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Quantitative Trait Loci Associated with Reversal Learning and Latent Inhibition in Honeybees (Apis mellifera)

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Abstract

A study was conducted to identify quantitative trait loci (QTLs) that affect learning in honeybees. Two F1 supersister queens were produced from a cross between two established lines that had been selected for differences in the speed at which they reverse a learned discrimination between odors. Different families of haploid drones from two of these F1 queens were evaluated for two kinds of learning performance—reversal learning and latent inhibition—which previously showed correlated selection responses. Random amplified polymorphic DNA markers were scored from recombinant, haploid drone progeny that showed extreme manifestations of learning performance. Composite interval mapping procedures identified two QTLs for reversal learning (lrn2 and lrn3: LOD, 2.45 and 2.75, respectively) and one major QTL for latent inhibition (lrn1: LOD, 6.15). The QTL for latent inhibition did not map to either of the linkage groups that were associated with reversal learning. Identification of specific genes responsible for these kinds of QTL associations will open up new windows for better understanding of genes involved in learning and memory.

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REFERENCES

  • Abramson, C. I., and Bitterman, M. E. (1986). Latent inhibition in honeybees. Anim. Learn. Behav. 14: 184–189.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Benatar, S. T., Cobey, S., and Smith, B. H. (1995). Selection on a haploid genotype for discrimination learning performance: Correlation between drone honeybees (Apis mellifera) and their worker progeny (Hymenoptera: Apidae). J. Insect. Behav. 8: 637–652.

    Google Scholar 

  • Bhagavan, S., Benatar, S. T., Cobey, S., and Smith, B. H. (1994). Effect of genotype but not of age or cast on olfactory learning performance in the honeybee. Apis mellifera. Anim. Behav. 48: 1357–1369.

    Google Scholar 

  • Bice, P., Foroud, T., Bo, R., Castelluccio, P., Lumeng, L., Li, T., and Carr, L. G. (1998). Genomic screen for QTLs underlying alcohol consumption in the P and NP rat lines. Mammal. Genome 9: 949–955.

    Google Scholar 

  • Bitterman, M. E. (1972). Comparative studies of the role of inhibition in reversal learning. In Boakes, R. A., and Halliday, M. S. (eds.), Inhibition and Learning, Academic Press, London, pp. 153–174.

    Google Scholar 

  • Boynton, S., and Tully, T. (1992). Latheo, a new gene involved in associative learning and memory in Drosophila melanogaster identified from P element mutagenesis. Genetics 131: 655–672.

    PubMed  Google Scholar 

  • Brandes, C. (1988). Estimation of heritability of learning behaviour in honeybees (Apis mellifera capensis). Behav. Genet. 18: 119–132.

    PubMed  Google Scholar 

  • Brandes, C., and Menzel, R. (1990). Common mechanisms in proboscis extension conditioning and visual learning revealed by genetic selection in honeybees (Apis mellifera capensis). J. Comp. Physiol. 166: 545–552.

    Google Scholar 

  • Brandes, C., Frisch, B., and Menzel, R. (1988). Time course of memory formation differs in honeybee lines selected for good and bad learning. Anim. Behav. 36: 981–985.

    Google Scholar 

  • Caldarone, B., Saavedra, C., Tartaglia, K., Wehner M. J., Dudek, C. B., and Flaherty, L. (1997). Quantitative trait loci analysis affecting contextual conditioning in mice. Nature Genet. 17: 335–337.

    PubMed  Google Scholar 

  • Cardon, L. R., Smith, S. D., Fulker, D. W., Kimberling, W. J., Pennington, B. F., and Defries, J. C. (1994). Quantitative trait loci for reading disability on chromomose 6. Science 266: 276–279.

    PubMed  Google Scholar 

  • Chandra, S., Hosler, J., and Smith, B. H. (2000). Heritable variation for latent inhibition and its correlation to reversal learning in the honeybees, Apis mellifera. J. Comp. Psych. 114: 86–97.

    Google Scholar 

  • Chen, C., and Tonegawa, S. (1997). Molecular genetic analysis of synaptic plasticity, activity dependent, learning and memory in the mammalian brain. Annu. Rev. NeuroSci. 20: 157–184.

    PubMed  Google Scholar 

  • Crabbe, J. C., Beknap, J. K., and Buck, K. J. (1994). Genetics animal models of alcohol and drug abuse. Science 264: 1715–1723.

    PubMed  Google Scholar 

  • Crain, W. R., Davidson, E. H., and Britten, R. J. (1976). Contrasting patterns of DNA sequence arrangement in Apis mellifera (honeybee) and Muscal domestica (housefly). Chromosoma 59: 1–12.

    PubMed  Google Scholar 

  • Darvasi, A., and Soller, M. A. (1997). Simple method to calculate resolving power and confidence interval of a QTL map location. Behav. Genet. 27: 125–132.

