Türkiye’deki beş bal arısı, Apis mellifera L., 1758 (Hymenoptera: Apidae) ırkında tımar davranışı ile ilgili neuroxin-1, ataxin-3 ve atlastin genlerinin kantitasyonu

Öz

Varroa destructor Anderson & Trueman, 2000 (Acari: Varroidae) kontrolünde birçok yöntem kullanılmış olmasına rağmen, tatmin edici sonuçlar henüz elde edilememiştir. Araştırmalar, bazı bal arısı, Apis mellifera L., 1758 (Hymenoptera: Apidae) kolonilerinin Varroa akarlarına diğerlerinden daha yüksek direnç veya duyarlılık sergilediğini göstermiştir. Genetik temele dayanan direnç mekanizmalarından birisi de tımar davranışıdır ve arıcılık için umut vericidir. Tımar davranışı ile ilgili cevaplanmamış birçok sorunun olması bu çalışmanın ortaya çıkmasına neden olmuştur. Türkiye'deki beş bal arısı ırkından işçi arıların V. destructor istilasına tepki olarak tımar davranışları test edilmiştir. Tımar davranışı gösteren ve göstermeyen her bir bal arısı ırkında üç aday genin (neuroxin-1, ataxin-3 ve atlastin) ekspresyon seviyelerinin kantitasyonu kantitatif polimeraz zincir reaksiyonu yöntemi ile değerlendirilmiştir. Neuroxin-1, ataxin-3 ve atlastin genlerinin ekspresyon seviyeleri önemli farklılıklar gösterse de Suriye ırkı haricinde tımar davranışı bu genlerin ekspresyon seviyeleri ile ilişkili bulunmamıştır. Ayrıca fenotipik olarak bal arısı ırkları arasında tımar davranışı açısından istatistiksel farklılık bulunmamıştır. Elde edilen sonuçlar, tımar davranışının, tek başına nöral gen ifadeleriyle ilişkili olmayabileceğini göstermektedir. Bununla birlikte tımar davranışı ile ilgili daha fazla moleküler çalışmaya ihtiyaç duyulduğu görülmektedir.

Anahtar Kelimeler

• Apis mellifera
• aday gen
• tımar davranışı
• kantitasyon
• Varroa destructor

Quantitation of neuroxin-1, ataxin-3 and atlastin genes related to grooming behavior in five races of honey bee, Apis mellifera L., 1758 (Hymenoptera: Apidae), in Turkey

Abstract

Although many methods have been used to control Varroa destructor Anderson & Trueman, 2000 (Acari: Varroidae), the satisfactory results have not yet been achieved. However, research has shown that some colonies of honey bee, Apis mellifera L., 1758 (Hymenoptera: Apidae), exhibit higher resistance or sensitivity to Varroa mites than others. One of the resistance mechanisms based on genetics is grooming behavior and it has been promising for beekeeping. The fact that there are many unanswered questions about grooming behavior led to the idea of this study. Worker bees from five honey bee races in Turkey were individually tested for their grooming behavior in response to V. destructor mite infestation. The quantitation of the expression levels of three candidate genes (neurexin-1, ataxin-3 and atlastin) in each honey bee race with and without grooming behavior was evaluated by quantitative polymerase chain reaction. Although expression levels of neurexin-1, ataxin-3 and atlastin genes showed significant differences among individuals, grooming levels of individuals were not related to the expression levels of these genes except in Syrian honeybees. Also, phenotypically no statistical differences were found among the honey bee races in terms of grooming behavior. The results show that grooming behavior may not be associated with neural gene expression alone. However, it is seen that more molecular studies related to grooming behavior are needed.

Keywords

• Apis mellifera
• candidate gene
• grooming behavior
• quantitation
• Varroa destructor

