References

vavilov

Вавиловский журнал генетики и селекции

Vavilov Journal of Genetics and Breeding

2500-3259

Institute of Cytology and Genetics of Siberian Branch of the RAS

10.18699/VJ20.683

vavilov-2845

Research Article

ГЕНЕТИКА И СЕЛЕКЦИЯ РАСТЕНИЙ НА ИММУНИТЕТ, КАЧЕСТВО, ПРОДУКТИВНОСТЬ И СТРЕССОУСТОЙЧИВОСТЬ

ANIMAL GENETICS AND BREEDING

Генетические маркеры резистентности медоносной пчелы к Varroa destructor

Genetic markers for the resistance of honey bee to Varroa destructor

https://orcid.org/0000-0003-4960-6559

Каскинова

М. Д.

Kaskinova

M. D.

kaskinovamilyausha@mail.ru

https://orcid.org/0000-0002-3285-118X

Гайфуллина

Л. Р.

Gaifullina

L. R.

https://orcid.org/0000-0003-0123-7037

Салтыкова

Е. С.

Saltykova

E. S.

https://orcid.org/0000-0001-6189-4472

Поскряков

А. В.

Poskryakov

A. V.

https://orcid.org/0000-0002-9235-680X

Николенко

А. Г.

Nikolenko

A. G.

Институт биохимии и генетики – обособленное структурное подразделение Уфимского федерального исследовательского центра Российской академии наукРоссияInstitute of Biochemistry and Genetics – Subdivision of the Ufa Federal Research Center of the Russian Academy of SciencesRussian Federation

2020

31122020

248853860

2020

Каскинова М.Д., Гайфуллина Л.Р., Салтыкова Е.С., Поскряков А.В., Николенко А.Г.

Kaskinova M.D., Gaifullina L.R., Saltykova E.S., Poskryakov A.V., Nikolenko A.G.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://vavilov.elpub.ru/jour/article/view/2845

В середине ХХ в. был зафиксирован первый случай заражения европейских пчел Apis mellifera L. клещом-эктопаразитом Varroa destructor, изначальным хозяином которого является азиатская пчела Apis cerana. Клещ распространился по всей Европе, Северной и Южной Америке, и единственным континентом, свободным от этого паразита, осталась Австралия. Без обработки акарицидами семья медоносной пчелы погибает в течение 1–4 лет. Использование синтетических акарицидов не оправдало себя – они делают непригодными продукты пчеловодства и у клещей возникает к ним резистентность, что заставляет использовать еще большие концентрации препаратов, которые могут быть токсичны для пчел. Единственная безопасная мера борьбы – использование методов биологического контроля. Одним из таких методов является селекция семей пчел, обладающих естественной резистентностью к клещу. В обзоре обобщены публикации, посвященные поиску генетических маркеров, ассоциированных с устойчивостью к V. destructor. Рассматриваются основные механизмы устойчивости пчел к клещу (Varroa-чувствительное гигиеническое поведение и груминг) и методы их оценки. Обсуждаются исследования, направленные на поиск локусов и генов-кандидатов, ассоциированных с устойчивостью к варроатозу, при помощи картирования локусов количественных признаков и полногеномного поиска ассоциаций. Обобщены исследования транскриптомного профиля Varroa-устойчивых пчел. Рассмотрены наиболее вероятные гены-кандидаты – потенциальные маркеры для селекции Varroa-резистентных пчел. Резистентность к клещу проявляется в виде разнообразных фенотипов и находится под полигенным контролем. Установление генных путей, задействованных в механизме резистентности к Varroa, поможет создать методологическую базу для селекции устойчивых к варроатозу семей A. mellifera.

In the mid-20th century, the first case of infection of European bees Apis mellifera L. with the ectoparasite mite Varroa destructor was recorded. The original host of this mite is the Asian bee Apis cerana. The mite V. destructor was widespread throughout Europe, North and South America, and Australia remained the only continent free from this parasite. Without acaricide treatment any honeybee colony dies within 1–4 years. The use of synthetic acaricides has not justified itself – they make beekeeping products unsuitable and mites develop resistance to them, which forces the use of even greater concentrations that can be toxic to the bees. Therefore, the only safe measure to combat the mite is the use of biological control methods. One of these methods is the selection of bee colonies with natural mite resistance. In this article we summarize publications devoted to the search for genetic markers associated with resistance to V. destructor. The first part discusses the basic mechanisms of bee resistance (Varroa sensitive hygienic behavior and grooming) and methods for their assessment. The second part focuses on research aimed at searching for loci and candidate genes associated with resistance to varroosis by mapping quantitative traits loci and genome-wide association studies. The third part summarizes studies of the transcriptome profile of Varroa resistant bees. The last part discusses the most likely candidate genes – potential markers for breeding Varroa resistant bees. Resistance to the mite is manifested in a variety of phenotypes and is under polygenic control. The establishing of gene pathways involved in resistance to Varroa will help create a methodological basis for the selection of Varroa resistant honeybee colonies.

