Skip to main content

Advertisement

Log in

Quantitative conservation genetics of wild and managed bees

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

Abstract

Quantitative genetic traits provide insights into the evolutionary potential of populations, as heritability estimates measure the population’s ability to respond to global changes. Although wild and managed bees are increasingly threatened by the degradation of natural habitats and climate change, risking plant biodiversity and agriculture production, no study has yet performed a systematic review of heritability estimates across the group. Here we help fill this knowledge gap, gathering all available heritability estimates for ants, bees, and wasps, evaluating which factors affect these estimates and assessing the reported genetic correlations between traits. Using a model selection approach to analyze a dataset of more than 800 heritability estimates, we found that heritability is influenced by trait type, with morphological traits exhibiting the highest heritability estimates, and defense and metabolism-related traits showing the lowest estimates. Study system, sociality degree, experimental design, estimation type (narrow or broad-sense heritability), and sample size were not found to affect heritability estimates. Results remained unaltered when correcting for phylogenetic inertia, and when analyzing social bees separately. Genetic correlations between honeybee traits revealed both positive coefficients, usually for traits in the same category, and negative coefficients, suggesting trade-offs among other traits. We discuss these findings and highlight the importance of maintaining genetic variance in fitness-related traits. Our study shows the importance of considering heritability estimates and genetic correlations when designing breeding and conservation programs. We hope this meta-analysis helps identify sustainable breeding approaches and conservation strategies that help safeguard the evolutionary potential of wild and managed bees.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allendorf F, Luikart G, Aitken SN (2012) Conservation and the genetics of populations. Wiley-Blackwell, West Sussex

    Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4

  • Bennett D, Hoffmann A (1998) Effects of size and fluctuating asymmetry on field fitness of the parasitoid Trichogramma carverae (Hymenoptera: Trichogrammatidae). J Anim Ecol 67:580–591

    Article  Google Scholar 

  • Bienefeld K, Pirchner F (1990) Heritabilities for several colony traits in the honeybee (Apis mellifera carnica). Apidologie 21:175–183

    Article  Google Scholar 

  • Bienefeld K, Ehrhardt K, Reinhardt F (2007) Genetic evaluation in the honey bee considering queen and worker effects—a BLUP-animal model approach. Apidologie 38:77–85. doi:10.1051/apido:2006050

    Article  Google Scholar 

  • Biesmeijer J, Roberts S (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313(5785):351–354

    Article  CAS  PubMed  Google Scholar 

  • Brascamp EW, Willam A, Boigenzahn C et al (2016) Heritabilities and genetic correlations for honey yield, gentleness, calmness and swarming behaviour in Austrian honey bees. Apidologie. doi:10.1007/s13592-016-0427-9

    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 

  • Brown MJF, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40:410–416. doi:10.1051/apido/2009019

    Article  Google Scholar 

  • Büchler R, Costa C, Hatjina F (2014) The influence of genetic origin and its interaction with environmental effects on the survival of Apis mellifera L. colonies in Europe. J Agric Res 53(2):205–214

    Google Scholar 

  • Byatt MA, Chapman NC, Latty T, Oldroyd BP (2015) The genetic consequences of the anthropogenic movement of social bees. Insectes Soc 63(1):15–24. doi:10.1007/s00040-015-0441-3

    Article  Google Scholar 

  • Cameron SA, Hines HM, Williams PH (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol J Linn Soc 91:161–188. doi:10.1111/j.1095-8312.2007.00784.x

    Article  Google Scholar 

  • Chapman NC, Lim J, Oldroyd BP (2008) Population genetics of commercial and feral honey bees in Western Australia. J Econ Entomol 101:272–277

    Article  CAS  PubMed  Google Scholar 

  • Charmantier A, Garant D (2005) Environmental quality and evolutionary potential: lessons from wild populations. Proc Biol Sci 272:1415–1425. doi:10.1098/rspb.2005.3117

    Article  PubMed  PubMed Central  Google Scholar 

  • Collins AM, Rinderer TE, Harbo JR, Brown MA (1984) Heritabilities and correlations for several characters in the honey bee. J Hered 75:135–140

    Article  Google Scholar 

  • Conte YL, Bruchou C, Benhamouda K (1994) Heritability of the queen brood post-capping stage duration in Apis mellifera mellifera L. Apidologie 25:513

    Article  Google Scholar 

  • Costa-Maia FM, Toledo VDAAD, Martins EN et al (2011) Estimates of covariance components for hygienic behavior in Africanized honeybees (Apis mellifera). Rev Bras Zootec 40:1909–1916. doi:10.1590/S1516-35982011000900010

    Article  Google Scholar 

  • Danforth BN, Cardinal S, Praz C et al (2013) The impact of molecular data on our understanding of bee phylogeny and evolution. Ann Rev Entamol 58:57–78

