Models of division of labor in social insects.

Division of labor is one of the most basic and widely studied aspects of colony behavior in social insects. Studies of division of labor are concerned with the integration of individual worker behavior into colony level task organization and with the question of how regulation of division of labor may contribute to colony efficiency. Here we describe and critique the current models concerned with the proximate causes of division of labor in social insects. The models have identified various proximate mechanisms to explain division of labor, based on both internal and external factors. On the basis of these factors, we suggest a classification of the models. We first describe the different types of models and then review the empirical evidence supporting them. The models to date may be considered preliminary and exploratory; they have advanced our understanding by suggesting possible mechanisms for division of labor and by revealing how individual and colony-level behavior may be related. They suggest specific hypotheses that can be tested by experiment and so may lead to the development of more powerful and integrative explanatory models.

[1]  F. D. The Social Insects: their Origin and Evolution , 1928, Nature.

[2]  Edward O. Wilson,et al.  The Ergonomics of Caste in the Social Insects , 1968, The American Naturalist.

[3]  E. Wilson The Insect Societies , 1974 .

[4]  E. R. Jaycox,et al.  Behavioral Changes in Worker Honey Bees (Apis mellifera) Induced by Injections of a Juvenile Hormone Mimic , 1974 .

[5]  Charles D. Michener,et al.  The Social Behavior of the Bees , 1974 .

[6]  Michael Möglich,et al.  Social Carrying Behavior and Division of Labor During Nest Moving in Ants , 1974 .

[7]  J. Traniello,et al.  Caste in a Primitive Ant: Absence of Age Polyethism in Amblyopone , 1978, Science.

[8]  Caste and ecology in the social insects , 1979 .

[9]  A. Collins Effect of age on the response to alarm pheromones by caged honey bees. , 1980 .

[10]  P. Hogeweg,et al.  Socioinformatic processes: MIRROR modelling methodology , 1985 .

[11]  R. Hellmich,et al.  Selection for high and low pollenhoarding honey bees , 1985 .

[12]  E O Wilson,et al.  The Sociogenesis of Insect Colonies , 1985, Science.

[13]  Deborah M. Gordon,et al.  The dynamics of the daily round of the harvester ant colony (Pogonomyrmex barbatus) , 1986, Animal Behaviour.

[14]  M. Winston,et al.  The influence of age and task specialization on the production and perception of honey bee pheromones , 1987 .

[15]  H. Reeve,et al.  Queen regulation of worker foraging in paper wasps: a social feedback control system (Polistes fuscatus, Hymenoptera: Vespidae) , 1987 .

[16]  Edward O. Wilson,et al.  Causes of ecological success: the case of the ants. The sixth tansley lecture , 1987 .

[17]  J. Deneubourg,et al.  Self-organization mechanisms in ant societies. II: Learning in foraging and division of labor , 1987 .

[18]  Deborah M. Gordon,et al.  Group-level dynamics in harvester ants: young colonies and the role of patrolling , 1987, Animal Behaviour.

[19]  G. Robinson,et al.  Genetic basis for division of labor in an insect society , 1989 .

[20]  G. Robinson,et al.  Hormonal and Genetic Control of Behavioral Integration in Honey Bee Colonies , 1989, Science.

[21]  Deborah M. Gordon,et al.  Dynamics of task switching in harvester ants , 1989, Animal Behaviour.

[22]  J. Deneubourg,et al.  Collective patterns and decision-making , 1989 .

[23]  Robert E. Page,et al.  Self Organization and Adaptation in Insect Societies , 1990, PSA: Proceedings of the Biennial Meeting of the Philosophy of Science Association.

[24]  G. Robinson,et al.  Juvenile hormone does not affect division of labor in bumble bee colonies (Hymenoptera: Apidae). , 1990 .

[25]  R. E. Page,et al.  The Genetics of Division of Labour in Honey Bee Colonies , 1991 .

[26]  Gene E. Robinson,et al.  Hormonal regulation of behavioural development in the honey bee is based on changes in the rate of juvenile hormone biosynthesis , 1991 .

[27]  S. Camazine,et al.  A model of collective nectar source selection by honey bees , 1991 .

[28]  Guy Theraulaz,et al.  Social Regulation of Foraging Activities in Polistes Dominulus Christ: a Systemic Approach To Behavioural Organization , 1991 .

