Final Report Summary - IDENTITY CODE (Behavioural syndromes, division of labour and communication of identity in complex insect societies)
‘Identity Code’ -Behavioural syndromes, division of labour and communication of identity in complex insect societies-
project website: http://identitycode.weebly.com
Individual variation is ubiquitous in nature. It is probable very important to be different, for instance, in morphology, life-history traits and behaviour. The persistence of individual variation might appear perplexing, because if traits influencing reproductive success and survival are heritable, individuals that do not perform optimally in a given environment should be penalized by natural selection and would eventually disappear from the population. We nevertheless observe phenotypic variation in all living forms around us and this is maintained under natural selection. In humans, one of the most familiar forms of individual variation that we can observe concerns personality. Humans indeed tend to behave consistently over time and across different situations. To date, most studies on animal personality (behavioural syndromes) have focussed on few model organisms with absent, or relatively simple, social structure. ‘Identity Code’ explored behavioural syndromes in one of the most advanced and successful animal societies: the ants.
Social recognition is a key component of any well functioning society. Social insects -ants in particular, with their multifaceted societies- represent the pinnacle of social evolution. Their ecological success is the result of an extremely well organized society, often based on extensive division of labour. This includes reproduction, with one or few individuals devoted to egg-laying (queens), while the majority of the society members contribute to colony maintenance (workers). The extent to which this labour partitioning is implemented depends on the efficiency of communication strategies. In particular, the communication of identity: the who’s who? of an ant society.
Identity is typically communicated via the chemical channel by multi-component cues (e.g. hydrocarbons present on the insect cuticle) that encode multiple messages allowing recognition of identity at different levels: the inter-individual, the within-colony and the between-colony level (d’Ettorre & Moore 2008; d’Ettorre & Lenoir 2010; van Zweden & d’Ettorre 2010; Bos & d’Ettorre 2012; d’Ettorre 2013). How effectively individual or group identity can be detected may depend on the behavioural type of the receiver, but this has not been systematically explored in social insects. Therefore, the project ‘Identity Code’ tried to bridge this gap with an interdisciplinary and integrated approach.
Highlights of the main results achieved by the ‘Identity Code’ project:
- Context dependent behavioural strategies
Worker carpenter ant that are sick (experimentally induced sickness), become unsociable, in the sense that they are more aggressive towards foreigner ants (similarly to humans); moreover they leave the natal nest in order to avoid social contact with their healthy nestmates, thus preventing disease-spreading (Bos et al 2012a). In a different but comparable situation, young virgin queens of leaf-cutter ants that fail to mate and disperse, assume worker roles (brood care, colony defense) to help their natal colony to grow and reproduce (Nehring et al 2012). These two examples show that despite behavioural types and roles are constant by definition, natural selection provides individuals with adaptive behavioural flexibility.
- Communication of queen identity and regulation of reproduction
The ant queen typically has the monopoly of reproduction and she need to signal to her workers that she is healthy and productive, for workers will only help queens that assure their procreative role, which increases their indirect fitness (reproductive success). The queen signal is a pheromone, which chemically regulate worker reproduction. This signal has been identified for the first time in the back garden ant (Holman et al 2010). We also discovered that queens might be inhibited by their own pheromone, so that regulation of productivity works via negative feedback 5Holman et al 2013a). Moreover, this pheromone is evolutionary conserved among the ant genus Lasius. This is the first known case of universal queen pheromone (Holman et al 2013b).
- Perception of biologically relevant chemical compounds and learning abilities
To understand the chemical communication code of ants it is necessary to explore their perceptual and learning abilities. We made the first innovative steps to unravel the mechanisms used by ants to communicate social identity by characterizing perceptual similarity of cuticular hydrocarbons (Bos et al 2012b, 2013), learning and memory abilities (Guerrieri et al 2011), and the link between sucrose responsiveness, learning success and task specialization (Perez et al. 2013).
