Skip to main content

Advertisement

Log in

Successful maintenance of a stingless bee population despite a severe genetic bottleneck

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Stingless bees play an important ecological role as pollinators of many wild plant species in the tropics and have significant potential for the pollination of agricultural crops. Nevertheless, conservation efforts as well as commercial breeding programmes require better guidelines on the amount of genetic variation that is needed to maintain viable populations. In this context, we carried out a long-term genetic study on the stingless bee Melipona scutellaris to evaluate the population viability consequences of prolonged breeding from a small number of founder colonies. In particular, it was artificially imposed a genetic bottleneck by setting up a population starting from only two founder colonies, and continued breeding from it for a period of over 10 years in a location outside its natural area of occurrence. We show that despite a great reduction in the number of alleles present at both neutral microsatellite loci and the sex-determining locus relative to its natural source population, and an increased frequency in the production of sterile diploid males, the genetically impoverished population could be successfully bred and maintained for at least 10 years. This shows that in stingless bees, breeding from a small stock of colonies may have less severe consequences than previously suspected. In addition, we provide a simulation model to determine the number of colonies that are needed to maintain a certain number of sex alleles in a population, thereby providing useful guidelines for stingless bee breeding and conservation efforts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Adams J, Rothman ED, Kerr WE, Paulino ZL (1977) Estimation of the number of sex alleles and queen matings from diploid male frequencies in a population of Apis mellifera. Genetics 86:583–596

    PubMed  CAS  Google Scholar 

  • Aidar DS, Kerr WE (2001) Número de alelos XO em uma população de Melipona quadrifasciata anthidioides Lepeletier (Hymenoptera, Apidae, Meliponinae). Rev Bras Zool 18:1237–1244

    Article  Google Scholar 

  • Alves DA, Imperatriz-Fonseca VL, Francoy TM et al (2009) The queen is dead–long live the workers: intraspecific parasitism by workers in the stingless bee Melipona scutellaris. Mol Ecol 18:4102–4111

    Article  PubMed  CAS  Google Scholar 

  • Alves RMO, Carvalho CAL, Souza BA, Santos WS (in press) Areas of natural occurrence of Melipona scutellaris Latreille, 1811 (Hymenoptera: Apidae) in the State of Bahia, Brazil. An Acad Bras Cienc

  • Biesmeijer JC, Roberts SPM, Reemer M et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354

    Article  PubMed  CAS  Google Scholar 

  • Brown JC, Albrecht C (2001) The effect of tropical deforestation on stingless bees of the genus Melipona (Insecta: Hymenoptera: Apidae: Meliponini) in central Rondonia, Brazil. J Biogeogr 28:623–634

    Article  Google Scholar 

  • Camargo CA (1979) Sex determination in bees. XI Production of diploid males and sex determination in Melipona quadrifasciata. J Apic Res 18:77–84

    Google Scholar 

  • Camargo JMF, Pedro SRM (2007) Meliponini Lepeletier, 1836. In: Moure JS, Urban D, Melo GAR (eds) Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Sociedade Brasileira de Entomologia, Curitiba, pp 272–578

    Google Scholar 

  • Carvalho GA (2001) The number of sex alleles (CSD) in a bee population and its practical importance (Hymenoptera: Apidae). J Hymenopt Res 10:10–15

    Google Scholar 

  • Carvalho-Zilse GA, Kerr WE (2004) Natural substitutions of queens and flight distance of males in tiúba (Melipona compressipes fasciculata Smith, 1854) and uruçu (Melipona scutellaris Latreille, 1811) (Apidae, Meliponini). Acta Amazonica 34:649–652

    Article  Google Scholar 

  • Carvalho-Zilse GA, Costa-Pinto MFF, Nunes-Silva CG, Kerr WE (2009) Does beekeeping reduce genetic variability in Melipona scutellaris (Apidae, Meliponini)? Genet Mol Res 8:758–765