[29]  Genotypic variability for rates of behavioral development in worker honeybees (Apis mellifera L.) , 1992 .

[30]  B. Goodwin,et al.  A Parallel Distributed Model of the Behaviour of Ant Colonies , 1992 .

[31]  G. Robinson Regulation of division of labor in insect societies. , 1992, Annual review of entomology.

[32]  Chris Tofts,et al.  Doing the right thing: Ants, honeybees and naked mole-rats. , 1992, Trends in ecology & evolution.

[33]  G. Robinson,et al.  Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[34]  G. Robinson,et al.  Selective neuroanatomical plasticity and division of labour in the honeybee , 1993, Nature.

[35]  L. E. Snyder Non-random behavioural interactions among genetic subgroups in a polygynous ant , 1993, Animal Behaviour.

[36]  Chris Tofts Algorithms for task allocation in ants. (A study of temporal polyethism: Theory) , 1993 .

[37]  Sean O'Donnell,et al.  Methoprene accelerates age polyethism in workers of a social wasp (Polybia occidentalis) , 1993 .

[38]  Nigel R. Franks,et al.  Task allocation in ant colonies within variable environments (A study of temporal polyethism: Experimental) , 1993 .

[39]  G. Robinson,et al.  Temporal polyethism in social insects is a developmental process , 1994, Animal Behaviour.

[40]  N. Franks,et al.  Social resilience in individual worker ants and its role in division of labour , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[41]  N. Franks,et al.  Foraging for work: how tasks allocate workers , 1994, Animal Behaviour.

[42]  N. Franks,et al.  Social Evolution in Ants , 2019 .

[43]  G. Theraulaz,et al.  Nest building in a social wasp: postures and constraints (Hymenoptera: Vespidae) , 1995 .

[44]  T. Seeley The Wisdom of the Hive , 1995 .

[45]  Guy Theraulaz,et al.  Modelling the Collective Building of Complex Architectures in Social Insects with Lattice Swarms , 1995 .

[46]  Scott Camazine,et al.  Self-Organized Thermoregulation of Honeybee Clusters , 1995 .

[47]  G. Robinson,et al.  Genotypic constraints on plasticity for corpse removal in honey bee colonies , 1995, Animal Behaviour.

[48]  N. Franks,et al.  Spatial relationships within nests of the ant Leptothorax unifasciatus (Latr.) and their implications for the division of labour , 1995, Animal Behaviour.

[49]  N. Calderone Temporal division of labor in the honey bee, Apis mellifera A developmental process or the result of environmental influences? , 1995 .

[50]  N. Calderone,et al.  Temporal polyethism and behavioural canalization in the honey bee, Apis mellifera , 1996, Animal Behaviour.

[51]  Regulation of nectar collection in relation to honey storage levels by honey bees, Apis mellifera , 1996 .

[52]  G. Robinson,et al.  Regulation of honey bee division of labor by colony age demography , 1996, Behavioral Ecology and Sociobiology.

[53]  ROBERT L. JEANNE,et al.  Regulation of nest construction behaviour in Polybia occidentalis , 1996, Animal Behaviour.

[54]  S. O’Donnell,et al.  RAPD markers suggest genotypic effects on forager specialization in a eusocial wasp , 1996, Behavioral Ecology and Sociobiology.

[55]  E. Bonabeau,et al.  Quantitative study of the fixed threshold model for the regulation of division of labour in insect societies , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  D. Gordon The organization of work in social insect colonies , 1996, Nature.

[57]  R E Page,et al.  The evolution of insect societies. , 1997, Endeavour.

[58]  J. Traniello,et al.  Ecology, evolution and division of labour in social insects , 1997, Animal Behaviour.

[59]  S. Fahrbach Regulation of Age Polyethism in Bees and Wasps by Juvenile Hormone , 1997 .

[60]  N. Franks,et al.  Studies of the division of labour: neither physics nor stamp collecting , 1997, Animal Behaviour.

[61]  S. Beshers,et al.  Division of labour and ‘foraging for work’: simulating reality versus the reality of simulations , 1997, Animal Behaviour.

[62]  Sandra D. Mitchell,et al.  Self-organization and the evolution of division of labor , 1998 .

