Breeding for hygienic behavior in honey bees (Apis mellifera): a strong paternal effect

References

• Aizen, M. A., & Harder, L. D. (2009). The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Current Biology, 19(11), 915–918. https://doi.org/10.1016/j.cub.2009.03.071
   PubMed Web of Science ®Google Scholar
• Arathi, H. S., & Spivak, M. (2001). Influence of colony genotypic composition on the performance of hygienic behaviour in the honey bee Apis mellifera L. Animal Behavior, 62(1), 57–66. https://doi.org/10.1006/anbe.2000.1731
   Web of Science ®Google Scholar
• Baudry, E., Solignac, M., Garnery, L., Gries, M., Cornuet, J., & Koeniger, N. (1998). Relatedness among honeybees (Apis mellifera) of a drone congregation. Proceedings of the Royal Society of London. Series B: Biological Sciences, 265(1409), 2009–2014. https://doi.org/10.1098/rspb.1998.0533
   Web of Science ®Google Scholar
• Behrens, D., Huang, Q., Geßner, C., Rosenkranz, P., Frey, E., Locke, B., Moritz, R. F., & Kraus, F. B. (2011). Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor. Ecology and Evolution, 1(4), 451–458. https://doi.org/10.1002/ece3.17
   PubMed Web of Science ®Google Scholar
• Bigio, G., Al Toufailia, H., Hughes, W. O. H., & Ratnieks, F. L. W. (2014). The effect of one generation of controlled mating on the expression of hygienic behaviour in honey bees. Journal of Apicultural Research, 53(5), 563–568. https://doi.org/10.3896/IBRA.1.53.5.07
   Web of Science ®Google Scholar
• Blacquière, T., Boot, W., Calis, J., Moro, A., Neumann, P., & Panziera, D. (2019). Darwinian black box selection for resistance to settled invasive Varroa destructor parasites in honey bees. Biological Invasions, 21(8), 2519–2528. https://doi.org/10.1007/s10530-019-02001-0
   Web of Science ®Google Scholar
• Boecking, O., Bienefeld, K., & Drescher, W. (2000). Heritability of the Varroa-specific hygienic behaviour in honey bees (Hymenoptera: Apidae). Journal of Animal Breeding and Genetics, 117(6), 417–424. https://doi.org/10.1046/j.1439-0388.2000.00271.x
   Web of Science ®Google Scholar
• Boot, W. J., Calis, J. N. M., Beetsma, J., Hai, D. M., Lan, N. K., Toan, T. V., Trung, L. Q., & Minh, N. H. (1999). Natural selection of Varroa jacobsoni explains the different reproductive strategies in colonies of Apis cerana and Apis mellifera. Experimental & Applied Acarology, 23(2), 133–144. https://doi.org/10.1023/A:1006050527004
   Web of Science ®Google Scholar
• Boutin, S., Alburaki, M., Mercier, P.-L., Giovenazzo, P., & Derome, N. (2015). Differential gene expression between hygienic and non-hygienic honeybee (Apis mellifera L.) hives. BMC Genomics, 16, 500. https://doi.org/10.1186/s12864-015-1714-y
   PubMed Web of Science ®Google Scholar
• Brascamp, E. W., & Bijma, P. (2014). Methods to estimate breeding values in honey bees. Genetics, selection, evolution 46(1), 53. https://doi.org/10.1186/s12711-014-0053-9
   PubMed Web of Science ®Google Scholar
• Bubalo, D., Pechhacker, H., Licek, E., Kezic, N., & Sulimanovic, D. (2005). The effect of Varroa destructor infestation on flight activity and mating efficiency of drones (Apis mellifera L.). Vet. Med. Austria, 92, 11–15.
   Google Scholar
• Büchler, R., Androonov, S., Bienefeld, K., Costa, C., Hatjina, F., Kezic, N., Kryger, P., Spivak, M., Uzunov, A., & Wilde, J. (2013). Standard methods for rearing and selection of Apis mellifera queens. In Dietemann V, Ellis JD, and Neumann P (Eds), Coloss Beebook I: Standard Methods for Apis mellifera research. IBRA. https://doi.org/10.3896/IBRA.1.52.1.07
   Google Scholar
• Büchler, R., Berg, S., & Le Conte, Y. (2010). Breeding for resistance to Varroa destructor in Europe. Apidologie, 41(3), 393–408. https://doi.org/10.1051/apido/2010011
   Web of Science ®Google Scholar
• Büchler, R., Drescher, W., & Tornier, I. (1992). Grooming behaviour of Apis cerana, Apis mellifera and Apis dorsata and its effect on the parasitic mites Varroa jacobsoni and Tropilaelaps clareae. Experimental and Applied Acarology, 16(4), 313–319. https://doi.org/10.1007/BF01218573
   Web of Science ®Google Scholar
• Collins, A. M. (1986). Quantitative Genetics (pp. 426). Academic Press. Inc.
