The evolutionary transition from physical control to chemical regulation of worker reproduction - evidence from the primitively eusocial wasp Ropalidia marginata
Most insect societies can be classified as either primitively or highly eusocial. Primitively eusocial insect societies are usually led by queens who are morphologically indistinguishable from the workers and use aggression to control the workers, thereby typically holding top positions in the colony’s dominance hierarchy. Highly eusocial species have morphologically large queens who regulate worker reproduction through pheromones, and achieve larger colony sizes than their primitively eusocial counterparts. Ropalidia marginata is a primitively eusocial wasp, but queens in this species do not usually lead the colony's dominance hierarchy and use pheromones to signal their presence to workers. Since new colonies are founded by one or a few individuals and grow through time, young colonies are small enough to permit suppression of worker reproduction through aggression. Queens in small colonies indeed sometimes occupy the top position in the colony's dominance hierarchy. It is thus possible that queens in R. marginata switch from physical control to chemical regulation of worker reproduction within the life cycle of a colony. Alternately, queens might use pheromones to maintain their reproductive monopoly, irrespective of colony sizes, the queen's position in the dominance hierarchy being an artefact of colony size. We analysed data from 100 colonies of R. marginata to test these two competing hypotheses, and found support for the latter. Our findings are consistent with the hypothesis that the evolution of highly eusocial societies from primitively eusocial ones involved a one-step transition from physical control to chemical regulation of worker reproduction.
Alexander, R., K. Noonan, and B. Crespi. 1991. The evolution of eusociality. Pp. 3-44 in P. W. Sherman, J. U. M. Jarvis, and R. D. Alexander, eds. The Biology of the Naked Mole Rat. Princeton University Press, Princeton, New Jersey.
Bang, A., S. Deshpande, A. Sumana, and R. Gadagkar. 2010. Choosing an appropriate index to construct dominance hierarchies in animal societies: a comparison of three indices. Anim Behav 79:631-636.
Batra, S. W. T. 1966. Nests and social behavior of halictine bees of India (Hymenoptera: Halictidae). Indian Journal of Entomology 28:375-393.
Bhadra, A., A. Mitra, S. A. Deshpande, K. Chandrasekhar, D. G. Naik, A. Hefetz, and R. Gadagkar. 2010. Regulation of reproduction in the primitively eusocial wasp Ropalidia marginata: on the trail of the queen pheromone. Journal of chemical ecology 36:424-431.
Bhattacharya, K. and T. Vicsek. 2010. Collective decision making in cohesive flocks. New Journal of Physics 12:093019.
Bloch, G., A. Hefetz, and K. Hartfelder. 2000. Ecdysteroid titer, ovary status, and dominance in adult worker and queen bumble bees (Bombus terrestris). Journal of insect physiology 46:1033-1040.
Bourke, A. 1988. Dominance orders, worker reproduction, and queen-worker conflict in the slave-making ant Harpagoxenus sublaevis. Behavioral Ecology and Sociobiology 23:323-333.
Bourke, A. 1999. Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245-257.
Camazine, S., J.-L. Deneubourg, N. R. Franks, J. Sneyd, G. Theraulaz, and E. Bonabeau. 2003. Self-Organization in Biological Systems. Princeton University Press, Princeton, New Jersey.
Chandrashekara, K. and R. Gadagkar. 1991. Behavioural Castes, Dominance and Division of Labour in a Primitively Eusocial Wasp. Ethology 87:269-283.
Clarke, F. and C. Faulkes. 1997. Dominance and queen succession in captive colonies of the eusocial naked mole–rat, Heterocephalus glaber. Proc R Soc Lond B Biol Sci 264:993-1000.
Clutton-Brock, T., P. Brotherton, R. Smith, G. McIlrath, R. Kansky, D. Gaynor, M. O'riain, and J. Skinner. 1998. Infanticide and expulsion of females in a cooperative mammal. Proc R Soc Lond B Biol Sci 265:2291-2295.
Creel, S., N. M. Creel, M. G. Mills, and S. L. Monfort. 1997. Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behavioral Ecology 8:298-306.
Dapporto, L., A. Santini, F. R. Dani, and S. Turillazzi. 2007. Workers of a Polistes paper wasp detect the presence of their queen by chemical cues. Chemical senses 32:795-802.
Dietemann, V., C. Peeters, and B. Holldobler. 2005. Role of the queen in regulating reproduction in the bulldog ant Myrmeciagulosa: control or signalling? Anim Behav 69:777–784.