    Article  CAS  Google Scholar 

  • Davis ES, Murray TE, Fitzpatrick N et al (2010) Landscape effects on extremely fragmented populations of a rare solitary bee, Colletes floralis. Mol Ecol 19:4922–4935. doi:10.1111/j.1365-294X.2010.04868.x

    Article  PubMed  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. doi:10.1051/apido/2009027

    Article  Google Scholar 

  • Dowton M, Austin A (1994) Molecular phylogeny of the insect order Hymenoptera: Apocritan relationships. Proc Natl Acad Sci USA 91(21):9911–9915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans JD, Schwarz RS, Chen YP et al (2013) Standard methods for molecular research in Apis mellifera. J Apic Res. doi:10.3896/IBRA.1.52.4.11

    Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Inglaterra

    Google Scholar 

  • Fjerdingstad EJ (2005) Control of body size of Lasius niger ant sexuals–worker interests, genes and environment. Mol Ecol 14:3123–3132. doi:10.1111/j.1365-294X.2005.02648.x

    Article  PubMed  Google Scholar 

  • Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821

    Article  Google Scholar 

  • Giannini TC, Boff S, Cordeiro GD et al (2014) Crop pollinators in Brazil: a review of reported interactions. Apidologie. doi:10.1007/s13592-014-0316-z

    Google Scholar 

  • Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. doi:10.1126/science.1255957

    Google Scholar 

  • Gupta P, Reinsch N, Spötter A et al (2013) Accuracy of the unified approach in maternally influenced traits–illustrated by a simulation study in the honey bee (Apis mellifera). BMC Genet 14:36. doi:10.1186/1471-2156-14-36

    Article  PubMed  PubMed Central  Google Scholar 

  • Harbo JR (1992) Breeding honey bees (Hymenoptera: Apidae) for more rapid development of larvae and pupae. J Econ Entomol 85:2125–2130. doi:10.1093/jee/85.6.2125

    Article  Google Scholar 

  • Harbo JR, Harris JW (1999) Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J Econ Entomol 92:261–265. doi:10.1093/jee/92.2.261

    Article  Google Scholar 

  • Harmon LJ, Weir JT, Brock CD et al (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131. doi:10.1093/bioinformatics/btm538

    Article  CAS  PubMed  Google Scholar 

  • Hendry AP, Letcher BH, Gries G (2003) Estimating natural selection acting on stream-dwelling Atlantic Salmon: implications for the restoration of extirpated populations. Conserv Biol 17:795–805. doi:10.1046/j.1523-1739.2003.02075.x

    Article  Google Scholar 

  • Hoffman EA, Kovacs JL, Goodisman MAD (2008) Genetic structure and breeding system in a social wasp and its social parasite. BMC Evol Biol 8:13. doi:10.1186/1471-2148-8-239

    Article  Google Scholar 

  • Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216. doi:10.1126/science.1156108

    Article  CAS  PubMed  Google Scholar 

  • Jaffé R, Dietemann V, Allsopp MH et al (2010) Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conserv Biol 24:583–593. doi:10.1111/j.1523-1739.2009.01331.x

    Article  PubMed  Google Scholar 

  • Jaffé R, Pope N, Carvalho AT et al (2015) Bees for development: Brazilian survey reveals how to optimize stingless beekeeping. PLoS ONE 10(3):e0121157

    Article  PubMed  PubMed Central  Google Scholar 

  • Jensen H, Szulkin M, Slate J (2014) Molecular quantitative genetics. Oxford University Press, Oxford, pp 209–227

    Google Scholar 

  • Jha S (2015) Contemporary human-altered landscapes and oceanic barriers reduce bumble bee gene flow. Mol Ecol 24:993–1006. doi:10.1111/mec.13090

    Article  CAS  PubMed  Google Scholar 

  • Jha S, Kremen C (2013) Urban land use limits regional bumble bee gene flow. Mol Ecol. doi:10.1111/mec.12275

    PubMed  Google Scholar 

  • Kennedy CM, Lonsdorf E, Neel MC et al (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599. doi:10.1111/ele.12082

    Article  PubMed  Google Scholar 

  • Koffler S, Menezes C, Menezes PR et al (2015) Temporal variation in honey production by the stingless bee Melipona subnitida (Hymenoptera: Apidae): long-term management reveals its potential as a commercial species in Northeastern Brazil. J Econ Entomol 108:858–867. doi:10.1093/jee/tov055

    Article  PubMed  Google Scholar 

  • Kovacs JL, Hoffman EA, Marriner SM et al (2009) Environmental and genetic influences on queen and worker body size in the social wasp Vespula maculifrons. Insectes Soc 57:53–65. doi:10.1007/s00040-009-0050-0

