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Confirmation of QTL Effects and Evidence of Genetic Dominance of Honeybee Defensive Behavior: Results of Colony and Individual Behavioral Assays

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Abstract

The stinging and guarding components of the defensive behavior of European, Africanized, hybrid, and backcross honeybees (Apis mellifera L.) were compared and analyzed at both colony and individual levels. Hybrid and Africanized backcross colonies stung as many times as Africanized ones. European backcross colonies stung more than European bees but not as many times as Africanized or Africanized backcross colonies. The degree of dominance for the number of times that worker bees stung a leather patch was estimated to be 84.3%, 200.8%, and 145.8% for hybrid, backcross European, and backcross Africanized colonies, respectively. Additionally, both guards at the colony entrance and fast-stinging workers of one European backcross colony had a significantly higher frequency of an Africanized DNA marker allele, located near “sting1,” a QTL previously implicated in stinging behavior at the colony level. However, guards and fast-stinging bees from a backcross to the Africanized parental colony did not differ from control bees in their frequency for the Africanized and European markers, as would be expected if large genetic dominance effects for sting1 exist. These results support the hypothesis that genetic dominance influences the defensive behavior of honeybees and confirm the effect of sting1 on the defensiveness of individual worker bees.

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REFERENCES

  • Adams, J., Rothman, E. D., Kerr, W. E., and Paulino, Z. L. (1977). Estimation of the number of sex alleles and queen matings from diploid male frequencies in a population of Apis mellifera. Genetics 86:583–596.

    Google Scholar 

  • Breed, M. D., and Rogers, K. B. (1991). The behavioral genetics of colony defense in honeybees: Genetic variability for guarding behavior. Behav. Genet. 21:295–303.

    Google Scholar 

  • Breed, M. D., Rogers, K. B., Hunley, J. A., and Moore, A. J. (1988). A correlation between guard behavior and defensive response in the honeybee, Apis mellifera. Anim. Behav. 37:515–516.

    Google Scholar 

  • Breed, M. D., Robinson, G. E., and Page, R. E. (1990). Division of labor during honeybee colony defense. Behav. Ecol. Sociobiol. 27:395–401.

    Google Scholar 

  • Cajero, A. S. (1995). Achievements and actions of the national program for the control of the African bee. Proc. IX Seminario Americano Apicultura, Colima, Mexico (1995).

  • Calderone, N. W., and Page, R. E. (1988). Genotypic variability in age polyethism and task specialisation in the honeybee, Apis mellifera (Hymenoptera: Apidae). Behav. Ecol. Sociobiol. 22:17–25.

    Google Scholar 

  • Calderone, N. W., and Page, R. E. (1991). The evolutionary genetics of division of labor in colonies of the honeybee (Apis mellifera). Am. Nat. 138:69–92.

    Google Scholar 

  • Calderone, N. W., and Page, R. E. (1992). Effects of interactions among genetically diverse nestmates on task specialisation by foraging honeybees (Apis mellifera). Behav. Ecol. Sociobiol. 30:219–226.

    Google Scholar 

  • Collins, A. M. (1986). Bidirectional selection for colony defense in Africanized honeybees. Am. Bee J. 126:827–828.

    Google Scholar 

  • Collins, A. M., Rinderer, T. E., Harbo, J. R., and Bolten, A. B. (1982). Colony defense by Africanized and European honeybees. Science 218:72–74.

    Google Scholar 

  • Collins, A. M., Rinderer, T. E., Harbo, J. R., and Brown, M. A. (1984). Heritabilities and correlations for several characters in the honeybee. J. Hered. 75:135–140.

    Google Scholar 

  • Collins, A. M., Rinderer, T. E., and Tucker, K. W. (1988). Colony defense of two honeybee types and their hybrids. I. Naturally mated queens. J. Apic. Res. 27:137–140.

    Google Scholar 

  • Crozier R. H., Consul P. C. (1976). Conditions for genetic polymorphisms in social Hymenoptera under selection at the colony level. Theor Popul Biol 10:1–9.