    Article  PubMed  CAS  Google Scholar 

  • Castro MS (2002) Bee fauna of some tropical and exotic fruits: potencial pollinators and their conservation. In: Kevan P, Imperatriz-Fonseca VL (eds) Pollinating bees—the conservation link between agriculture and nature. Ministry of Environment, Brasília, pp 275–288

    Google Scholar 

  • Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cornuet JM (1980) Rapid estimation of the number of sex alleles in panmictic honeybee populations. J Apic Res 19:3–5

    Google Scholar 

  • Cortopassi-Laurino M, Imperatriz-Fonseca VL, Roubik DW et al (2006) Global meliponiculture: challenges and opportunities. Apidologie 37:275–292

    Article  Google Scholar 

  • Costanza R, d’ Arge R, de Groot R et al (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    Article  CAS  Google Scholar 

  • Crozier RH (1976) Counter-intuitive property of effective population size. Nature 262:384

    Article  PubMed  CAS  Google Scholar 

  • De la Rúa P, Jaffé R, Dall’Olio R et al (2009) Biodiversity, conservation and current threats to European honeybees. Apidologie 40:263–284

    Article  Google Scholar 

  • Efron B, Tibshirani R (1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Statistical Science 1:54–77

    Article  Google Scholar 

  • Efron B, Tibshirani R (1993) An introduction to the bootstrap. Chapman& Hall/CRC, Florida

    Google Scholar 

  • Efron B, Tibshirani RJ (1998) An Introduction to Bootstrap. Chapman & Hall, London

    Google Scholar 

  • Estoup A, Solignac M, Cornuet JM (1994) Precise assessment of the number of patrilines and of genetic relatedness in honey bee colonies. Proc R Soc Lond B 258:1–7

    Article  CAS  Google Scholar 

  • Estoup A, Garnery L, Solignac M, Cornuet JM (1995) Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140:679–695

    PubMed  CAS  Google Scholar 

  • Goulson D, Lye GC, Darvill B (2008) Decline and Conservation of Bumble Bees. Annu Rev Entomol 53:191

    Article  PubMed  CAS  Google Scholar 

  • Green CL, Oldroyd BP (2002) Queen mating frequency and maternity of males in the stingless bee Trigona carbonaria Smith. Insectes Soc 49:196

    Article  Google Scholar 

  • Hasselmann M, Gempe T, Schiott M et al (2008) Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454:519–522

    Article  PubMed  CAS  Google Scholar 

  • Heard TA (1999) The role of stingless bees in crop pollination. Annu Rev Entomol 44:183–206

    Article  PubMed  CAS  Google Scholar 

  • Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53:209–230

    Article  PubMed  CAS  Google Scholar 

  • Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: The conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112

    Article  Google Scholar 

  • Kerr WE (1986) Mutation in bees 3. Application in bee populations of a mutation rate of μ = 1.6 × 10−6. Brazil J Genet 9:1–10

    Google Scholar 

  • Kerr WE (1987) Sex determination in bees XXI. Number of xo-heteroalleles in a natural population of Melipona compressipes fasciculata Apidae. Insect Soc 34:274–279

    Article  Google Scholar 

  • Kerr WE, Vencovsky R (1982) Bee breeding. 1. Effect of the number of colonies. Brazil J Genet 5:279–285

    Google Scholar 

  • Kimura M, Crow J (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725

    PubMed  CAS  Google Scholar 

  • Laidlaw HH, Gomes FP, Kerr WE (1956) Estimation of the number of lethal alleles in a panmictic population of Apis mellifera L. Genetics 41:179–188

    PubMed  CAS  Google Scholar 

  • Michener CD (1974) The social behavior of the bees. Harvard University Press, Massachusetts

    Google Scholar 

  • Nogueira-Neto P (2002) Inbreeding and building up small populations of stingless bees (Hymenoptera, Apidae). Rev Bras Zool 19:1181–1214

    Article  Google Scholar 

  • Owen RE, Owen ARG (1989) Effective population size in social Hymenoptera with worker-produced males. Heredity 63:59–65

