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RESEARCH ARTICLE

Management tools for genetic diversity in an isolated population of the honeybee (Apis mellifera) in New Zealand

Gertje E. L. Petersen https://orcid.org/0000-0003-2956-0426 A D , Peter F. Fennessy A and Peter K. Dearden B C
+ Author Affiliations
- Author Affiliations

A AbacusBio Ltd, 442 Moray Place, Dunedin 9016, New Zealand.

B Department of Biochemistry, University of Otago, 710 Cumberland Street, Dunedin 9016, New Zealand.

C Genomics Aotearoa, 710 Cumberland Street, Dunedin 9016, New Zealand.

D Corresponding author. Email: GPetersen@abacusbio.co.nz

Animal Production Science - https://doi.org/10.1071/AN21102
Submitted: 26 February 2021  Accepted: 1 June 2021   Published online: 20 September 2021

Abstract

Context: Beekeepers and honeybee queen breeders alike currently have few tools at their disposal for the management of genetic diversity inside their populations. Pedigree information is often absent, beekeepers cannot afford to genotype selection candidates due to costs, and acquisition of material for genotyping without risk to individual queen bees is difficult. However, in New World honeybee populations where import of additional genetic material to refresh the population is restricted (e.g. Australia) or impossible (e.g. New Zealand), management of genetic diversity is important for population sustainability. While the role of individual beekeepers in maintaining genetic resources becomes crucial under these circumstances, a more holistic approach to the management of genetic diversity is needed to allow for maximum impact of their contribution.

Aims: The establishment of affordable genotyping methodologies for successful strategies in managing honeybee genetic diversity, as well as the necessary delivery systems for the results to support the beekeeping community by providing interpretation in the context of the wider population.

Methods: Genotyping-by-sequencing of honeybee samples collected as part of a national survey were used as the basis for assessment of New Zealand’s honeybee genetic diversity and development of a tool with largely self-explanatory outputs that can be used directly by beekeepers.

Key results: It would appear that New Zealand’s honeybee population is sufficiently diverse to maintain population viability. However, both within regions and within companies, genetic diversity is significantly reduced, especially in the case of specialised queen breeders, indicating that active management will be necessary to achieve long-term sustainability.

Conclusions: Interactive tools are needed to help beekeepers understand their role in maintaining overall genetic diversity in the honeybee population as well as the potential impact of planned bee movement and queen acquisitions. Regular rounds of voluntary bee sampling can be used as the basis for management decisions without concentrating genotyping load on specific operators and restricting diversity assessments to subpopulations.

Implications: The described strategy is expected to both improve the outlook of New Zealand’s honeybee population as a whole and facilitate stringent genetic improvement programs by enabling queen breeders to make informed selection decisions and giving beekeepers confidence in the viability of their population.

Keywords: genetic diversity, inbreeding management, honeybee, Apis mellifera, genotyping-by-sequencing.


References

Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available at http://www.bioinformatics.babraham.ac.uk/projects/fastqc

Bienefeld K (2016) Breeding success or genetic diversity in honey bees? Bee World 93, 40–44.
Breeding success or genetic diversity in honey bees?Crossref | GoogleScholarGoogle Scholar |

Bienefeld K, Ehrhardt K, Reinhardt F (2008) Noticeable success in honey bee selection after the introduction of genetic evaluation using BLUP. American Bee Journal 2008, 739–742.

Bilodeau L, Avalos A, Danka RG (2020) Genetic diversity of the complementary sex-determiner (csd) gene in two closed breeding stocks of Varroa-resistant honey bees. Apidologie 51, 1125–1132.
Genetic diversity of the complementary sex-determiner (csd) gene in two closed breeding stocks of Varroa-resistant honey bees.Crossref | GoogleScholarGoogle Scholar |

Büchler R, Costa C, Hatjina F, Andonov S, Meixner MD, Le Conte Y, Uzunov A, Berg S, Bienkowska M, Bouga M, Drazic M, Dyrba W, Kryger P, Panasiuk B, Pechhacker H, Petrov P, Kezić N, Korpela S, Wilde J (2014) The influence of genetic origin and its interaction with environmental effects on the survival of Apis mellifera L. colonies in Europe. Journal of Apicultural Research 53, 205–214.
The influence of genetic origin and its interaction with environmental effects on the survival of Apis mellifera L. colonies in Europe.Crossref | GoogleScholarGoogle Scholar |

