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.
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
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
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
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
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
Camargo CA (1979) Sex determination in bees. XI Production of diploid males and sex determination in Melipona quadrifasciata. J Apic Res 18:77–84
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
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
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
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
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
Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662
Cook J, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol Evol 10:281–286
Cornuet JM (1980) Rapid estimation of the number of sex alleles in panmictic honeybee populations. J Apic Res 19:3–5
Cortopassi-Laurino M, Imperatriz-Fonseca VL, Roubik DW et al (2006) Global meliponiculture: challenges and opportunities. Apidologie 37:275–292
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
Crozier RH (1976) Counter-intuitive property of effective population size. Nature 262:384
De la Rúa P, Jaffé R, Dall’Olio R et al (2009) Biodiversity, conservation and current threats to European honeybees. Apidologie 40:263–284
Efron B, Tibshirani R (1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Statistical Science 1:54–77
Efron B, Tibshirani R (1993) An introduction to the bootstrap. Chapman& Hall/CRC, Florida
Efron B, Tibshirani RJ (1998) An Introduction to Bootstrap. Chapman & Hall, London
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
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
Goulson D, Lye GC, Darvill B (2008) Decline and Conservation of Bumble Bees. Annu Rev Entomol 53:191
Green CL, Oldroyd BP (2002) Queen mating frequency and maternity of males in the stingless bee Trigona carbonaria Smith. Insectes Soc 49:196
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
Heard TA (1999) The role of stingless bees in crop pollination. Annu Rev Entomol 44:183–206
Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53:209–230
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: The conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112
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
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
Kerr WE, Vencovsky R (1982) Bee breeding. 1. Effect of the number of colonies. Brazil J Genet 5:279–285
Kimura M, Crow J (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725
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
Michener CD (1974) The social behavior of the bees. Harvard University Press, Massachusetts
Nogueira-Neto P (2002) Inbreeding and building up small populations of stingless bees (Hymenoptera, Apidae). Rev Bras Zool 19:1181–1214
Owen RE, Owen ARG (1989) Effective population size in social Hymenoptera with worker-produced males. Heredity 63:59–65
Packer L, Owen R (2001) Population genetic aspects of pollinator decline. Conserv Ecol 5:4
Page RE, Marks RW (1982) The population genetics of sex determination in honey bees—Random mating in closed populations. Heredity 48:263–270
Paxton RJ, Weissschuh N, Quezada-Euán JJG (1999) Characterization of dinucleotide microsatellite loci for stingless bees. Mol Ecol 8:690–692
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
Peters JM, Queller DC, Imperatriz-Fonseca VL, Strassmann JE (1998) Microsatellite loci for stingless bees. Mol Ecol 7:784–787
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
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
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
Slaa EJ, Sanchez Chaves LA, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315
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
Tóth E, Queller DC, Dollin A, Strassmann JE (2004) Conflict over male parentage in stingless bees. Insectes Soc 51:1–11
Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247–254
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
Woyke J (1963) What happens to diploid drone larvae in a honeybee colony. J Apic Res 2:73–75
Yokoyama S, Nei M (1979) Population dynamics of sex-determining alleles in honey bees and self-incompatibility alleles in plants. Genetics 91:609–626
Zayed A (2009) Bee genetics and conservation. Apidologie 40:237–262
Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742
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
Zayed A, Constantin SA, Packer L (2007) Successful biological invasion despite a severe genetic load. PLoS ONE 2:e868
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
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-010-0171-z