Reorganization of the Central Nervous Systems in Response to Changes in Social Environment Among Insects

Ken Sasaki; Takashi Nagao

doi:10.20965/jrm.2007.p0369

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JRM Vol.19 No.4 pp. 369-373

doi: 10.20965/jrm.2007.p0369

(2007)

Paper:

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Reorganization of the Central Nervous Systems in Response to Changes in Social Environment Among Insects

Ken Sasaki and Takashi Nagao

Human Information Systems, Kanazawa Institute of Technology, 3-1 Yakkaho, Hakusan, Ishikawa 924-0838, Japan

Received:

January 11, 2007

Accepted:

March 26, 2007

Published:

August 20, 2007

Keywords:

social insect, brain, plasticity, reproduction, caste

Abstract

Caste is a polyphenism for efficiently accomplishing various tasks in a group for social insects, and morphological differentiation is based on nutritional conditions in larval development. Adult worker insects can plastically convert part of their internal organs and behaviors to those of a queen while maintaining external morphology as is. Behavioral change together with caste transition is caused by physiological change in the brain, and behavioral change affects even the brain morphologically, eventually creating an “adaptive” brain specialized in caste. This phenomenon, a typical example of “mobiligence,” is a model case in which physiological and morphological transitions in the brain are detected.

Cite this article as:

K. Sasaki and T. Nagao, “Reorganization of the Central Nervous Systems in Response to Changes in Social Environment Among Insects,” J. Robot. Mechatron., Vol.19 No.4, pp. 369-373, 2007.