    Google Scholar 

  • DeGrandi-Hoffman, G., Collins, A. M., Martin, J. H., Schmidt, J. O., and Spangler, H. G. (1998). Nest defense behavior in colonies from crosses between Africanized and European honeybees (Apis mellifera L.) (Hymenoptera: Apidae). J. Insect Behav. 11:37–45.

    Google Scholar 

  • Gary, N. E., and Lorenzen, K. (1987). Vacuum device for collecting and dispensing honeybees (Hymenoptera: Apidae) and other insects into small cages. Ann. Entomol. Soc. Am. 80:664–666.

    Google Scholar 

  • Giray, T., Guzmán-Novoa, E., Aron, C. W., Zelinsky, B., Fahrbach, S. E., and Robinson, G. E. (2000). Genetic variation in worker temporal polyethism and colony defensiveness in the honeybee, Apis mellifera. Behav. Ecol. 11:44–55.

    Google Scholar 

  • Guzmán-Novoa, E., and Gary, N. E. (1993). Genotypic variability of components of foraging behavior in honeybees (Hymenoptera: Apidae). J. Econ. Entomol. 86:715–721.

    Google Scholar 

  • Guzmán-Novoa, E., and Page, R. E. (1993). Backcrossing Africanized honeybee queens to European drones reduces colony defensive behavior. Ann. Entomol. Soc. Am. 86:352–355.

    Google Scholar 

  • Guzmán-Novoa, E., and Page, R. E. (1994a). Genetic dominance and worker interactions affect honeybee colony defense. Behav. Ecol. 5:91–97.

    Google Scholar 

  • Guzmán-Novoa, E., and Page, R. E. (1994b). The impact of africanized bees on Mexican beekeeping. Am. Bee J. 134:101–106.

    Google Scholar 

  • Guzmán-Novoa, E., and Page, R. E. (1999). Selective breeding of honeybees (Hymenoptera: Apidae) in Africanized areas. J. Econ. Entomol. 92:521–525.

    Google Scholar 

  • Guzmán-Novoa, E., and Page, R. E., and Gary, N. E. (1994). Be-havioral and life-history components of division of labor in honeybees (Apis mellifera L.). Behav. Ecol. Sociobiol. 34:409–417.

    Google Scholar 

  • Guzmán-Novoa, E., Page, R. E., Spangler, H. G., and Erickson, E. H. (1999). A comparison of two assays to test the defensive behaviour of honeybees (Apis mellifera). J. Apic. Res. 38:205–209.

    Google Scholar 

  • Hall, H. G. (1990). Parental analysis of introgressive hybridization between African and European honeybees using nuclear DNA RFLPs. Genetics 125:611–621.

    Google Scholar 

  • Hall, H. G. (1992a). DNA studies reveal processes involved in the spread of new world African honeybees. Florida Entomol. 75:51–59.

    Google Scholar 

  • Hall, H. G. (1992b). Further characterization of nuclear DNA RFLP markers that distinguish African and European honeybees. Arch. Ins. Biochem. Biophys. 19:163–175.

    Google Scholar 

  • Hall, H. G., and Muralidharan, K. (1989). Evidence from mitochondrial DNA that African honeybees spread as continuous maternal Lineages. Nature 339:211–213.

    Google Scholar 

  • Hall, H. G., and Smith, D. R. (1991). Distinguishing African and European honeybee matrilines using amplified mitochondrial DNA. Proc. Nat. Acad. Sci. USA 88:4548–4552.

    Google Scholar 

  • Hellmich, R. L., Kulincevic, J. M., and Rothenbuhler, W. C. (1985). Selection for high and low pollen-hoarding honeybees. J. Hered. 76:155–158.

    Google Scholar 

  • Hillesheim, E., Koeniger, N., and Moritz, R. F. A. (1989). Colony performance in honeybees (Apis mellifera capensis Esch.) depends on the proportion of subordinate and dominant workers. Behav. Ecol. Sociobiol. 24:291–296.

    Google Scholar 

  • Hunt, G. J. (1997). Insect DNA extraction protocol. In Micheli M. R. and R. Bova, eds. Fingerprinting Methods Based on Arbitrarily Primed PCR. Springer-Verlag, Berlin, pp. 21–24.