Apis melliferaVarroa destructorVarroa-резистентностьмаркер-опосредованная селекция

Apis melliferaVarroa destructorVarroa resistancemarker-assisted selection

References1

Albo G.N., Cordoba S.B., Reynaldi F.J. Chalkbrood: pathogenesis and the interaction with honeybee defenses. Int. J. Envir. Agric. Res. 2017;3(1):71-80.

Anderson D.L., Trueman J.W.H. Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp. Appl. Acarol. 2000;24:165-189. DOI 10.1023/A:1006456720416.

Arathi S., Burns I., Spivak M. Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. Ethology. 2003;106:365-379. DOI 10.1046/j.1439-0310.2000.00556.x.

Arechavaleta-Velasco M.E., Alcala-Escamilla K., Robles-Rios C., Tsuruda J.M., Hunt G.J. Fine-scale lingkage mapping reveals a small set of candidate genes influencing honey bee grooming behavior in response to Varroa mites. PLoS One. 2012;7:e47269. DOI 10.1371/journal.pone.0047269.

Aumeier P. Bioassay for grooming effectiveness towards Varroa destructor mites in Africanized and Carniolan honey bees. Apidologie. 2001;32:81-90. DOI 10.1051/apido:2001113.

Beggs K.T., Mercer A.R. Dopamine receptor activation by honey bee queen pheromone. Curr. Biol. 2009;19:1206-1209. DOI 10.1016/j.cub.2009.05.051.

Behrens D., Huang Q., Geßner C., Rosenkranz P., Frey E., Locke B., Moritz R.F.A., Kraus F.B. Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor. Ecol. Evol. 2011;1(4):451-458. DOI 10.1002/ece3.17.

Bienefeld K. Recording the proportion of damaged Varroa jacobsoni Oud. in the debris of honey bee colonies (Apis mellifera). Apidologie. 1999;30:249-256.

Boecking O., Spivak M. Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie. 1999;30:141-158. DOI 10.1051/apido:19990205.

Boutin S., Alburaki M., Mercier P.-L., Giovenazzo P., Derome N. Differential gene expression between hygienic and non-hygienic honeybee (Apis mellifera L.) hives. BMC Genom. 2015;16:500. DOI 10.1186/s12864-015-1714-y.

Calderon R.A., van Veen J.W., Sommeijer M.J., Sanchez L.A. Reproductive biology of Varroa destructor in Africanized honey bees (Apis mellifera). Exp. Appl. Acarol. 2010;50(4):281-297. DOI 10.1007/s10493-009-9325-4.

Chandler D., Sunderland K.D., Ball B.V., Davidson G. Prospective biological control agents of Varroa destructor n. sp., an important pest of the European honeybee, Apis mellifera. Biocontrol Sci. Technol. 2001;11(4):429-448. DOI 10.1080/09583150120067472.

Conlon B.H., Aurori A., Giurgiu A.I., Kefuss J., Dezmirean D.S., Moritz R.F.A., Routtu J. A gene for resistance to the Varroa mite (Acari) in honey bee (Apis mellifera) pupae. Mol. Ecol. 2019; 28(12):2958-2966. DOI 10.1111/mec.15080.

Conlon B.H., Frey E., Rosenkranz P., Locke B., Moritz R.F.A., Routtu J. The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones. J. Evol. Biol. 2018;31:801-809. DOI 10.1111/jeb.13271.

Danka R.G., Harris J.W., Villa J.D., Dodds G. Varying congruence of hygienic responses to Varroa destructor and freeze-killed brood among different types of honeybees. Apidologie. 2013;44:447- 457. DOI 10.1007/s13592-013-0195-8.

Darvasi A., Soller M. A simple method to calculate resolving power and confidence interval of QTL map location. Behav. Genet. 1997; 27:125-132. DOI 10.1023/A:1025685324830.