[63]  Guy Theraulaz,et al.  Response Threshold Reinforcement and Division of Labor in Insect Societies , 1998 .

[64]  G. Theraulaz,et al.  Response threshold reinforcements and division of labour in insect societies , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[65]  J. Erber,et al.  The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.) , 1998, Journal of Comparative Physiology A.

[66]  E. Bonabeau,et al.  Fixed response thresholds and the regulation of division of labor in insect societies , 1998 .

[67]  S. O’Donnell Genetic effects on task performance, but not on age polyethism, in a swarm-founding eusocial wasp , 1998, Animal Behaviour.

[68]  Karl Crailsheim,et al.  Protein trophallaxis and the regulation of pollen foraging by honey bees (Apis mellifera L.) , 1998 .

[69]  Iain D. Couzin,et al.  The Dynamics of Specialization and Generalization within Biological Populations , 1998, Adv. Complex Syst..

[70]  S. O’Donnell Dominance and polyethism in the eusocial wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae) , 1998, Behavioral Ecology and Sociobiology.

[71]  G. Robinson,et al.  Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers. , 1998, Journal of insect physiology.

[72]  Deneubourg,et al.  Group and mass recruitment in ant colonies: the influence of contact rates , 1998, Journal of theoretical biology.

[73]  Gene E. Robinson,et al.  Social control of division of labor in honey bee colonies , 1999 .

[74]  G. Robinson,et al.  Biogenic amines and division of labor in honey bee colonies , 1999, Journal of Comparative Physiology A.

[75]  Robert E. Page,et al.  The emergence of division of labour in forced associations of normally solitary ant queens , 1999 .

[76]  S. Cahan,et al.  Undertaking specialization in the desert leaf-cutter ant Acromyrmex versicolor , 1999, Animal Behaviour.

[77]  Susan M. Bertram,et al.  Division of labor in a dynamic environment: response by honeybees (Apis mellifera) to graded changes in colony pollen stores , 1999, Behavioral Ecology and Sociobiology.

[78]  G. Robinson,et al.  Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies , 1999, Journal of Comparative Physiology A.

[79]  Naug,et al.  Flexible division of labor mediated by social interactions in an insect colony-a simulation model , 1999, Journal of theoretical biology.

[80]  Guy Theraulaz,et al.  Dominance orders in animal societies: The self-organization hypothesis revisited , 1999, Bulletin of mathematical biology.

[81]  Jay E. Mittenthal,et al.  Response thresholds and division of labor in insect colonies. , 1999 .

[82]  Jean-Louis Deneubourg,et al.  Information Processing in Social Insects , 1999, Birkhäuser Basel.

[83]  Walter R. Tschinkel,et al.  Ritualized conflict in Odontomachus brunneus and the generation of interaction-based task allocation: a new organizational mechanism in ants , 1999, Animal Behaviour.

[84]  J. Deneubourg,et al.  Self-organized defensive behavior in honeybees. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[85]  Guy Theraulaz,et al.  Role and variability of response thresholds in the regulation of division of labor in insect societies , 1999 .

[86]  P. Visscher,et al.  House-hunting by honey bee swarms: collective decisions and individual behaviors , 1999, Insectes Sociaux.

[87]  T. Pankiw,et al.  Response thresholds to sucrose predict foraging division of labor in honeybees , 2000, Behavioral Ecology and Sociobiology.

[88]  Gene E. Robinson,et al.  Juvenile Hormone Paces Behavioral Development in the Adult Worker Honey Bee , 2000, Hormones and Behavior.

[89]  David R. Tarpy,et al.  Perception of the pollen need by foragers in a honeybee colony , 2000, Animal Behaviour.

[90]  J. Fewell,et al.  Colony-level selection effects on individual and colony foraging task performance in honeybees, Apis mellifera L. , 2000, Behavioral Ecology and Sociobiology.

[91]  G. Robinson,et al.  Social inhibition and the regulation of temporal polyethism in honey bees. , 2001, Journal of theoretical biology.

[92]  Gene E. Robinson,et al.  Octopamine influences division of labor in honey bee colonies , 2001, Journal of Comparative Physiology A.

[93]  C. Baer,et al.  Population genomics: genome-wide sampling of insect populations. , 2001, Annual review of entomology.