References

1. Andino, G. K. & G. J. Hunt, 2011. A scientific note on a new assay to measure honey bee mite-grooming behavior. Apidologie, 42 (4): 481-484.
2. Arechavaleta-Velasco, M. E., K. Alcala-Escamilla, C. Robles-Rios, J. M. Tsuruda & G. J. Hunt, 2012. Fine-scale linkage mapping reveals a small set of candidate genes influencing honey bee grooming behavior in response to Varroa mites. PLoS One, 7 (11): e47269.
3. Arechavaleta-Velasco, M. E. & E. Guzman-Novoa, 2001. Relative effect of four characteristics that restrain the population growth of the mite Varroa destructor in honey bee (Apis mellifera) colonies. Apidologie, 32 (2): 157-174.
4. Aumeier, P., 2000. Grooming as a tolerance factor against Varroa jacobsoni: a critical assessment on Africanized bees. Apidologie, 31 (5): 633-634.
5. Aumeier, P., 2001. Bioassay for grooming effectiveness towards Varroa destructor mites in Africanized and Carniolan honey bees. Apidologie, 32 (1): 81-90.
6. Bak, B. & J. Wilde, 2015. Grooming behavior by worker bees of various subspecies of honey bees to remove Varroa destructor mites. Journal of Apicultural Research, 54 (3): 207-215.
7. Bodur, C., M. Kence & A. Kence, 2007. Genetic structure of honeybee, Apis mellifera L. (Hymenoptera: Apidae) populations of Turkey inferred from microsatellite analysis. Journal of Apicultural Research, 46 (1): 50-56.
8. Boecking, O. & E. Genersch, 2008. Varroosis-the ongoing crisis in bee keeping. Journal Fur Verbraucherschutz Und Lebensmittelsicherheit, 3 (2): 221-228.