Diao Q., Sun L., Zheng H., Zeng Z., Wang S., Xu S., Zheng H., Chen Y., Shi Y., Wang Y., Meng F., Sang Q., Cao L., Liu F., Zhu Y., Li W., Li Z., Dai C., Yang M., Chen S., Chen R., Zhang S., Evans J.D., Huang Q., Liu J., Hu F., Su S., Wu J. Genomic and transcriptomic analysis of the Asian honeybee Apis cerana provides novel insights into honeybee biology. Sci. Rep. 2018;8:822. DOI 10.1038/s41598-017-17338-6.

Dietemann V., Pflugfelder J., Anderson D., Charriere J.D., Chejanovsky N., Dainat B., de Miranda J.R., Delaplane K.S., Dillier F.-X., Fuch S., Gallmann P., Gauthier L., Imdorf A., Koeniger N., Kralj J., Meikle W.G., Pettis J.S., Rosenkranz P., Sammataro D., Smith D.R., Yañez O., Neumann P.J. Varroa destructor: research avenues towards sustainable control. J. Apic. Res. 2012;51(1):125-132. DOI 10.3896/IBRA.1.51.1.15.

Dolezelova E., Nothacker H.-P., Civelli O., Bryant P.J., Zurovec M. Drosophila adenosine receptor activates cAMP and calcium signaling. Insect Biochem. Mol. Biol. 2007;37(4):318-329. DOI 10.1016/j.ibmb.2006.12.003.

Evans J.D., Cook S.C. Genetics and physiology of Varroa mites. Curr. Opin. Insect Sci. 2018;26:130-135. DOI 10.1016/j.cois.2018.02.005.

Facchini E., Bijma P., Pagnacco G., Rizzi R., Brascamp E.W. Hygienic behaviour in honeybees: a comparison of two recording methods and estimation of genetic parameters. Apidologie. 2019; 50:163-172. DOI 10.1007/s13592-018-0627-6.

Feyereisen R. Insect p450 enzymes. Annu. Rev. Entomol. 1999;44: 507-533. DOI 10.1146/annurev.ento.44.1.507.

Fries I., Huazhen W., Jin C.S., Wei S. Grooming behavior and damaged mites (Varroa jacobsoni) in Apis cerana cerana and Apis mellifera ligustica. Apidologie. 1996;27:3-11. DOI 10.1051/apido:19960101.

Gilliam M., Taber S., Richardson G.V. Hygienic behavior of honey bees in relation to chalkbrood disease. Apidologie. 1983;14: 29-39.

Gramacho K.P., Gonçalves L.S., Rosenkranz P., Jong D.D. Influence of body fluid from pin-killed honey bee pupae on hygienic behavior. Apidologie. 1999;30:367-374. DOI 10.1051/apido:19990502.

Haddad N., Batainh A.M., Migdadi O.S., Saini D., Krishnamurthy V., Parameswaran S., Alhamuri Z. Next generation sequencing of Apis mellifera syriaca identifies genes for Varroa resistance and beneficial bee keeping traits. Insect Sci. 2015;23:1-12. DOI 10.1111/1744-7917.12205.

Hamiduzzaman M.Md., Emsen B., Hunt G.J., Subramanyam S., Williams C.E., Tsuruda J.M., Guzman Novoa E. Differential gene expression associated with honey bee grooming behavior in response to Varroa mites. Behav. Genet. 2017;47:335-344. DOI 10.1007/s10519-017-9834-6.

Harbo J.R., Harris J.W. Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae). J. Econ. Entomol. 1999;92: 261-265.

Harbo J.R., Harris J.W. Suppressed mite reproduction explained by the behaviour of adult bees. J. Apic. Res. 2005;44(1):21-23. DOI 10.1080/00218839.2005.11101141.

Harpur B.A., Guarna M.M., Huxter E., Higo H., Moon K.-M., Hoover S.E., Ibrahim А., Melathopoulos A.P., Desai S., Currie R.W., Pernal S.F., Foster L.J., Zayed A. Integrative genomics reveals the genetics and evolution of the honey bee’s social immune system. Genome Biol. Evol. 2019;11(3):937-948. DOI 10.1093/gbe/evz018.

Harris J. Bees with Varroa sensitive hygiene preferentially remove mite infested pupae aged ≤ five days post capping. J. Apic. Res. 2007;46:134-139. DOI 10.3896/IBRA.1.46.3.02.

Harris J.W., Danka R.G., Villa J.D. Honey bees (Hymenoptera: Apidae) with the trait of varroa sensitive hygiene remove brood with all reproductive stages of varroa mites (Mesostigmata: Varroidae). Ann. Entomol. Soc. Am. 2010;103:146-152. DOI 10.1603/AN09138.