    PubMed  Google Scholar 

  • De Belle, J. S., Hiliker, A. J., and Sokolowski, M. B. (1989). Genetic localization of foragaing (for): A major gene for larval behavior in Drosophila melanogaster. Genetics 123: 157–163.

    PubMed  Google Scholar 

  • Dubnau, J., and Tully, T. (1998). Gene discovery in Drosophila: New insights for learning and memory. Annu. Rev. Neurosci. 21: 407–444.

    PubMed  Google Scholar 

  • Dura, J. M., Preat, T., and Tully, T. (1993). Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J. Neurogenet. 9: 1–14.

    PubMed  Google Scholar 

  • Estivilli, X., Farral, M., Scambler, P. J., Bell, G. M., Hawley, K. M. F., Lench, N. J., Bates, G. P., and Kruyer, H. C. (1987). A candidate for cystic fibrosis locus isolated by selection for methylation-free islands. Nature 326: 840–845.

    PubMed  Google Scholar 

  • Falconer, D. S., and Mackay, T. F. C. (1996). Introduction to Quantitative Genetics, Addison Wesley Longman, Essex, UK.

    Google Scholar 

  • Ferguson, H. J., Cobey, S., and Smith, B. H. (2001). Sensitivity to a change in reward is heritable in the honey bee, Apis mellifera. Anim. Behav. 61: 527–534.

    Google Scholar 

  • Fisher, P. J., Turic, D., Williams, N. M., Mcguffin, P., Asherson, P., Ball, D., Craig, I., Eley, T., Hill, L., Chorney, K., M. J., Benbow, C. P., Lubinski, D., Plomin, R., and Owen, M. (1999). DNA pooling identifies QTLs on chromosome 4 for general cognitive ability in children. Hum. Mol. Genet. 8: 915–922.

    PubMed  Google Scholar 

  • Getz, M. W., Brückner, D., and Smith, K. B. (1986). Conditioning honeybees to discriminate between heritable odors from full and half sisters. J. Comp. Physiol. 159: 251–256.

    Google Scholar 

  • Gusella, J. F., Wexler, N. S., Conneally, P. M., Naylor, S. L., Anderson, M. A., Tanzi, R. E., Watkins, P. C., and Ottina, K. (1983). Apolymorphic DNA marker genetically linked to Huntington' disease. Nature 306: 234–238.

    PubMed  Google Scholar 

  • Hall, J. C. (1994). Pleiotropy of behavioral genes. In Greenspan, R. J., and Kyriacou, C. P. (eds.), Flexibility and Constraint in Behavioral Systems, John Wiley, New York, pp. 15–27.

    Google Scholar 

  • Harbo, J. R. (1986). Propagation and instrumental insemination. In Rinderer, T. E. (ed.), Genetics and Breeding, Academic Press, Orlando, FL, pp. 361–387.

    Google Scholar 

  • Hunt, G. J., and Page, R. E. (1995). Linkage map of the honeybee, Apis mellifera, based on RAPD markers. Genetics 139: 1371–1382.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Jansen, R. C. (1994). Controlling type I and type II errors in mapping quantitative trait loci. Genetics 138: 871–881.

    PubMed  Google Scholar 

  • Jordan, R. A., and Brosemer, R. W. (1974). Characterization of DNA from three bee species. J. Insect Physiol. 20: 2513–2520.

    PubMed  Google Scholar 

  • Lai, C., Lyaman, R. F., Long, A. D., Langley, C. H., and Mackay, T. F. (1994). Naturally occurring variation in bristle number and DNA polymorphisms at the scabrous locus of Drosophila melanogaster. Science 266: 1697–1702.

    PubMed  Google Scholar 

  • Laidlaw, H. H., and Page, R. E. (1984). Polyandry in honey bees (Apis mellifera): Sperm utilization and intracolony genetic relationships. Genetics 108: 985–997.

    Google Scholar 

  • Lander, E. S., and Botstein, D. (1989). Mapping Mendalian factors underlying quantitative traits. Genetics 121: 185–199.

    PubMed  Google Scholar 

  • Lander, E. S., and Schork, N. I. (1994). Genetic dissection of complex traits. Science 265: 2037–2048.

    PubMed  Google Scholar 

  • Lander, E., and Kruglyak, L. (1995). Genetic dissection of complex traits: Guidelines for interpreting and reporting linkage results. Nature Genet. 11: 241–247.

    PubMed  Google Scholar 

  • Lubow, R. E. (1973). Latent inhibition. Psychol. Bull. 79: 398–407.

    PubMed  Google Scholar 

  • Lubow, R. E. (1997). Latent inhibition as a measure of learned inattention: Some problems and solutions. Behav. Brain Res. 88: 75–83.

    PubMed  Google Scholar 

  • Lubow, R. E., Weiner, I., and Feldon, J. (1983). An animal model of attention. In Spiegelstein, M. Y., and Levy A. (eds.), Behavioral Models and the Analysis of Drug Action, Elsevier, Amsterdam, pp. 8901–8907.