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References

[1] G. C. Arnold, S. Budharugsa, and C. Masson, “Organization of the antennal lobe in the queen honey bee, Apis mellifera L.,” Int. J. Insect Morphol. Embryol., 17, pp. 185-195, 1988.
[2] G. Bicker and R. Menzel, “Chemical codes for the control of behaviour in arthropods,” Nature, 337, pp. 33-39, 1989.
[3] W. Blenau, M. Schmidt, D. Faensen, and F. Schurmann, “Neurons with dopamine-like immunoreactivity target mushroom body Kenyon cell somata in the brain of some hymenopteran insects,” Int. J. Insect Morphol. Embryol., 28, pp. 203-210, 1999.
[4] G. Bloch, T. Simon, G. E. Robinson, and A. Hefetz, “Brain biogenic amines and reproductive dominance in bumble bees (Bombus terrestris),” J. Comp. Physiol. A, 186, pp. 261-268, 2000.
[5] C. Brandes, M. Sugawa, and R. Menzel, “High-performance liquid chromatography (HPLC) measurement of catecholamines in single honeybee brains reveals caste-specific differences between worker bees and queens in Apis mellifera,” Comp. Biochem. Physiol., 97C, pp. 53-57, 1990.
[6] K. S. Delaplane and J. R. Harbo, “Drone production by young versus old worker honeybees in queenless colonies,” Apidologie, 18, pp. 115-120, 1987.
[7] T. C. D. Dombroski, Z. J. P. Simoes, and M. M. G. Bitondi, “Dietary dopamine causes ovary activation in queenless Apis mellifera workers,” Apidologie, 34, pp. 281-289, 2003.
[8] C. A. Evers and T. D. Seeley, “Kin discrimination and aggression in honey bee colonies with laying workers,” Anim. Behav., 34, pp. 924-944, 1986.
[9] S. E. Fahrbach and G. E. Robinson, “Juvenile hormone, behavioral maturation, and brain structure in the honey bee,” Dev. Neurosci., 18, pp. 102-114, 1996.
[10] W. Gronenberg and J. Liebig, “Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos,” Naturewiss., 89, pp. 343-345, 1999.
[11] K. Harano, K. Sasaki, and T. Nagao, “Depression of brain dopamine and its metabolite after mating in European honeybee (Apis mellifera) queens,” Naturwiss., 92, pp. 310-313, 2004.
[12] M. H. Haydak, “Do the nurse honey bees recognize the sex of the larvae?” Science, 127, p. 1113, 1958.
[13] N. Koeniger, “Uber die fahigkeit der bienenkonigin (Apis mellifica L.) zwischen arbeiten und drohnenzellen zu unterscheiden,” Apidologie, 1, pp. 115-142, 1970.
[14] D. B. Michelsen, “Catecholamines affect storage and retrieval of conditioned odour stimuli in honey bees,” Comp. Biochem. Physiol., 91C, pp. 479-482, 1988.
[15] C. D. Michener, “The Social Behavior of the Bees: A comparative study,” Harvard Univ. Press, Cambridge, Mass., 1974.
[16] A. R. Mercer and R. Menzel, “The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera,” J. Comp. Physiol., 145, pp. 363-368, 1982.
[17] S. M. Morgan, V. M. B. Huryn, S. R. Downes, and A. R. Mercer, “The effects of queenlessness on the maturation of the honey bee olfactory system,” Behav. Brain Res., 91, pp. 115-126, 1998.
[18] C. C. Nice and J. A. Fordyce, “How caterpillars avoid overheating: behavioral and phenotypic plasticity of pipevine swallowtail larvae,” Oecologia, 146, pp. 541-548, 2006.
[19] R. E. Page and E. H. Erickson, “Reproduction by worker honey bees (Apis mellifera L.),” Behav. Ecol. Sociobiol., 23, pp. 117-126, 1998.
[20] L. Z. Pinto, M. A. F. B. Laure, M. M. G. Bitondi, K. Hartfelder, and Z. L. P. Simoes, “Ventral nerve cord remodeling in a stingless bee (Melipona quadrifasciata anthidioides, Hymenoptera, Apidae) depends on ecdysteroid fluctuation and programmed cell death,” Int. J. Dev. Biol., 47, pp. 385-388, 2003.
[21] S. M. Rogers, T. Matheson, K. Sasaki, K. Kendrick, S. J. Simpson, and M. Burrows, “Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in locust,” J. Exp. Biol., 207, pp. 3603-3617, 2004.
[22] S. F. Sakagami, “Occurrence of an aggressive behaviour in queenless hives, with considerations on the social organization of honeybee,” Insectes. Soc., 1, pp. 331-343, 1954.
[23] K. Sasaki, H. Sobajima, T. Satoh, and Y. Obara, “Activation in vitro of unfertilized egg development in honeybee queens,” Naturwiss., 84, pp. 74-76, 1997.
[24] K. Sasaki and T. Nagao, “Distribution and levels of dopamine and its metabolites in brains of reproductive workers in honeybees,” J. Insect Physiol., 47, pp. 1205-1216, 2001.
[25] K. Sasaki and Y. Obara, “Nutritional factors affecting the egg sex ratio adjustment by a honeybee queen,” Insectes Soci., 48, pp. 355-359, 2001.
[26] K. Sasaki and T. Nagao, “Brain tyramine and reproductive states of workers in honeybees,” J. Insect Physiol., 48, pp. 1075-1085, 2002.
[27] K. Sasaki and Y. Obara, “Egg activation and timing of sperm acceptance by an egg in honeybees (Apis mellifera L.),” Insectes Soci., 49, pp. 234-240, 2002.
[28] K. Sasaki, H. Kitamura, and Y. Obara, “Discrimination of larval sex and timing of male brood elimination by workers in honeybees (Apis mellifera L.),” Appl. Entomol. Zool., 39, pp. 393-399, 2004.
[29] K. Sasaki and K. Harano, “Potential effects of tyramine on the transition to reproductive workers in honeybees (Apis mellifera L.),” Physiol. Entomol., 32, pp. 194-198, 2007.
[30] K. Sasaki, K. Yamasaki, and T. Nagao, “Neuro-endocrine correlates of ovarian development and egg-laying behaviors in the primitively eusocial wasp (Polistes chinensis),” J. Insect Physiol., 53, in press.
[31] D. J. Schulz and G. E. Robinson, “Octopamine influences division of labor in honey bee colonies,” J. Comp. Physiol. A, 187, pp. 53-61, 2001.
[32] A. M. Shapiro, “Seasonal Polyphenism,” M. K. Hecht and W. C. Steere, W.C. (eds.) Evolutionary Biology, Vol.9, Plenum, New York, pp. 259-333, 1976.
[33] D. Sigg, C. M. Thompson, and A. R. Mercer, “Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera (L.),” J. Neurosci., 17, pp. 7148-7156, 1997.
[34] S. J. Simpson, A. R. McCaffery, B. F. Hagele, “A behavioural analysis of phase change in the desert locust. Biol. Rev., 74, pp. 461-480, 1999.
[35] R. E. Snodgrass, “Anatomy of the Honey Bee,” Cornell Univ. Press, Ithaca, N.Y., 1956.
[36] H. H. W. Velthuis, F. J. Verheijen, and A. J. Gottenbos, “Laying worker honey bee: similarities to the queen,” Nature, 207, p. 1314, 1965.
[37] J. de Wilde and J. Beetsma, “The physiology of caste development in social insects,” Adv. Insect Physiol., 16, pp. 167-246, 1982.
[38] M. L. Winston, “The Biology of the Honey Bee,” Harvard Univ. Press, Cambridge, Mass., 1987.
[39] G. S. Withers, S. E. Fahrbach, and G. E. Robinson, “Selective neuroanatomical plasticity and division of labour in the honeybee,” Nature, 364, pp. 238-240, 1993.