    Google Scholar 

  • Hunt, G. J., Page, R. E., Fondrk, M. K., and Dullum, C. J. (1995). Major quantitative trait loci affecting honeybee foraging behavior. Genetics 141:1537–1545.

    Google Scholar 

  • Hunt, G. J., Guzmán-Novoa, E., Fondrk, M. K., and Page, R. E. (1998). Quantitative trait loci for honeybee stinging behavior and body size. Genetics 148:1203–1213.

    Google Scholar 

  • Hunt, G. J., Collins, A. M., Rivera, R., Page, R. E., and Guzmán-Novoa, E. (1999). Quantitative trait loci influencing honeybee alarm pheromone levels. J. Hered. 90:585–589.

    Google Scholar 

  • Kerr, W. E. (1967). The history of the introduction of African bees to Brazil. S. Afr. Bee J. 39:3–5.

    Google Scholar 

  • Lobo, J. A., Lama, M. A. D., and Mestriner, M. A. (1989). Population differentiation and racial admixture in the Africanized honeybee (Apis mellifera L.). Evolution 43:794–802.

    Google Scholar 

  • Moffett, J. O., Maki, D. L., Andre, T., and Fierro, M. M. (1987). The Africanized bee in Chiapas, México. Am. Bee J. 127:517–520.

    Google Scholar 

  • Moore, A. J., Breed, M. D., and Moor, M. J. (1987). The guard honeybee: Ontogeny and behavioral variability of workers performing a specialized task. Anim. Behav. 35:1159–1167.

    Google Scholar 

  • Moritz, R. F. A., and Hillesheim, E. (1985). Inheritance of dominance in honeybees (Apis mellifera capensis Esch.). Behav. Ecol. Sociobiol. 17:87–89.

    Google Scholar 

  • Moritz, R. F. A., and Meusel, M. S. (1992). Mitochondrial gene frequencies in Africanized honeybees (Apis mellifera L.): Theoretical model and empirical evidence. J. Evol. Biol. 5:71–72.

    Google Scholar 

  • Muralidharan, K., and Hall, H. G. (1990). Prevalence of African DNA RFLP alleles in neotropical African honeybees. Arch. Ins. Biochem. Biophys. 15:229–236.

    Google Scholar 

  • Nielsen, D. I., Ebert, P. R., Page, R. E., Hunt, G. J., and Guzmán-Novoa, E. (2000). Improved polymerase chain reaction–based mitochondrial genotype assay for identification of the Africanized honeybee (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 93:1–6.

    Google Scholar 

  • Owen, R. E. (1986). Colony-level selection in the social insects: Sin-gle locus additive and non-additive models. Theor. Popul. Biol. 29:198–234.

    Google Scholar 

  • Page, R. E. (1986). Sperm utilization in social insects. Annu. Rev. Entomol. 31:297–320.

    Google Scholar 

  • Page, R. E., and Laidlaw, H. H. (1988). Full sisters and super sisters: A terminological paradigm. Anim. Behav. 36:944–945.

    Google Scholar 

  • Page, R. E., and Robinson, G. E. (1991). The genetics of the division of labour in honeybee colonies. Adv. Insect Physiol. 23:117–169.

    Google Scholar 

  • Page, R. E., Jr., Waddington, K. D., Hunt, G. J., and Fondrk, M. K. (1995). Genetic determinants of honeybee foraging behavior. Anim. Behav. 50:1617–1625.

    Google Scholar 

  • Page, R. E., Jr., Fondrk, M. K., Hunt G. J., Guzmán-Novoa, E., Humphries, M. A., Nguyen, K., and Greene, A. (2000). Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. J. Hered. 91:474–479.

    Google Scholar 

  • Quezada-Euán, J. J. G., and Medina, L. M. (1998). Hybridization between European and Africanized honeybees (Apis mellifera L.) in tropical Yucatan, Mexico: I. Morphometric changes in feral and managed colonies. Apidologie 29:555–568.

    Google Scholar 

  • Ribbands, C. R. (1954). The defence of the honeybee community. Proc. Roy. Soc. London (B) 142:514–524.