    Article  Google Scholar 

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

    Google Scholar 

  • Page RE, Marks RW (1982) The population genetics of sex determination in honey bees—Random mating in closed populations. Heredity 48:263–270

    Article  Google Scholar 

  • Paxton RJ, Weissschuh N, Quezada-Euán JJG (1999) Characterization of dinucleotide microsatellite loci for stingless bees. Mol Ecol 8:690–692

    PubMed  CAS  Google Scholar 

  • Paxton RJ, Bego LR, Shah MM, Mateus S (2003) Low mating frequency of queens in the stingless bee Scaptotrigona postica and worker maternity of males. Behav Ecol Sociobiol 53:174–181

    Google Scholar 

  • Peters JM, Queller DC, Imperatriz-Fonseca VL, Strassmann JE (1998) Microsatellite loci for stingless bees. Mol Ecol 7:784–787

    PubMed  CAS  Google Scholar 

  • Peters JM, Queller DC, Imperatriz-Fonseca VL et al (1999) Mate number, kin selection and social conflicts in stingless bees and honeybees. Proceedings of the Royal Society B: Biological Sciences 266:379

    Article  Google Scholar 

  • Ross KG, Fletcher DJC (1986) Diploid male production—a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 19:283–291

    Article  Google Scholar 

  • Schmid-Hempel P, Schmid-Hempel R, Brunner PC et al (2007) Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck. Heredity 99:414–422

    Article  PubMed  CAS  Google Scholar 

  • Slaa EJ, Sanchez Chaves LA, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315

    Article  Google Scholar 

  • Tóth E, Strassmann JE, Nogueira-Neto P et al (2002) Male production in stingless bees: variable outcomes of queen-worker conflict. Mol Ecol 11:2661–2667

    Article  PubMed  Google Scholar 

  • Tóth E, Queller DC, Dollin A, Strassmann JE (2004) Conflict over male parentage in stingless bees. Insectes Soc 51:1–11

    Article  Google Scholar 

  • Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254

    Article  Google Scholar 

  • Wenseleers T, Alves DA, Francoy TM et al (2011) Intraspecific colony take-over by unrelated queens in a highly eusocial bee. Biol Lett. doi:10.1098/rsbl.2010.0819

  • Whiting PW (1943) Multiple alleles complementary sex determination of Habrobracon. Genetics 28:365–382

    PubMed  CAS  Google Scholar 

  • Woyke J (1963) What happens to diploid drone larvae in a honeybee colony. J Apic Res 2:73–75

    Google Scholar 

  • Yokoyama S, Nei M (1979) Population dynamics of sex-determining alleles in honey bees and self-incompatibility alleles in plants. Genetics 91:609–626

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742

    Article  PubMed  CAS  Google Scholar 

  • Zayed A, Roubik D, Packer L (2004) Use of diploid male frequency data as an indicator of pollinator decline. Proc R Soc Lond B 271:S9–S12

    Article  Google Scholar 

  • Zayed A, Constantin SA, Packer L (2007) Successful biological invasion despite a severe genetic load. PLoS ONE 2:e868

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the São Paulo Research Foundation (05/58093-8 to D.A.A.; 04/15801-0 to V.L.I.F.), the National Council of Technological and Scientific Development (480957/2004-5 to V.L.I.F.) and the FWO-Flanders (to T.W. and J.B.) for financial support. We are especially thankful to Dr. P. Nogueira-Neto for providing valuable support and helpful expertise, allowing us to collect data from his hives in São Simão. We also thank Mr. F. Carvalho, Mrs. S. Carvalho and Dr. M. Cortopassi-Laurino for their help with sample collection in Igarassu. Work was carried out under permit numbers 139311, 08BR001591/DF and 08BR002483/DF from the Brazilian Ministry of Environment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Denise Araujo Alves.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alves, D.A., Imperatriz-Fonseca, V.L., Francoy, T.M. et al. Successful maintenance of a stingless bee population despite a severe genetic bottleneck. Conserv Genet 12, 647–658 (2011). https://doi.org/10.1007/s10592-010-0171-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-010-0171-z

Keywords

Navigation