Hu H., Bienefeld K., Wegener J., Zautke F., Hao Y., Feng M., Han B., Fang Y., Wubie A.J., Li J. Proteome analysis of the hemolymph, mushroom body, and antenna provides novel insight into honeybee resistance against varroa infestation. J. Proteome Res. 2016;15(8): 2841-2854. DOI 10.1021/acs.jproteome.6b00423.

Invernizzi C., Zefferinoa I., Santosa E., Sanchez L., Mendoza Y. Multilevel assessment of grooming behavior against Varroa destructor in Italian and Africanized honey bees. J. Apic. Res. 2015; 54(4):321-327. DOI 10.1080/00218839.2016.1159055.

Ji T., Yin L., Liu Z., Liang Q., Luo Y., Shen J., Shen F. Transcriptional responses in eastern honeybees (Apis cerana) infected with mites, Varroa destructor. Genet. Mol. Res. 2014;13(4):8888-8900. DOI 10.4238/2014.October.31.4.

Jiang S., Robertson T., Mostajeran M., Robertson A.J., Qiu X. Differential gene expression of two extreme honey bee (Apis mellifera) colonies showing Varroa tolerance and susceptibility. Insect Mol. Biol. 2016;25(3):272-282. DOI 10.1111/imb.12217.

Kamler M., Nesvorna M., Stara J., Erban T., Hubert J. Comparison of tau-fluvalinate, acrinathrin, and amitraz effects on susceptible and resistant populations of Varroa destructor in a vial test. Exp. Appl. Acarol. 2016;69(1):1-9. DOI 10.1007/s10493-016-0023-8.

Kim J.S., Kim M.J., Kim H.-K., Vung N.N., Kim I. Development of single nucleotide polymorphism markers specific to Apis mellifera (Hymenoptera: Apidae) line displaying high hygienic behavior against Varroa destructor, an ectoparasitic mite. J. Asia Pac. Entomol. 2019;22:1031-1039. DOI 10.1016/j.aspen.2019.08.005.

Kurze C., Routtu J., Moritz R.F.A. Parasite resistance and tolerance in honeybees at the individual and social level. Zoology. 2016; 119(4):290-297. DOI 10.1016/j.zool.2016.03.007.

лLand B., Seeley T. The grooming invitation dance of the honey bee. Ethology. 2004;110:1-10. DOI 10.1046/j.1439-0310.2003.00947.x.

Lartigue A., Gruez A., Briand L., Blon F., Bezirard V., Walsh M., Pernollet J.-C., Tegoni M., Cambillau C. Sulfur single-wavelength anomalous diffraction crystal structure of a pheromone-binding protein from the honeybee Apis mellifera L. J. Biol. Chem. 2004; 279(6):4459-4464. DOI 10.1074/jbc.M311212200.

Lattorff H.M.G., Buchholz J., Fries I., Moritz R.F.A. A selective sweep in a Varroa destructor resistant honeybee (Apis mellifera) population. Infect. Genet. Evol. 2015;31:169-176. DOI 10.1016/j.meegid.2015.01.025.

Le Conte Y., Alaux C., Martin J.-F., Harbo J.R., Harris J.W., Dantec C., Severac D., Cros-Arteil S., Navajas M. Social immunity in honeybees (Apis mellifera): transcriptome analysis of varroahygienic behaviour. Insect Mol. Biol. 2011;20(3):399-408. DOI 10.1111/j.1365-2583.2011.01074.x.

Leclercq G., Pannebakker B., Gengler N., Nguyen B.K., Francis F. Drawbacks and benefits of hygienic behavior in honey bees (Apis mellifera L.): a review. J. Apic. Res. 2017;56(4):366-375. DOI 10.1080/00218839.2017.1327938.

Locke B. Inheritance of reduced Varroa mite reproductive success in reciprocal crosses of mite-resistant and mite-susceptible honey bees (Apis mellifera). Apidologie. 2016a;47(4):583-588. DOI 10.1007/s13592-015-0403-9.

Locke B. Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie. 2016b;47(3):467-482. DOI 10.1007/s13592-015-0412-8.

Martin S.J., Highfield A.C., Brettell L., Villalobos E.M., Budge G.E., Powell M. Global honey bee viral landscape altered by a parasitic mite. Science. 2012;336(6086):1304-1306. DOI 10.1126/science.1220941.