Faulkes, C. G. and N. C. Bennett. 2001. Family values: group dynamics and social control of reproduction in African mole-rats. Trends in Ecology and Evolution 16:184-190.
Fletcher, D. J. and K. G. Ross. 1985. Regulation of reproduction in eusocial Hymenoptera. Ann Rev Entomol 30:319-343.
Frank, L. G. 1986. Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction. Anim Behav 34:1510-1527.
Gabathuler, U., N. Bennett, and J. Jarvis. 1996. The social structure and dominance hierarchy of the Mashona mole‐rat, Cryptomys darlingi (Rodentia: Bathyergidae) from Zimbabwe. Journal of Zoology 240:221-231.
Gadagkar, R. 1991 Belonogaster, Mischocyttarus, Parapolybia, and Independent-founding Ropalidia. Pp. 149-190 in K. G. Ross, and R. W. Matthews, eds. The Social Biology of wasps. . Cornell University Press, Ithaca, New York.
Gadagkar, R. 2001. The social biology of Ropalidia marginata : toward understanding the evolution of eusociality. Harvard University Press, Cambridge, MA.
Heinze, J., B. Holldobler, and C. Peeters. 1994 Conflict and cooperation in ant societies. Naturwissenschaften. 81.:489–497.
Hölldobler, B. and E. O. Wilson. 1990. The Ants. Springer, Berlin.
Huston, M., L. Aarssen, M. Austin, B. Cade, J. Fridley, E. Garnier, J. Grime, J. Hodgson, W. Lauenroth, and K. Thompson. 2000. No consistent effect of plant diversity on productivity. Science 289:1255a-1255.
Jacobs, D., N. Bennett, J. Jarvis, and T. Crowe. 1991. The colony structure and dominance hierarchy of the Damaraland mole‐rat, Cryptomys damarensis (Rodentia: Bathyergidae), from Namibia. Journal of Zoology 224:553-576.
Jeanne, R. L. 1972. Social biology of the neotropical wasp Mischocyttarus drewseni. Bulletin of the Museum of Comparative Zoology 144:63 - 150.
Kardile, S. and R. Gadagkar. 2002. Docile sitters and active fighters in paper wasps: a tale of two queens. Die Naturwissenschaften 89:176-179.
Keane, B., P. Waser, S. Creel, N. Creel, L. Elliott, and D. Minchella. 1994. Subordinate reproduction in dwarf mongooses. Anim Behav 47:65-75.
Keller, L. and P. Nonacs. 1993. The role of queen pheromones in social insects: Queen control or queen signal? Animal Behaviour. 45:787-794.
Koenig, W. D., J. Haydock, and M. T. Stanback. 1998. Reproductive roles in the cooperatively breeding acorn woodpecker: incest avoidance versus reproductive competition. American Naturalist 151:243-255.
Kolmer, K. and J. Heinze. 2000. Rank orders and division of labour among unrelated cofounding ant queens. Proc R Soc Lond B Biol Sci 267:1729-1734.
Lytle, D. A. 2001. Convergent growth regulation in arthropods: biological fact or statistical artifact? Oecologia 128:56-61.
Michener, C. D. 1969. Comparative social behavior of bees. Ann Rev Entomol 14:299-342.
Mitra, A. and R. Gadagkar. 2011. Can Dufour's gland compounds honestly signal fertility in the primitively eusocial wasp Ropalidia marginata? Die Naturwissenschaften 98:157-161.
Mitra, A. and R. Gadagkar. 2012a. Queen signal should be honest to be involved in maintenance of eusociality: chemical correlates of fertility in Ropalidia marginata. Insectes Sociaux 59:251-255.
Mitra, A. and R. Gadagkar. 2012b. Road to Royalty - Transition of Potential Queen to Queen in the Primitively Eusocial Wasp Ropalidia marginata. Ethology 118:694 - 702.
Monnin, T. and C. Peeters. 1999. Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behavioral Ecology 10:323-332.
Monnin, T., F. L. Ratnieks, and C. R. Brandão. 2003. Reproductive conflict in animal societies: hierarchy length increases with colony size in queenless ponerine ants. Behavioral Ecology and Sociobiology 54:71-79.
Nachman, G. and K. E. Heller. 1999. Fluctuating asymmetry as an index of fitness: causality or statistical artifact? Oikos:357-365.
Noirot, C. and J. Pasteels. 1988. The worker caste is polyphyletic in termites. Sociobiology 14:15-20.