   Google Scholar
• de Mattos, I. M., de Jong, D., & Soares, A. E. E. (2016). Island population of European honeybees in Northeastern Brazil that have survived Varroa infestations for over 30 years. Apidologie, 47(6), 818–827. https://doi.org/10.1007/s13592-016-0439-5
   Web of Science ®Google Scholar
• Dietemann, V., Pflugfelder, J., Anderson, D., Charrière, J.-D., Chejanovsky, N., Dainat, B., de Miranda, J., Delaplane, K., Dillier, F.-X., Fuch, S., Gallmann, P., Gauthier, L., Imdorf, A., Koeniger, N., Kralj, J., Meikle, W., Pettis, J., Rosenkranz, P., Sammataro, D., … Neumann, P. (2012). Varroa destructor: Research avenues towards sustainable control. Journal of Apicultural Research, 51(1), 125–132. https://doi.org/10.3896/IBRA.1.51.1.15
   Web of Science ®Google Scholar
• Duay, P., De Jong, D., & Engels, W. (2002). Decreased flight performance and sperm production in drones of the honey bee (Apis mellifera) slightly infested by Varroa destructor mites during pupal development. Genetics and Molecular Research, 1(3), 227–232.
   PubMedGoogle Scholar
• Erez, T., Bonda, E., Cahanov, P., Rueppell, O., Wagoner K., Chejanovsky, N., & Soroker V. (2022). Multiple benefits of breeding honey bees for hygienic behavior. Journal of the Insect Pathology, 193. https://doi.org/10.1016/j.jip.2022.107788
   Google Scholar
• Estoup, A., Solignac, M., & Cornuet, J. M. (1994). Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies. Proceedings of the Royal Society B: Biological Sciences, 258, 1–7. https://doi.org/10.1098/rspb.1994.0133
   Web of Science ®Google Scholar
• Gallai, N., Salles, J. M., Settele, J., & Vaissière, B. E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics, 68(3), 810–821. https://doi.org/10.1016/j.ecolecon.2008.06.014
   Web of Science ®Google Scholar
• Glinski, Z., & Jarosz, J. (1984). Alterations in haemolymph proteins of drone honey bee larvae parasitized by Varroa jacobsoni. Apidologie, 15(3), 329–338. https://doi.org/10.1051/apido:19840305
   Web of Science ®Google Scholar
• Gray, A., Brodschneider, R., Adjlane, N., Ballis, A., Brusbardis, V., Charrière, J.-D., Chlebo, R., F. Coffey, M., Cornelissen, B., Amaro da Costa, C., Csáki, T., Dahle, B., Danihlík, J., Dražić, M. M., Evans, G., Fedoriak, M., Forsythe, I., de Graaf, D., Gregorc, A., … Soroker, V. (2019). Loss rates of honey bee colonies during winter 2017/18 in 36 countries participating in the COLOSS survey, including effects of forage sources. Journal of Apicultural Research, 58(4), 479–485. https://doi.org/10.1080/00218839.2019.1615661
   Web of Science ®Google Scholar
• Gray, A., Adjlane, N., Arab, A., Ballis, A., Brusbardis, V., Charrière, J.-D., Chlebo, R., Coffey, M. F., Cornelissen, B., Amaro da Costa, C., Dahle, B., Danihlík, J., Dražić, M. M., Evans, G., Fedoriak, M., Forsythe, I., Gajda, A., de Graaf, D. C., Gregorc, A., … Brodschneider, R. (2020). Honey bee colony winter loss rates for 35 countries participating in the COLOSS survey for winter 2018–2019, and the effects of a new queen on the risk of colony winter loss. Journal of Apicultural Research, 59(5), 744–751. https://doi.org/10.1080/00218839.2020.1797272