9. Boecking, O. & W. Ritter, 1993. Grooming and removal behavior of Apis mellifera intermissa in Tunisia against Varroa jacobsoni. Journal of Apicultural Research, 32 (3-4): 127-134.
10. Bozic, J. & T. Valentincic, 1995. Quantitative analysis n of social grooming behaviour in the honey bee Apis mellifera carnica. Apidologie, 26 (2): 141-147.
11. Büchler, R., 1993. Rate of damaged mites in natural mite fall with regard to seasonal effects and infestation development. Apidologie, 24 (5): 492-493.
12. Büchler, R., W. Drescher & I. Tornier, 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.
13. De Figueiró Santos, J., F. C. Coelho & P. A. Bliman, 2016. Behavioral Modulation of Infestation by Varroa destructor in Bee Colonies. Implications for Colony Stability. Plos One, 11 (9): e0160465.
14. Delfinado-Baker, M., W. Rath & O. Boecking, 1992. Phoretic bee mites and honey bee grooming behavior. International Journal of Acarology, 18 (4): 315-322.
15. Eliash, N., N. K. Singh, S. Thangarajan, N. Sela, D. Leshkowitz, Y. Kamer, I. Azidman, A. Rafaeli & V. Soroker, 2017. Chemosensing of honeybee parasite, Varroa destructor: Transcriptomic analysis. Nature Scientific Reports, 7 (1): 13091.
16. Fries, I., W. Huazhen, S. Wei & C. S. Jin, 1996. Grooming behavior and damaged mites (Varroa jacobsoni) in Apis cerana cerana and Apis mellifera ligustica. Apidologie, 27 (1): 3-11.
17. Fries, I., A. Imdorf & P. Rosenkranz, 2006. Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie, 37 (5): 564-570.
18. Gallai, N., J. M. Salles, J. Settele & B. E. Vaissiere, 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics, 68 (3): 810-821.
19. Guzman-Novoa, E., B. Emsen, P. Unger, L. G. Espinosa-Montano & T. Petukhova, 2012. Genotypic variability and relationships between mite infestation levels, mite damage, grooming intensity, and removal of Varroa destructor mites in selected strains of worker honey bees (Apis mellifera L.). Journal of Invertebrate Pathology, 110 (3): 314-320.
20. Hamiduzzaman, M. M., B. Emsen, G. J. Hunt, S. Subramanyam, C. E. Williams, J. M. Tsuruda & E. Guzman Novoa, 2017. Differential gene expression associated with honey bee grooming behavior in response to Varroa mites. Behavior Genetics, 47 (3): 335-344.
21. Huang, Z. Y., G. Bian, Z. Xi & X. Xie, 2017. Genes important for survival or reproduction in Varroa destructor identified by RNAi. Insect Science, 26 (1): 68-75.
22. Kandemir, I., M. Kence & A. Kence, 2000. Genetic and morphometric variation in honey bee (Apis mellifera L.) populations of Turkey. Apidologie, 31 (3): 343-356.
23. Kence, M., D. Oskay, T. Giray & A. Kence, 2013. Honey bee colonies from different races show variation in defenses against the varroa mite in a ‘common garden’. Entomologia Experimentalis et Applicata, 149 (1): 36-43.
24. Kolmes, S. A., 1989. Grooming specialists among worker honey bees Apis mellifera. Animal Behaviour, 37 (6): 1048-1049.
25. Le Conte, Y., G. De Vaublanc, D. Crauser, F. Jeanne, J. C. Rousselle & J. M. Bécard, 2007. Honey bee colonies that have survived Varroa destructor. Apidologie, 38 (6): 566-572.
26. Livak, K. J. & T. D. Schmittgen, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25 (4): 402-408.
27. Milum, V. G., 1947. Grooming dance and associated activities of the honey bee. Illinois Academy of Science Transactions, 40: 194-196.
28. Mondragon, L., M. Spivak & R. Vandame, 2005. A multifactorial study of the resistance of honey bees Apis mellifera to the mite Varroa destructor over one year in Mexico. Apidologie, 36 (3): 345-358.
29. Moretto, G., L. S. Gonçalves & D. De Jong, 1993. Heritability of Africanized and European honey bee defensive behavior against the mite Varroa jacobsoni. Brazilian Journal of Genetics, 16 (1): 71-77.
30. Moretto, G., L. S. Gonçalves & D. De Jong, 1997. Relação entre o grau de infestação causado pela varroatose em abelhas adultas e a capacidade das operárias de se livrarem do ácaro Varroa jacobsoni. Naturalia, 22: 207-211.
31. Morfin, N., K. Given, M. Evans, E. Guzman-Novoa & G. J. Hunt, 2020. Grooming behavior and gene expression of the Indiana “mite-biter” honey bee stock. Apidologie, 51 (2): 267-275.
32. Navajas, M., A. Migeon, C. Alaux, M. L. Martin-Magniette, G. E. Robinson, J. D. Evans, S. Cros-Arteil, D. Crauser & Y. Le Conte, 2008. Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics, 9 (1): 1-11.
33. Oldroyd, B. P., 1999. Coevolution while you wait: Varroa jacobsoni, a new parasite of western honey bees. Trends in Ecology and Evolution, 14 (8): 312-315.
34. Peng, Y. S. C., 1988. “The Resistance Mechanism of the Asian Honey Bee (Apis cerana) to the Mite Varroa jacobsoni, 426-429”. In: Africanized honey bees and bee mites (Eds. G. R. Needham, R. E. Page Jr, M. Delfinado-Baker & C. E. Bowman). Ellis Horwood Limited, Chichester, USA, 572 pp.
35. Peng, Y. S. C., Y. Fang, S. Xu, L. Ge & M. E. Nasr, 1987. Response of foster Asian honeybee (Apis cerana Fabr.) colonies to the brood of European honeybee (Apis mellifera L.) infested with parasitic mite, Varroa jacobsoni Oudemans. Journal of Invertebrate Pathology, 49 (3): 259-264.
36. Ramsey, S. D., R. Ochoa, G. Bauchan, C. Gulbronson, J. D. Mowery, A. Cohen, D. Lim, J. Joklik, J. M. Cicero, J. D. Ellis, D. Hawthorne & D. Van Engelsdorp, 2019. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116 (5): 1792-1801.
37. Rinderer, T. E., L. I. De Guzman & A. M. Frake, 2013. Associations of parameters related to the fall of Varroa destructor (Mesostigmata: Varroidae) in Russian and Italian honey bee (Hymenoptera: Apidae) colonies. Journal of Economic Entomology, 106 (2): 566-575.
38. Rosenkranz, P., P. Aumeier & B. Ziegelmann, 2010. Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103 (1): 96-119.
39. Rosenkranz, P., I. Fries, O. Boecking & M. Stürmer, 1997. Damaged Varroa mites in the debris of honey bee (Apis mellifera L) colonies with and without hatching brood. Apidologie, 28 (6): 427-37.
40. Seeley, T. D., 2007. Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie, 38 (1): 19-29.
41. Solorzano, C. D., A. L. Szalanski, M. Kence, A. Kence, J. A. Mckern & J. W. Austin, 2009. Phylogeography and population genetics of honey bees (Apis mellifera L.) from Turkey based on COI-COII sequence data. Sociobiology, 53 (1): 237-246.
42. Thakur, R. K., K. Bienefeld & R. Keller, 1997. Varroa defense behavior in A. mellifera carnica. American Bee Journal, 137 (2): 143-148.
43. Van Alphen, J. J. & B. J. Fernhout, 2020. Natural selection, selective breeding, and the evolution of resistance of honeybees (Apis mellifera) against Varroa. Zoological Letters, 6 (1): 1-20.
44. Vandame, R., S. Morand, M. E. Colin & L. P. Belzunces, 2002. Parasitism in the social bee Apis mellifera: quantifying costs and benefits of behavioral resistance to Varroa destructor mites. Apidologie, 33 (5): 433-445.
45. Zaitoun, S. T., A. M. Al-Ghzawi & H. K. Shannag, 2001. Grooming behaviour of Apis mellifera syriaca towards Varroa jacobsoni in Jordan. Journal of Applied Entomology, 125 (1-2): 85-87.