Cassady JP, Young LD, Leymaster KA (2002) Heterosis and recombination effects on pig growth and carcass traits. Journal of Animal Science 80, 2286–2302.
Heterosis and recombination effects on pig growth and carcass traits.Crossref | GoogleScholarGoogle Scholar | 12350006PubMed |

Chang W, Cheng J, Allaire JJ, Xie Y, McPherson J (2020) shiny: web application framework for R. R package version 1.5.0. Available at http://www.rstudio.com/shiny/

Chapman NC, Harpur BA, Lim J, Rinderer TE, Allsopp MH, Zayed A, Oldroyd BP (2015) A SNP test to identify Africanized honeybees via proportion of ‘African’ ancestry. Molecular Ecology Resources 15, 1346–1355.
A SNP test to identify Africanized honeybees via proportion of ‘African’ ancestry.Crossref | GoogleScholarGoogle Scholar | 25846634PubMed |

Chapman NC, Harpur BA, Lim J, Rinderer TE, Allsopp MH, Zayed A, Oldroyd BP (2016) Hybrid origins of Australian honeybees (Apis mellifera). Apidologie 47, 26–34.
Hybrid origins of Australian honeybees (Apis mellifera).Crossref | GoogleScholarGoogle Scholar |

Cobey SW, Sheppard WS, Tarpy DR (2011) Status of breeding practices and genetic diversity in domestic U.S. honey bees. In ‘Honey bee colony health: challenges and sustainable solutions’. pp. 25–36. (CRC Press: Boca Raton, FL, USA)

De la Rúa P, Jaffé R, Dall’Olio R, Muñoz I, Serrano J (2009) Biodiversity, conservation and current threats to European honeybees. Apidologie 40, 263–284.
Biodiversity, conservation and current threats to European honeybees.Crossref | GoogleScholarGoogle Scholar |

Delaney DA (2008) Genetic characterization of US honey bee populations. PhD Thesis, Washington State University, WA, USA.

Dodds KG, McEwan JC, Brauning R, Anderson RM, van Stijn TC, Kristjánsson T, Clarke SM (2015) Construction of relatedness matrices using genotyping-by-sequencing data. BMC Genomics 16, 1047
Construction of relatedness matrices using genotyping-by-sequencing data.Crossref | GoogleScholarGoogle Scholar | 26654230PubMed |

Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379
A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species.Crossref | GoogleScholarGoogle Scholar | 21573248PubMed |

Evans JD, Shearman DCA, Oldroyd BP (2004) Molecular basis of sex determination in haplodiploids. Trends in Ecology & Evolution 19, 1–3.
Molecular basis of sex determination in haplodiploids.Crossref | GoogleScholarGoogle Scholar |

Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE 9, e90346
TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline.Crossref | GoogleScholarGoogle Scholar | 24587335PubMed |

Harpur BA, Minai S, Kent CF, Zayed A (2012) Management increases genetic diversity of honey bees via admixture. Molecular Ecology 21, 4414–4421.
Management increases genetic diversity of honey bees via admixture.Crossref | GoogleScholarGoogle Scholar | 22564213PubMed |

Hyink O, Laas F, Dearden PK (2013) Genetic tests for alleles of complementary-sex-determiner to support honeybee breeding programmes. Apidologie 44, 306–313.
Genetic tests for alleles of complementary-sex-determiner to support honeybee breeding programmes.Crossref | GoogleScholarGoogle Scholar |

Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589–595.
Fast and accurate long-read alignment with Burrows-Wheeler transform.Crossref | GoogleScholarGoogle Scholar | 20080505PubMed |

Matheson A, Reid M (2018) ‘Practical Beekeeping in New Zealand.’ (Exisle Publishing: Dunedin, New Zealand)

Mattila HR, Burke KM, Seeley TD (2008) Genetic diversity within honeybee colonies increases signal production by waggle-dancing foragers. Proceedings. Biological Sciences 275, 809–816.
Genetic diversity within honeybee colonies increases signal production by waggle-dancing foragers.Crossref | GoogleScholarGoogle Scholar | 18198143PubMed |