   Web of Science ®Google Scholar
• Harbo, J. R., & Harris, J. W. (1999). Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). Journal of Economic Entomology, 92(2), 261–265. https://doi.org/10.1093/jee/92.2.261
   Web of Science ®Google Scholar
• Harbo, J. R., & Harris, J. W. (2001). Resistance to Varroa destructor (Mesostigmata: Varroidae) when mite-resistant queen honey bees (Hymenoptera: Apidae) were free-mated with unselected drones. Journal of Economic Entomology, 94(6), 1319–1323. https://doi.org/10.1603/0022-0493-94.6.1319
   PubMed Web of Science ®Google Scholar
• Hoppe, A., Du, M., Bernstein, R., Tiesler, F. K., Kärcher, M., & Bienefeld, K. (2020). Substantial genetic progress in the international Apis mellifera carnica population since the implementation of genetic evaluation. Insects, 11(11), 768–786. https://www.mdpi.com/2075-4450/11/11/768 https://doi.org/10.3390/insects11110768
   PubMed Web of Science ®Google Scholar
• Jaffé, R., & Moritz, R. F. A. (2010). Mating flights select for symmetry in honeybee drones (Apis mellifera). Die Naturwissenschaften, 97(3), 337–343. https://doi.org/10.1007/s00114-009-0638-2
   PubMed Web of Science ®Google Scholar
• Jandricic, S. E., & Otis, G. W. (2003). The potential for using male selection in breeding honey bees resistant to Varroa destructor. Bee World, 84(4), 155–164. https://doi.org/10.1080/0005772X.2003.11099597
   Web of Science ®Google Scholar
• Jensen, A. B., Palmer, K. A., Chaline, N., Raine, N. E., Tofilski, A., Martin, S. J., Pedersen, B. V., Boomsma, J. J., & Ratnieks, F. L. (2006). Quantifying honey bee mating range and isolation in semi-isolated valleys by DNA microsatellite paternity analysis. Conservation Genetics, 6(4), 527–537. https://doi.org/10.1007/s10592-005-9007-7
   Web of Science ®Google Scholar
• Kefuss, J., Vanpoucke, J., Bolt, M., & Kefuss, C. (2015). Selection for resistance to Varroa destructor under commercial beekeeping conditions. Journal of Apicultural Research, 54(5), 563–576. https://doi.org/10.1080/00218839.2016.1160709
   Web of Science ®Google Scholar
• Koeniger, N., Koeniger, G., & Pechhacker, H. (2005). The nearer the better? Drones (Apis mellifera) prefer nearer drone congregation areas. Insectes Sociaux, 52(1), 31–35. https://doi.org/10.1007/s00040-004-0763-z
   Web of Science ®Google Scholar
• Kulincevic, J. M., Rinderer, T. E., Mladjan, V. J., & Buco, S. M. (1992). Five years of bi-directional genetic selection for honey bees resistant and susceptible to Varroa jacobsoni. Apidologie, 23(5), 443–452. https://doi.org/10.1051/apido:19920506
   Web of Science ®Google Scholar
• Kurze, C., Routtu, J., & Moritz, R. F. A. (2016). Parasite resistance and tolerance in honeybees at the individual and social level. Zoology (Jena, Germany), 119(4), 290–297. https://doi.org/10.1016/j.zool.2016.03.007
   PubMed Web of Science ®Google Scholar
• Laidlaw, HH. Jr, & Page, RE. Jr. (1986). Mating designs. Academic Press. Inc.
