Rasmont, P. (2010) Les bourdons de la Belgique. Website Atlas Hymenoptera, Gembloux Agro-Biotech, Université de Mons, Gembloux, Mons. http://www.zoologie.umh.ac.be/hymenoptera/page.asp?id=160. Accessed 10 January, 2012.

  • Peakall, R., Smouse, F. (2006) GENALEX 6: Genetic Analysis in Excel. Population Genetic Software for Teaching and Research. Australian National University, Canberra, Australia

    Google Scholar 

  • Rasmont, P., Iserbyt, I. (2010) Atlas of the European Bees: genus Bombus. STEP Project, Atlas Hymenoptera, Mons, Gembloux. http://www.zoologie.umh.ac.be//hymenoptera/page.asp?ID=169. Accessed 25 December, 2011.

  • Rasmont, P., Mersch, P. (1988) Premiere estimation de la dérive faunique chez les bourdons de la Belgique (Hymenoptera, Apidae). Ann. Soc. Royal Zool. Bel 118, 141–147

    Google Scholar 

  • Rasmont, P., Leclercq, J., Jacob-Remacle, A., Pauly, A., Gaspar, C. (1993) The faunistic drift of Apoidea in Belgium. pp. 65-87, in Bruneau, E., Bees for pollination, Commission of the European Communities, Brussels, 237 pp.

  • Rasmont, P., Pauly, A., Terzo, M., Patiny, S., Michez, D., Iserbyt, S., Barbier, Y., Haubruge, E. (2005) The survey of wild bees (Hymenoptera, Apoidea) in Belgium and France. FAO, Roma, 18 pp.

  • Reber Funk, C., Schmidt-Hempel, R., Schmid-Hempel, P. (2006) Microsatellite loci for Bombus spp. Mol. Ecol. Notes 6, 83–86

    Article  Google Scholar 

  • Schmid-Hempel, P., Schmid-Hempel, R., Brunner, P.C., Seeman, O.D., Allen, G.R. (2007) Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck. Heredity 99, 414–422

    PubMed  Article  CAS  Google Scholar 

  • Söderman, G. (1999) Diversity of pollinator communities in Eastern Fennoskandia and Eastern Baltics. Results from pilot monitoring with yellow traps in 1997–1998. The Finnish Environment 355, Finnish Environment Institute, Helsinki.

  • Sorati, M., Newman, M., Hovman, A.A. (1996) Inbreeding and incompatibility in Trichogramma brassicae: evidence and implications for quality control. Entomol. Exp. Appl 78, 283–290

    Article  Google Scholar 

  • Strange, J.P., Knoblett, J., Griswold, T. (2009) DNA amplification from pin-mounted bumble bees (Bombus) in a museum collection: effects of fragment size and specimen age on successful PCR. Apidologie 40, 134–139

    Article  CAS  Google Scholar 

  • Stroot, P., Depiereux (1989) Proposition d'une méthodologie pour établir des listes rouges d'invertébrés menacé. Biol. Conserv 48, 163–179

  • Thompson, H.M. (2001) Assessing the exposure and toxicity of pesticides to bumblebees (Bombus sp.). Apidologie 32, 305–321

    Article  CAS  Google Scholar 

  • Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P. (2004) MICROCHECKER: software for identifying and correcting genotyping errors. Mol. Ecol. Notes 4, 535–538

    Article  Google Scholar 

  • Voveikov, G.S. (1953) Estestvennaya smena samok vo cem’ya shchmelej (Hym. Bomb.). Russkoe entomol obozrenie 33, 174–184

    Google Scholar 

  • Wandeler, P., Hoeck, P.E.A., Keller, L.F. (2007) Back to the future: museum specimens in population genetics. Trends Ecol. Evol 22, 634–642

    PubMed  Article  Google Scholar 

  • Wang, J.L. (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166, 1963–1979

    PubMed  Article  Google Scholar 

  • Whitehorn, P.R., Tinsley, M.C., Brown, M.J.F., Darvill, B., Goulson, D. (2009) Impacts of inbreeding on bumblebee colony fitness under field conditions. BMC Evol. Biol 9, 152

    PubMed  Article  Google Scholar 

  • Williams, P.H. (1982) The distribution and decline of British bumble bees (Bombus Latr.). J. Apic. Res 21, 236–245

    Google Scholar 

  • Zayed, A. (2009) Bee genetics and conservation. Apidologie 40, 237–262

    Article  Google Scholar 

Download references

Acknowledgments

This project was supported by the Special Research Fund of Ghent University, the Fund for Scientific Research-Flanders (FWO-Vlaanderen), and the Fonds de la Recherche Scientifique–Fonds de la Recherche Fondamentale Collective (FNRS-FRFC) (FRFC convention no. 2.4618.12).

Bombus veteranus : l’analyse de microsatellites de cette espèce à partir d’échantillons d’un museum révèle une consanguinité avant leur régression.

Microsatellites / ADN ancien / collections muséographiques / diversité génétique / déclin des bourdons

Mikrosatelliten-Analyse von Museumsproben verrät das Auftreten von Inzucht bereits vor dem Rückgang von Bombus veteranus.

Mikrosatelliten / ancient DNA / Museumssammlungen / geneRückgang von Hummeln / Rückgang von Hummeln

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guy Smagghe.

Additional information

Bombus veteranus : l’analyse de microsatellites de cette espèce à partir d’échantillons d’un museum révèle une consanguinité avant leur régression.

Microsatellites/ADN ancien/collections muséographiques/diversité génétique/déclin des bourdons

Mikrosatelliten-Analyse von Museumsproben verrät das Auftreten von Inzucht bereits vor dem Rückgang von Bombus veteranus.

Mikrosatelliten/ancient DNA/Museumssammlungen/geneRückgang von Hummeln/Rückgang von Hummeln

Manuscript editor: Marina Meixner

Electronic supplementary materials

Below is the link to the electronic supplementary material.

ESM 1

(PDF 127 kb)

ESM 2

(PDF 87 kb)

ESM 3

(PDF 88 kb)

ESM 4

(PDF 129 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Maebe, K., Meeus, I., Maharramov, J. et al. Microsatellite analysis in museum samples reveals inbreeding before the regression of Bombus veteranus . Apidologie 44, 188–197 (2013). https://doi.org/10.1007/s13592-012-0170-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-012-0170-9

Keywords

  • microsatellites
  • ancient DNA
  • museum collections
  • genetic diversity
  • bumblebee decline