This article is published under a Creative Commons Attribution-NoDerivatives 4.0 Internationa License.

[1] [1] G. C. Arnold, S. Budharugsa, and C. Masson, “Organization of the antennal lobe in the queen honey bee, Apis mellifera L.,” Int. J. Insect Morphol. Embryol., 17, pp. 185-195, 1988.

[2] [2] G. Bicker and R. Menzel, “Chemical codes for the control of behaviour in arthropods,” Nature, 337, pp. 33-39, 1989.

[3] [3] W. Blenau, M. Schmidt, D. Faensen, and F. Schurmann, “Neurons with dopamine-like immunoreactivity target mushroom body Kenyon cell somata in the brain of some hymenopteran insects,” Int. J. Insect Morphol. Embryol., 28, pp. 203-210, 1999.

[4] [4] G. Bloch, T. Simon, G. E. Robinson, and A. Hefetz, “Brain biogenic amines and reproductive dominance in bumble bees (Bombus terrestris),” J. Comp. Physiol. A, 186, pp. 261-268, 2000.

[5] [5] C. Brandes, M. Sugawa, and R. Menzel, “High-performance liquid chromatography (HPLC) measurement of catecholamines in single honeybee brains reveals caste-specific differences between worker bees and queens in Apis mellifera,” Comp. Biochem. Physiol., 97C, pp. 53-57, 1990.

[6] [6] K. S. Delaplane and J. R. Harbo, “Drone production by young versus old worker honeybees in queenless colonies,” Apidologie, 18, pp. 115-120, 1987.

[7] [7] T. C. D. Dombroski, Z. J. P. Simoes, and M. M. G. Bitondi, “Dietary dopamine causes ovary activation in queenless Apis mellifera workers,” Apidologie, 34, pp. 281-289, 2003.

[8] [8] C. A. Evers and T. D. Seeley, “Kin discrimination and aggression in honey bee colonies with laying workers,” Anim. Behav., 34, pp. 924-944, 1986.

[9] [9] S. E. Fahrbach and G. E. Robinson, “Juvenile hormone, behavioral maturation, and brain structure in the honey bee,” Dev. Neurosci., 18, pp. 102-114, 1996.

[10] [10] W. Gronenberg and J. Liebig, “Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos,” Naturewiss., 89, pp. 343-345, 1999.

[11] [11] K. Harano, K. Sasaki, and T. Nagao, “Depression of brain dopamine and its metabolite after mating in European honeybee (Apis mellifera) queens,” Naturwiss., 92, pp. 310-313, 2004.

[12] [12] M. H. Haydak, “Do the nurse honey bees recognize the sex of the larvae?” Science, 127, p. 1113, 1958.

[13] [13] N. Koeniger, “Uber die fahigkeit der bienenkonigin (Apis mellifica L.) zwischen arbeiten und drohnenzellen zu unterscheiden,” Apidologie, 1, pp. 115-142, 1970.

[14] [14] D. B. Michelsen, “Catecholamines affect storage and retrieval of conditioned odour stimuli in honey bees,” Comp. Biochem. Physiol., 91C, pp. 479-482, 1988.

[15] [15] C. D. Michener, “The Social Behavior of the Bees: A comparative study,” Harvard Univ. Press, Cambridge, Mass., 1974.

[16] [16] A. R. Mercer and R. Menzel, “The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera,” J. Comp. Physiol., 145, pp. 363-368, 1982.

[17] [17] S. M. Morgan, V. M. B. Huryn, S. R. Downes, and A. R. Mercer, “The effects of queenlessness on the maturation of the honey bee olfactory system,” Behav. Brain Res., 91, pp. 115-126, 1998.

[18] [18] C. C. Nice and J. A. Fordyce, “How caterpillars avoid overheating: behavioral and phenotypic plasticity of pipevine swallowtail larvae,” Oecologia, 146, pp. 541-548, 2006.