Pardi, L. 1948. Dominance order in Polistes wasps. Physiological Zoology. 21:1-13.
Poston, J. P. 1997. Dominance, access to colonies, and queues for mating opportunities by male boat-tailed grackles. Behavioral Ecology and Sociobiology 41:89-98.
Premnath, S., K. Chandrashekara, S. Chandran, and R. Gadagkar. 1990. Constructing Dominance hierarchies in a primitively eusocial wasp. In: Social Insects and the Environment. Pp. 80 in G. K. Veeresh, B. Mallik, and C. A. Viraktamath., eds. Proceedings of 11th International Congress of IUSSI, Bangalore, India, August, 1990. Oxford & IBH Publishing Co. Ltd., New Delhi.
Premnath, S., A. Sinha, and R. Gadagkar. 1995. Regulation of worker activity in a primitively eusocial wasp, Ropalidia marginata. Behavioral Ecology 6:117 - 123.
R Core Team. 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Reeve, H. K. 1991. Polistes. Pp. 99–148. in K. G. Ross, and R. W. Matthews, eds. The social biology of wasps. Cornell University Press., Ithaca.
Reeve, H. K. and G. J. Gamboa. 1983. Colony activity integration in primitively eusocial wasps: the role of the queen (Polistes fuscatus, Hymenoptera: Vespidae). Behavioral Ecology and Sociobiology 13:63-74.
Reeve, H. K. and G. J. Gamboa. 1987. Queen regulation of worker foraging in paper wasps: a social feedback control system (Polistes fuscatus, Hymenoptera: Vespidae). Behaviour 102:147-167.
Röseler, P. 1991. Reproductive competition during colony establishment. Pp. 309-335 in K. G. Ross, and R. W. Matthews, eds. The Social Biology of Wasps. Cornell University Press, Ithaca.
Rosenthal, C., N. Bennett, and J. Jarvis. 1992. The changes in the dominance hierarchy over time of a complete field‐captured colony of Cryptomys hottentotus hottentotus. Journal of Zoology 228:205-226.
Ross, K. G. and R. W. Matthews. 1991. The Social biology of wasps. Cornell University Press, Ithaca.
Schwarz, M. P. and R. E. Woods. 1994. Order of adult eclosion is a major determinant of reproductive dominance in the allodapine bee Exoneura bicolor. Anim Behav 47:373-378.
Sledge, M. F., F. Boscaro, and S. Turillazzi. 2001. Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behavioral Ecology and Sociobiology 49:401-409.
Stacey, P. B. and W. D. Koenig. 1990. Cooperative breeding in birds: long term studies of ecology and behaviour. Cambridge University Press.
Sumana, A., S. A. Deshpande, A. Bhadra, and R. Gadagkar. 2008. Workers of the primitively eusocial wasp Ropalidia marginata do not perceive their queen across a wire mesh partition. Journal of Ethology 26:207-212.
Sumana, A. and R. Gadagkar. 2003 Ropalidia marginata – a primitively eusocial wasp society headed by docile queens. Curr Sci 84:1464 - 1468.
Theraulaz, G., M. Pratte, and J. Gervet. 1989. Effects of removal of α-individuals from a Polistes dominulus Christ wasp society: changes in behavioural patterns resulting from hierarchical changes. Actes des Colloques Insectes Sociaux 5:169-179.
Turillazzi, S. 1985. Colonial cycle of Parischnogaster nigricans serrei (Du Buysson) in west Java (Hymenoptera Stenogastrinae). Insectes Sociaux 32:43-60.
Van Doorn, A. and J. Heringa. 1986. The ontogeny of a dominance hierarchy in colonies of the Bumblebee Bombus terrestris (Hymenoptera, Apidae). Insectes Sociaux 33:3-25.
Wallace, E. and N. Bennett. 1998. The colony structure and social organization of the giant Zambian mole-rat, Cryptomys mechowi. Journal of Zoology 244:51-61.
West-Eberhard, M. J. 1969. The social biology of polistine wasps. Museum of Zoology, University of Michigan, Ann Arbor,.
West-Eberhard, M. J. 1977. The establishment of reproductive dominance in social wasp colonies. Pp. 223–227. 8th InternationalCongress International Union Study of Social Insects., Wageningen,The Netherlands.
Wilson, E. O. 1971. The Insect Societies. The Belknap Press of Harvard University Press., Cambridge, MA.
Wilson, E. O. 1975. Sociobiology: The New Synthesis. Pp. 697. Belknap Press of Harvard University Press, Cambirdge, MA.