McDonnellC.M., AlauxC., Parrinello H., DesvignesJ.-P., Crauser D., DurbessonE., BeslayD., LeConteY. Ecto- and endoparasite induce similar chemical and brain neurogenomic responses in the honey bee (Apis mellifera). BMC Ecol. 2013;13:25. DOI 10.1186/1472-6785-13-25.

Mondet F., Alaux C., Severac D., Rohmer M., Mercer A.R., Conte Y.L. Antennae hold a key to Varroa sensitive hygiene behaviour in honey bees. Sci. Rep. 2015;5:10454. DOI 10.1038/srep10454.

Navajas M., Migeon A., Alaux C., Martin-Magniette M.L., Robinson G.E., Evans J.D., Cros-Arteil S., Crauser D., Le Conte Y. Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genom. 2008;9:301. DOI 10.1186/1471-2164-9-301.

Nazzi F., Le Conte Y., Berenbaum M.R. Ecology of Varroa destructor, the major ectoparasite of the western honey bee, Apis mellifera. Annu. Rev. Entomol. 2016;61:417-432. DOI 10.1146/annurev-ento-010715-023731.

Oxley P.R., Spivak M., Oldroyd B.P. Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Mol. Ecol. 2010;19:1452-1461. DOI 10.1111/j.1365-294X.

Plettner E., Eliash N., Singh N.K., Pinnelli G.R., Soroker V. The chemical ecology of host-parasite interaction as a target of Varroa destructor control agents. Apidologie. 2017;48(1):78-92. DOI 10.1007/s13592-016-0452-8.

Pritchard D.J. Grooming by honey bees as a component of varroa resistant behavior. J. Apic. Res. 2016;55(1):38-48. DOI 10.1080/00218839.2016.1196016.

Rosenkranz P., Aumeier P., Ziegelmann B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 2010;103:S96-119. DOI 10.1016/j.jip.2009.07.016.

Rothenbuhler W.C. Behavior genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood. Am. Zool. 1964;4:111-123.

Spivak M. Honey bee hygienic behavior and defense against Varroa jacobsoni. Apidologie. 1996;27:245-260. DOI 10.1051/apido:19960407.

Spivak M., Reuter G.S. Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior. Apidologie. 2001;32:555-565.

Spotter A., Gupta P., Mayer M., Reinsch N., Bienefeld K. Genomewide association study of a Varroa-specific defense behavior in honeybees (Apis mellifera). J. Hered. 2016;107(3):220-227. DOI 10.1093/jhered/esw005.

Spotter A., Gupta P., Nurnberg G., Reinsch N., Bienefeld K. Development of a 44K SNP assay focussing on the analysis of a varroa-specific defence behaviour in honey bees (Apis mellifera carnica). Mol. Ecol. Resour. 2012;12:323-332. DOI 10.1111/j.1755-0998.2011.03106.x.

Suenami S., Iino S., Kubo T. Pharmacologic inhibition of phospholipase C in the brain attenuates early memory formation in the honeybee (Apis mellifera L.). Biol. Open. 2018;7:bio028191. DOI 10.1242/bio.028191.

Tsuruda J.M., Harris J.W., Bourgeois L., Danka R.G., Hunt G.J. High-resolution linkage analyses to identify genes that influence Varroa sensitive hygiene behavior in honey bees. PLoS One. 2012; 7(11):e48276. DOI 10.1371/journal.pone.0048276.

Villa J.D., Danka R.G., Harris J.W. Simplified methods of evaluating colonies for levels of Varroa Sensitive Hygiene (VSH). J. Apic. Res. 2009;48(3):162-167. DOI 10.3896/IBRA.1.48.3.03.

Wallberg A., Schoning C., Webster M.T., Hasselmann M. Two extended haplotype blocks are associated with adaptation to high altitude habitats in East African honey bees. PLoS Genet. 2017; 13(5):e1006792. DOI 10.1371/journal.pgen.1006792.

Zakar E., Javor A., Kusza S. Genetic bases of tolerance to Varroa destructor in honey bees (Apis mellifera L.). Insect. Soc. 2014;61: 207-215. DOI 10.1007/s00040-014-0347-5.

Zhao G., Wang C., Wang H., Gao L., Liu Z., Xu B., Guo X. Characterization of the CDK5 gene in Apis cerana cerana (AccCDK5) and a preliminary identification of its activator gene, AccCDK5r1. Cell Stress Chaperones. 2018;23:13-28. DOI 10.1007/s12192-017-0820-y.

The authors declare that there are no conflicts of interest present.