Mattila HR, Reeve HK, Smith ML (2012) Promiscuous honey bee queens increase colony productivity by suppressing worker selfishness. Current Biology 22, 2027–2031.
Promiscuous honey bee queens increase colony productivity by suppressing worker selfishness.Crossref | GoogleScholarGoogle Scholar | 23022065PubMed |

Mondet F, De Miranda JR, Kretzschmar A, Le Conte Y, Mercer AR (2014) On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathogens 10, e1004323
On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor.Crossref | GoogleScholarGoogle Scholar | 25144447PubMed |

Moritz RFA (1981) Der Einfluss der Inzucht auf die Fitness der Drohnen von Apis mellifera carnica. [The Impact of Inbreeding on the Fitness of Drones of Apis Mellifera Carnica] Apidologie 12, 41–55.
Der Einfluss der Inzucht auf die Fitness der Drohnen von Apis mellifera carnica. [The Impact of Inbreeding on the Fitness of Drones of Apis Mellifera Carnica]Crossref | GoogleScholarGoogle Scholar | [in German]

New Zealand Ministry for Primary Industries (2020) Farm Monitoring Report NZ – Apiculture Report 2019. Ministry for Primary Industries, Wellington, New Zealand.

Nucleotide (1988) Accession No. QFDB01000000, Apis mellifera mellifera isolate:ACANBOUESSANT Genome sequencing and assembly. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information. Available at https://www.ncbi.nlm.nih.gov/nuccore/QFDB00000000.1 [Verified 20 February 2021]

Page RE, Metcalf RA (1982) Multiple mating, sperm utilization and social evolution. American Naturalist 119, 263–281.
Multiple mating, sperm utilization and social evolution.Crossref | GoogleScholarGoogle Scholar |

Palmer KA, Oldroyd BP (2000) Evolution of multiple mating in the genus Apis. Apidologie 31, 235–248.
Evolution of multiple mating in the genus Apis.Crossref | GoogleScholarGoogle Scholar |

Petersen GEL, Fennessy PF, van Stijn TC, Clarke SM, Dearden PK (2017) Genotyping-by-Sequencing for Genetic Improvement in honeybees. In ‘Proceedings of the 21st Conference of The Association for the Advancement of Animal Breeding and Genetics’, Townsville, Qld, Australia.

Petersen GEL, Fennessy PF, Van Stijn TC, Clarke SM, Dodds KG, Dearden PK (2020) Genotyping-by-sequencing of pooled drone DNA for the management of living honeybee (Apis mellifera) queens in commercial beekeeping operations in New Zealand. Apidologie
Genotyping-by-sequencing of pooled drone DNA for the management of living honeybee (Apis mellifera) queens in commercial beekeeping operations in New Zealand.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2018) R: a language and environment for statistical computing. Available at https://www.r-project.org/

van Engelsdorp D, Meixner MD (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology 103, S80–S95.
A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them.Crossref | GoogleScholarGoogle Scholar |

Van Raden PM (2008) Efficient methods to compute genomic predictions. Journal of Dairy Science 91, 4414–4423.
Efficient methods to compute genomic predictions.Crossref | GoogleScholarGoogle Scholar |

Vaziritabar S, Aghamirkarimi A, Esmaeilzade SM (2016) Evaluation of the defensive behaviour in two honeybee races Iranian honeybee (Apis mellifera meda) and Carniolan honeybee (Apis mellifera carnica) and grooming behaviour of different bee races in controlling Varroa destructor mite in honey bee colonies in. Journal of Entomology and Zoology Studies 4, 586–602.

Whitfield CW, Behura SK, Berlocher SH, Clark AG, Johnston JS, Sheppard WS, Smith DR, Suarez AV, Weaver DB, Tsutsui ND (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314, 642–645.
Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera.Crossref | GoogleScholarGoogle Scholar | 17068261PubMed |

Woyke J (1963) What happens to diploid drone larvae in a honeybee colony. Journal of Apicultural Research 2, 73–75.
What happens to diploid drone larvae in a honeybee colony.Crossref | GoogleScholarGoogle Scholar |

Zayed A (2009) Bee genetics and conservation. Apidologie 40, 237–262.
Bee genetics and conservation.Crossref | GoogleScholarGoogle Scholar |

Zayed A (2016) Evolution: insect invasions and natural selection. Nature 539, 500–502.
Evolution: insect invasions and natural selection.Crossref | GoogleScholarGoogle Scholar | 27820944PubMed |