   Google Scholar
• Lapidge, K. L., Oldroyd, B. P., & Spivak, M. (2002). Seven suggestive quantitative trait loci influence hygienic behavior of honey bees. Die Naturwissenschaften, 89(12), 565–568. https://doi.org/10.1007/s00114-002-0371-6
   PubMed Web of Science ®Google Scholar
• Lin, Z., Qin, Y., Page, P., Wang, S., Li, L., Wen, Z., Hu, F., Neumann, P., Zheng, H., & Dietemann, V. (2018). Reproduction of parasitic mites Varroa destructor in original and new honeybee hosts. Ecology and Evolution, 8(4), 2135–2145. https://doi.org/10.1002/ece3.3802
   PubMed Web of Science ®Google Scholar
• Maucourt, S., Fortin, F., Robert, C., & Giovenazzo, P. (2020). Genetic parameters of honey bee colonies traits in a Canadian selection program. Insects, 11(9), 587. https://doi.org/10.3390/insects11090587
   PubMed Web of Science ®Google Scholar
• Meixner, M. D., Kryger, P., & Costa, C. (2015). Effects of genotype, environment, and their interactions on honey bee health in Europe. Current Opinion in Insect Science, 10, 177–184. https://doi.org/10.1016/j.cois.2015.05.010
   PubMed Web of Science ®Google Scholar
• Milne, C. P. (1985). Estimates of the heritability of and genetic correlation between two components of honey bee (Hymenoptera: Apidae). Hygienic behavior: Uncapping and removing. Annals of the Entomological Society of America, 78(6), 841–844. https://doi.org/10.1093/aesa/78.6.841
   Web of Science ®Google Scholar
• Mondet, F., Alaux, C., Severac, D., Rohmer, M., Mercer, A. R., & Le Conte, Y. (2015). Antennae hold a key to Varroa-sensitive hygiene behaviour in honey bees. Scientific Reports, 5, 10454. https://doi.org/10.1038/srep10454
   PubMed Web of Science ®Google Scholar
• Nganso, B. T., Fombong, A. T., Yusuf, A. A., Pirk, C. W., Stuhl, C., & Torto, B. (2017). Hygienic and grooming behaviors in African and European honeybees—New damage categories in Varroa destructor. PLoS One, 12(6), e0179329. https://doi.org/10.1371/journal.pone.0179329
   PubMed Web of Science ®Google Scholar
• Oxley, P. R., & Oldroyd, B. P. (2010). The genetic architecture of honeybee breeding. Advances in Insect Physiology, 39, 83–118. https://doi.org/10.1016/B978-0-12-381387-9.00003-8
   Web of Science ®Google Scholar
• Oxley, P. R., Hinhumpatch, P., Gloag, R., & Oldroyd, B. P. (2010a). Genetic evaluation of a novel system for controlled mating of the honeybee, Apis mellifera. The Journal of Heredity, 101(3), 334–338. https://doi.org/10.1093/jhered/esp112
   PubMed Web of Science ®Google Scholar
• Oxley, P. R., Spivak, M., & Oldroyd, B. P. (2010b). Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Molecular Ecology, 19(7), 1452–1461. https://doi.org/10.1111/j.1365-294X.2010.04569.x
   PubMed Web of Science ®Google Scholar
• Page, P., Lin, Z., Buawangpong, N., Zheng, H., Hu, F., Neumann, P., Chantawannakul, P., & Dietemann, V. (2016). Social apoptosis in honey bee superorganisms. Scientific Reports, 6, 27210. https://doi.org/10.1038/srep27210
   PubMed Web of Science ®Google Scholar
• Peng, Y. S., Fang, Y., Xu, S., & Ge, L. (1987). The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans. Journal of Invertebrate Pathology, 49(1), 54–60. https://doi.org/10.1016/0022-2011(87)90125-X
   Web of Science ®Google Scholar
• Pérez-Sato, J. A., Châline, N., Martin, S. J., Hughes, W. O., & Ratnieks, F. L. (2009). Multi-level selection for hygienic behaviour in honeybees. Heredity, 102(6), 609–615. https://doi.org/10.1038/hdy.2009.20
   PubMed Web of Science ®Google Scholar
• Pernal, S. F., Sewalem, A., & Melathopoulos, A. P. (2012). Breeding for hygienic behaviour in honeybees (Apis mellifera) using free-mated nucleus colonies. Apidologie, 43(4), 403–416. https://doi.org/10.1007/s13592-011-0105-x
   Web of Science ®Google Scholar
• Plate, M., Bernstein, R., Hoppe, A., & Bienefeld, K. (2019). The importance of controlled mating in honeybee breeding. Genetics, Selection, Evolution, 51(1), 74. https://doi.org/10.1186/s12711-019-0518-y
   PubMed Web of Science ®Google Scholar
• Rangel, J., Traver, B., Stoner, M., Hatter, A., Trevelline, B., Garza, C., Shepherd, T., Seeley, T. D., & Wenzel, J. (2020). Genetic diversity of wild and managed honey bees (Apis mellifera) in Southwestern Pennsylvania, and prevalence of the microsporidian gut pathogens Nosema ceranae and N. apis. Apidologie, 51(5), 802–814. https://doi.org/10.1007/s13592-020-00762-5
   Web of Science ®Google Scholar
• Rath, W. (1999). Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie, 30(2–3), 97–110. https://doi.org/10.1051/apido:19990202
   Web of Science ®Google Scholar
• Robertson, A. J., Trost, B., Scruten, E., Robertson, T., Mostajeran, M., Connor, W., Kusalik, A., Griebel, P., & Napper, S. (2014). Identification of developmentally-specific kinotypes and mechanisms of Varroa mite resistance through whole-organism, kinome analysis of honeybee. Frontiers in Genetics, 5, 139. https://doi.org/10.3389/fgene.2014.00139
   PubMed Web of Science ®Google Scholar
• Rosenkranz, P., Aumeier, P., & Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103, S96–S119. https://doi.org/10.1016/j.jip.2009.07.016
   PubMed Web of Science ®Google Scholar
• Rothenbuhler, W. C. (1964). Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood. Animal Behaviour, 12(4), 578–583. https://doi.org/10.1016/0003-3472(64)90082-X
   Web of Science ®Google Scholar
• Saltelli, A. (2002). Sensitivity analysis for importance assessment. Risk Analysis: An Official Publication of the Society for Risk Analysis, 22(3), 579–590. https://doi.org/10.1111/0272-4332.00040
   PubMed Web of Science ®Google Scholar
• Sammataro, D., & Avitabile, A. (2011). The beekeeper’s handbook (4th ed.). Comstock Pub. Associates, Ithaca. Cornell University Press.