    Google Scholar 

  • Markel, P. D., Bennett, B., Beeson, M., Gordon, L., and Johnson, T. E. (1997). Confirmation of quantitative trait loci for ethanol sensitivity in long-sleep and short-sleep mice. Genome Res. 7: 92–99.

    PubMed  Google Scholar 

  • Menzel, R., and Bitterman, M. E. (1983). Learning by honeybees in unnatural situation. In Huber, F., and Markl, H. (eds.), Neuroethology and Behavioural Physiology, Springer-Verlag, Berlin, pp. 206–215.

    Google Scholar 

  • Menzel, R. (1990). Learning, memory, and ‘cognition’ in honeybees. In Kesner, R. P., and Olten, D. S. (eds.), Neurobiology of Comparative Cognition, Lawrence Erlbaum, Hillsdale, NJ, pp. 237–292.

    Google Scholar 

  • Osborne, K. A., Robichon, A., Burgess, E., Butland, S., Shaw, R. A., Coulthard, A., Pereira, H. S., Greenspan, R. J., and Sokolowski, M. B. (1997). Natural behavior polymorphism due to a cGMPdependent protein kinase of Drosophila. Science 277: 834–836.

    PubMed  Google Scholar 

  • Owen, E. H., Christensen, S. C., Paylor, R., and Wehner, J. M. (1997). Identification of quantitative trait loci involved in contextual and auditory-cued fear conditioning in BXD recombinant inbred strains. Behav. NeuroSci. 111: 292–300.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Paterson, A. H., Lander, E. S., Hewitt, J. D., Peterson, S., Lincoln, S. E., and Tanksley, S. D. (1988). Resolution of quantitative traits into Mendalian factors using a complete linkage map of restriction fragment length poylmorphisms. Nature 335: 721–726.

    PubMed  Google Scholar 

  • Phillips, P. C. (1999). From complex traits to complex alleles. Trends Genet. 15: 6–8.

    PubMed  Google Scholar 

  • Seeley, T. D. (1994). Honeybees foragers as sensory units of their colonies. Behav. Ecol. Sociobiol. 34: 51–62.

    Google Scholar 

  • Sokal, R. R., and Rohlf, J. E. (1997). Biometry, 3rd ed., W. H. Freeman, New York.

    Google Scholar 

  • St. George-Hyslop, P. H., Haines, J. L., Farrer, L. A., Polinsky, R., and Van Broeckhoven (1990). Genetic linkage studies that Alzheimer' disease is not a single homogenous disorder. Nature 347: 194–197.

    PubMed  Google Scholar 

  • Symula, D. J., Frazer, K. A., Ueda, Y., Denefle, P., Stevens, M. E., Wang, Z., Locksley, R., and Rubin, E. M. (1999). Functional screening of an asthama QTL in YAC transgenic mice. Nature Genet. 23: 241–244.

    PubMed  Google Scholar 

  • Takahashi, J. S., Pinto, L. H., and Vitaterna, M. H. (1994). Forward and reverse genetic approaches to behavior in the mouse. Science 264: 1724–1732.

    PubMed  Google Scholar 

  • Tanksley, S. D. (1993). Mapping polygenes. Annu. Rev. Genet. 27: 205–233.

    Google Scholar 

  • Tully, T., and Hirsch, J. (1982). Behavior genetic analysis of Phormia regina: Isolation of pure breeding lines for high and low levels of the central excitatory state (CES) from an unselected population. Behav. Genet. 12: 395–415.

    Google Scholar 

  • Van Ooijen, J. W. (1999). LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity 83: 613–624.

    Google Scholar 

  • Van Ooijen, J. W., and Maloepaard, C. (1996). Map QTL Version 3.0: Software for the Calculation of QTL Positions on Genetic Maps, DLO-Center for Plant Breeding and Reproduction Research, Wageningen, The Netherlands.

    Google Scholar 

  • Wehner, J. M., Radcliffe, R. A., Rosmann, S. T., Christensen, S. C., Rasmussen, D. L., Fulkner, D. W., and Wiles, M. (1997). Quantitative trait locus analysis of contextual fear conditioning in mice. Nature Genet. 17: 331–334.

    Google Scholar 

  • Williams, J. G. K., Kubelik, A. R., Llivak, K. J., Rafalski, J. A., and Tingey, S. V. (1990). DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res. 18: 6531–6535.

    PubMed  Google Scholar 

  • Zawistowski, S. L., and Hirsch, J. (1984). Conditioned discrimination in the behavior genetic analysis of the blow fly Phormia regina: Controls and bidirectional selection. Anim. Learn. Behav. 12: 402–408.

    Google Scholar 

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Chandra, S.B.C., Hunt, G.J., Cobey, S. et al. Quantitative Trait Loci Associated with Reversal Learning and Latent Inhibition in Honeybees (Apis mellifera). Behav Genet 31, 275–285 (2001). https://doi.org/10.1023/A:1012227308783

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