[19] [19] R. E. Page and E. H. Erickson, “Reproduction by worker honey bees (Apis mellifera L.),” Behav. Ecol. Sociobiol., 23, pp. 117-126, 1998.

[20] [20] L. Z. Pinto, M. A. F. B. Laure, M. M. G. Bitondi, K. Hartfelder, and Z. L. P. Simoes, “Ventral nerve cord remodeling in a stingless bee (Melipona quadrifasciata anthidioides, Hymenoptera, Apidae) depends on ecdysteroid fluctuation and programmed cell death,” Int. J. Dev. Biol., 47, pp. 385-388, 2003.

[21] [21] S. M. Rogers, T. Matheson, K. Sasaki, K. Kendrick, S. J. Simpson, and M. Burrows, “Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in locust,” J. Exp. Biol., 207, pp. 3603-3617, 2004.

[22] [22] S. F. Sakagami, “Occurrence of an aggressive behaviour in queenless hives, with considerations on the social organization of honeybee,” Insectes. Soc., 1, pp. 331-343, 1954.

[23] [23] K. Sasaki, H. Sobajima, T. Satoh, and Y. Obara, “Activation in vitro of unfertilized egg development in honeybee queens,” Naturwiss., 84, pp. 74-76, 1997.

[24] [24] K. Sasaki and T. Nagao, “Distribution and levels of dopamine and its metabolites in brains of reproductive workers in honeybees,” J. Insect Physiol., 47, pp. 1205-1216, 2001.

[25] [25] K. Sasaki and Y. Obara, “Nutritional factors affecting the egg sex ratio adjustment by a honeybee queen,” Insectes Soci., 48, pp. 355-359, 2001.

[26] [26] K. Sasaki and T. Nagao, “Brain tyramine and reproductive states of workers in honeybees,” J. Insect Physiol., 48, pp. 1075-1085, 2002.

[27] [27] K. Sasaki and Y. Obara, “Egg activation and timing of sperm acceptance by an egg in honeybees (Apis mellifera L.),” Insectes Soci., 49, pp. 234-240, 2002.

[28] [28] K. Sasaki, H. Kitamura, and Y. Obara, “Discrimination of larval sex and timing of male brood elimination by workers in honeybees (Apis mellifera L.),” Appl. Entomol. Zool., 39, pp. 393-399, 2004.

[29] [29] K. Sasaki and K. Harano, “Potential effects of tyramine on the transition to reproductive workers in honeybees (Apis mellifera L.),” Physiol. Entomol., 32, pp. 194-198, 2007.

[30] [30] K. Sasaki, K. Yamasaki, and T. Nagao, “Neuro-endocrine correlates of ovarian development and egg-laying behaviors in the primitively eusocial wasp (Polistes chinensis),” J. Insect Physiol., 53, in press.

[31] [31] D. J. Schulz and G. E. Robinson, “Octopamine influences division of labor in honey bee colonies,” J. Comp. Physiol. A, 187, pp. 53-61, 2001.

[32] [32] A. M. Shapiro, “Seasonal Polyphenism,” M. K. Hecht and W. C. Steere, W.C. (eds.) Evolutionary Biology, Vol.9, Plenum, New York, pp. 259-333, 1976.

[33] [33] D. Sigg, C. M. Thompson, and A. R. Mercer, “Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera (L.),” J. Neurosci., 17, pp. 7148-7156, 1997.

[34] [34] S. J. Simpson, A. R. McCaffery, B. F. Hagele, “A behavioural analysis of phase change in the desert locust. Biol. Rev., 74, pp. 461-480, 1999.

[35] [35] R. E. Snodgrass, “Anatomy of the Honey Bee,” Cornell Univ. Press, Ithaca, N.Y., 1956.

[36] [36] H. H. W. Velthuis, F. J. Verheijen, and A. J. Gottenbos, “Laying worker honey bee: similarities to the queen,” Nature, 207, p. 1314, 1965.

[37] [37] J. de Wilde and J. Beetsma, “The physiology of caste development in social insects,” Adv. Insect Physiol., 16, pp. 167-246, 1982.

[38] [38] M. L. Winston, “The Biology of the Honey Bee,” Harvard Univ. Press, Cambridge, Mass., 1987.

[39] [39] G. S. Withers, S. E. Fahrbach, and G. E. Robinson, “Selective neuroanatomical plasticity and division of labour in the honeybee,” Nature, 364, pp. 238-240, 1993.