   Google Scholar
• Seltzer, R., Cahanov, P., Kamer, Y., Hetzroni, A., Bieńkowska, M., Hefetz, A., & Soroker, V. (2021). The payoffs and tradeoffs of hygienic behavior: A five year field study on a local population of honey bees. Journal of Apicultural Research, 61, 492–501. https://doi.org/10.1080/00218839.2022.2048947
   Web of Science ®Google Scholar
• Spivak, M., & Danka, R. G. (2021). Perspectives on hygienic behavior in Apis mellifera and other social insects. Apidologie, 52(1), 1–16. https://doi.org/10.1007/s13592-020-00784-z
   Web of Science ®Google Scholar
• Tarpy, D. R., Nielsen, R., & Nielsen, D. I. (2004). A scientific note on the revised estimates of effective paternity frequency in Apis. Insectes Sociaux, 51(2), 203–204. https://doi.org/10.1007/s00040-004-0734-4
   Web of Science ®Google Scholar
• Traynor, K. S., Mondet, F., de Miranda, J. R., Techer, M., Kowallik, V., Oddie, M. A. Y., Chantawannakul, P., & McAfee, A. (2020). Varroa destructor: A complex parasite, crippling honey bees worldwide. Trends in Parasitology, 36(7), 592–606. https://doi.org/10.1016/j.pt.2020.04.004.
   PubMed Web of Science ®Google Scholar
• Tsuruda, J. M., Harris, J. W., Bourgeois, L., Danka, R. G., & Hunt, G. J. (2012). High-resolution linkage analyses to identify genes that influence Varroa sensitive hygiene behavior in honey bees. PLoS One, 7(11), e48276. https://doi.org/10.1371/journal.pone.0048276
   PubMed Web of Science ®Google Scholar
• Unger, P., & Guzmán-Novoa, E. (2010). Maternal effects on the hygienic behavior of Russian X Ontario hybrid honeybees (Apis mellifera L.). The Journal of Heredity, 101(1), 91–96. https://doi.org/10.1093/jhered/esp092
   PubMed Web of Science ®Google Scholar
• Utaipanon, P., Holmes, M. J., Chapman, N. C., & Oldroyd, B. P. (2019). Estimating the density of honey bee (Apis mellifera) colonies using trapped drones: Area sampled and drone mating flight distance. Apidologie, 50(4), 578–592. https://doi.org/10.1007/s13592-019-00671-2
   Web of Science ®Google Scholar
• Wang, S., Lin, Z., Chen, G., Page, P., Hu, F., Niu, Q., Su, X., Chantawannakul, P., Neumann, P., Zheng, H., & Dietemann, V. (2020). Reproduction of ectoparasitic mites in a coevolved system: Varroa spp.–Eastern honey bees, Apis cerana. Ecology and Evolution, 10(24), 14359–14371. https://doi.org/10.1002/ece3.7038
   PubMed Web of Science ®Google Scholar
• Yañez, O., Jaffé, R., Jarosch, A., Fries, I., Moritz, R. F. A., Paxton, R. J., & de Miranda, J. R. (2011). Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): Implications for sexual transmission of a major honey bee virus. Apidologie, 43(1), 17–30. https://doi.org/10.1007/s13592-011-0088-7
   Web of Science ®Google Scholar