    Article  Google Scholar 

  • Liu FH, Smith SM (2000) Estimating quantitative genetic parameters in haplodiploid organisms. Heredity (Edinb) 85:373–382

    Article  CAS  Google Scholar 

  • Meixner M, Costa C, Kryger P (2010) Conserving diversity and vitality for honey bee breeding. J Agric Res 49(1):85–92

    Google Scholar 

  • Moritz RFA (1985) Heritability of the postcapping stage in Apis mellifera and its relation to varroatosis resistance. J Hered 76:267–270

    Article  Google Scholar 

  • Mousseau T, Roff D (1987) Natural selection and the heritability of fitness components. Heredity (Edinb) 59:181–197

    Article  Google Scholar 

  • Munro JB, Heraty JM, Burks RA et al (2011) A molecular phylogeny of the chalcidoidea (Hymenoptera). PLoS ONE 6:e27023. doi:10.1371/journal.pone.0027023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niño EL, Cameron Jasper W (2015) Improving the future of honey bee breeding programs by employing recent scientific advances. Curr Opin Insect Sci 10:163–169. doi:10.1016/j.cois.2015.05.005

    Article  Google Scholar 

  • Nunes-Silva P, Hrncir M, Silva C et al (2013) Stingless bees, Melipona fasciculata, as efficient pollinators of eggplant (Solanum melongena) in greenhouses. Apidologie. doi:10.1007/s13592-013-0204-y

    Google Scholar 

  • Oldroyd B, Moran C (1983) Heritability of worker characters in the honeybee (Apis mellifera). Aust J Biol Sci 36(3):323–332

    Article  Google Scholar 

  • Oldroyd B, Rinderer T, Buco S (1991) Heritability of morphological characters used to distinguish European and Africanized honeybees. Theor Appl Genet 82:499–504. doi:10.1007/BF00588605

    Article  CAS  PubMed  Google Scholar 

  • Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. doi:10.1111/j.1600-0706.2010.18644.x

    Article  Google Scholar 

  • Oxley P, Oldroyd B (2010) The genetic architecture of honeybee breeding. Adv Insect Physiol 39:83

    Article  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. doi:10.1093/bioinformatics/btg412

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, et al (2016) nlme: linear and nonlinear mixed effects models

  • Postma E (2014) Four decades of estimating heritabilities in wild vertebrate populations: improved methods, more data, better estimates. Oxford University Press, Oxford

    Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  • Quicke DLJ, van Achterberg C (1900) Phylogeny of the subfamilies of Draconian. Ichneumonoidea, Hymenoptera

    Google Scholar 

  • Reed D, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? a meta-analysis. Evolution 55(6):1095–1103

    Article  CAS  PubMed  Google Scholar 

  • Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. doi:10.1111/j.2041-210X.2011.00169.x

    Article  Google Scholar 

  • Rinderer T (1977) Measuring the heritability of characters of honeybees. J Apic Res 16:95–98

    Article  Google Scholar 

  • Sachman-Ruiz B, Narváez-Padilla V, Reynaud E (2015) Commercial Bombus impatiens as reservoirs of emerging infectious diseases in central México. Biol Invasions 17:2043–2053. doi:10.1007/s10530-015-0859-6

    Article  Google Scholar 

  • Stephens P, Sutherland W (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends Ecol Evol 14(10):401–405

    Article  CAS  PubMed  Google Scholar 

  • Stürup M, den Boer S, Nash D et al (2011) Variation in male body size and reproductive allocation in the leafcutter ant Atta colombica: estimating variance components and possible trade-offs. Insectes Soc 58:47–55. doi:10.1007/s00040-010-0115-0

    Article  Google Scholar 

  • Tepedino V, Thompson R, Torchio P (1984) Heritability for size in the megachilid bee Osmia lignaria propinqua Cresson. Apidologie 15:83–88

    Article  Google Scholar 

  • Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era—concepts and misconceptions. Nat Rev Genet 9:255–266

    Article  CAS  PubMed  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • Wielewski P, Toledo VA, Martins EN et al (2014) Relationship Between Hygienic Behavior and Varroa destructor Mites in Colonies Producing Honey or Royal Jelly. Sociobiology 59:251–274

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the Shalene Jha, Margarita Lopez-Uribe, and Antonella Soro for organizing this special issue on bee conservation genetics. We also thank Dr. Tiago B. Quental for the interesting discussion on phylogenetic analyses and three anonymous referees for providing constructive suggestions to our manuscript. Funding was provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (SK), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (RJ, Grant Number 478982/2013-5).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sheina Koffler.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koffler, S., de Matos Peixoto Kleinert, A. & Jaffé, R. Quantitative conservation genetics of wild and managed bees. Conserv Genet 18, 689–700 (2017). https://doi.org/10.1007/s10592-016-0904-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-016-0904-8

Keywords

Navigation