    Google Scholar 

  • Rinderer, T. E., Steltzer, J. A., Oldroyd, B. P., Buco, S. M., and Rubink, W. L. (1991). Hybridization between European and Africanized honeybees in the neotropical Yucatan Peninsula. Science 253:309–312.

    Google Scholar 

  • Robinson, G. E., and Page, R. E., and Page, R. E. (1988). Genetic determination of guarding and undertaking in honeybee colonies. Nature 333:356–358.

    Google Scholar 

  • Robinson, G. E., and Page, R. E. (1989). Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honeybee colonies. Behav. Ecol. Sociobiol. 24:317–323.

    Google Scholar 

  • Robinson, G. E., Page, R. E., and Fondrk, M. K. (1990). Intracolonial behavioral variation in worker oviposition, oophagy, and larval care in queenless honeybee colonies. Behav. Ecol. Sociobiol. 26:315–323.

    Google Scholar 

  • Rothenbuhler, W. C., and Page, R. E. (1989). Genetic variability for temporal polyethism in colonies consisting in similarly-aged worker honeybees. Apidologie 29:433–437.

    Google Scholar 

  • Seeley, T. D. (1989). The honeybee colony as a superorganism. Am. Sci. 77:546–553.

    Google Scholar 

  • Sheppard, W. S., Soares, A. E. E., and DeJong, D. (1991). Hybrid status of honeybee populations near the historic origin of Africanization in Brazil. Apidologie 22:643–652.

    Google Scholar 

  • Smith, D. R., Taylor, O. R., and Brown, W. M. (1989). Neotropical Africanized honeybees have African mitochondrial DNA. Nature 339:213–215.

    Google Scholar 

  • Stort, A. C. (1975a). Genetic study of the aggressiveness of two subspecies of Apis mellifera in Brazil. II. Time at which the first sting reached the leather ball. J. Apic. Res. 14:171–175.

    Google Scholar 

  • Stort, A. C. (1975b). Genetic study of the aggressiveness of two subspecies of Apis mellifera in Brazil. IV. Number of stings in the gloves of the observer. Behav. Genet. 5:269–274.

    Google Scholar 

  • Stort, A. C. (1975c). Genetic study of the aggressiveness of two subspecies of Apis mellifera in Brazil. V. Number of stings in the leather ball. J. Kans. Entomol. Soc. 48:381–387.

    Google Scholar 

  • Sugden, E. A., and Williams, K. R. (1991). October 15: The day the bee arrived. Gle. Bee Cult. 119:18–21.

    Google Scholar 

  • Sylvester, H. A., and Rinderer, T. E. (1987). Fast africanized bee identification system (FABIS) manual. Am. Bee J. 127:511–516.

    Google Scholar 

  • Villa, J. D. (1988). Defensive behaviour of Africanized and European honeybees at two elevations in Colombia. J. Apic. Res. 27:141–145.

    Google Scholar 

  • Winston, M. L. (1987). The Biology of the Honeybee. Harvard University Press, Cambridge, MA.

    Google Scholar 

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Authors and Affiliations

  1. CENIFMA-INIFAP, Santa Crúz 29-B, Las Haciendas, 52140 Metepéc, Edo. de Méx., Mexico

    Ernesto Guzmán-Novoa & José L. Uribe

  2. Department of Entomology, Purdue University, West Lafayette, IN, 47907-1158

    Greg J. Hunt, Christine Smith & Miguel E. Arechavaleta-Velasco

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  1. Ernesto Guzmán-Novoa
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  2. Greg J. Hunt
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  3. José L. Uribe
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  4. Christine Smith
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  5. Miguel E. Arechavaleta-Velasco
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Correspondence to Ernesto Guzmán-Novoa.

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Guzmán-Novoa, E., Hunt, G.J., Uribe, J.L. et al. Confirmation of QTL Effects and Evidence of Genetic Dominance of Honeybee Defensive Behavior: Results of Colony and Individual Behavioral Assays. Behav Genet 32, 95–102 (2002). https://doi.org/10.1023/A:1015245605670

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