The results highlighted here, together with the others achievements of the project ‘Identity Code’, give a substantial and novel contribution to our understanding of the organization of societies and the pivotal role of individual identity in social interactions.
o Bos N. & d’Ettorre P. (2012) Recognition of social identity in ants. Frontiers in Psychology 3: 83
o Bos N., Lefèvre T., Bruun-Jensen A., d’Ettorre P. (2012a) Sick ants become unsociable. J Evol Biol 25, 342-
o Bos N., Dreier S., Jørgensen C.G. Nielsen J., Guerrieri F.J. d’Ettorre P. (2012b) Learning and perceptual similarity among cuticular hydrocarbons in ants. J Insect Physiol, 58,138-46.
o Bos N., d’Ettorre P., Guerrieri F.J. (2013). Chemical structure of odorants and perceptual similarity in ants. Journal of Experimental Biology (online early).
o d’Ettorre P., Moore, A.J. (2008) Chemical communication and the coordination of social interactions in insects. In: d’Ettorre, P., Hughes, D.P. (eds) Sociobiology of communication. Oxford University Press, Oxford, pp. 81-96.
o d’Ettorre P.,Lenoir, A. (2010) Nestmate recognition. In: Lach, L., Parr, C., Abbott, K. (eds) Ant Ecology. Oxford University Press, Oxford, pp 194-209.
o d’Ettorre P. (2013). Learning and Recognition of Identity in Ants. In: Menzel R., Benjamin P.R. (eds) Invertebrate Learning and Memory, Elsevier, San Diego: Academic Press, pp. 501-513. ISBN: 978-0-12-415823-8
o Guerrieri F.J. d’Ettorre P. , Devaud J-M & Giurfa M. (2011) Long-term olfactory memories are stabilised via protein synthesis in Camponotus fellah ants. J Exp Biol 214, 3300-3304
o Holman L., Jørgensen C.G. Nielsen J., d’Ettorre P. (2010) Identification of an ant queen pheromone regulating worker sterility. Proceedings Royal Society London B, 277: 3793-3800.
o Holman L., Leroy C., Jørgensen C.G. Nielsen J., d’Ettorre P. (2013a). Are queen ants inhibited by their own pheromone? Regulation of productivity via negative feedback. Behavioural Ecology, 24: 380-385.
o Holman L., Lanfear R., d’Ettorre P. (2013b). The evolution of queen pheromones in the ant genus Lasius. Journal of Evolutionary Biology (online early).
o Nehring V., Boomsma J.J. d’Ettorre P. (2012) Wingless virgin queens assume helper roles in Acromyrmex leaf-cutting ants. Current Biology 22, R671-673.
o Perez M., Rolland U., Giurfa M., d’Ettorre P. (2013). Sucrose responsiveness, learning success, and task specialization in ants. Learning & Memory (in press).
o van Zweden, J.S. d’Ettorre P.,(2010) The role of hydrocarbons in nestmate recognition. In: Blomquist, G.C. Bagnères, A.-G. (eds) Insect Hydrocarbons: Biology, Biochemistry and Chemical Ecology. Cambridge University Press, Cambridge, pp 222-243.
project website: http://identitycode.weebly.com
Individual variation is ubiquitous in nature. It is probable very important to be different, for instance, in morphology, life-history traits and behaviour. The persistence of individual variation might appear perplexing, because if traits influencing reproductive success and survival are heritable, individuals that do not perform optimally in a given environment should be penalized by natural selection and would eventually disappear from the population. We nevertheless observe phenotypic variation in all living forms around us and this is maintained under natural selection. In humans, one of the most familiar forms of individual variation that we can observe concerns personality. Humans indeed tend to behave consistently over time and across different situations. To date, most studies on animal personality (behavioural syndromes) have focussed on few model organisms with absent, or relatively simple, social structure. ‘Identity Code’ explored behavioural syndromes in one of the most advanced and successful animal societies: the ants.
Social recognition is a key component of any well functioning society. Social insects -ants in particular, with their multifaceted societies- represent the pinnacle of social evolution. Their ecological success is the result of an extremely well organized society, often based on extensive division of labour. This includes reproduction, with one or few individuals devoted to egg-laying (queens), while the majority of the society members contribute to colony maintenance (workers). The extent to which this labour partitioning is implemented depends on the efficiency of communication strategies. In particular, the communication of identity: the who’s who? of an ant society.
Identity is typically communicated via the chemical channel by multi-component cues (e.g. hydrocarbons present on the insect cuticle) that encode multiple messages allowing recognition of identity at different levels: the inter-individual, the within-colony and the between-colony level (d’Ettorre & Moore 2008; d’Ettorre & Lenoir 2010; van Zweden & d’Ettorre 2010; Bos & d’Ettorre 2012; d’Ettorre 2013). How effectively individual or group identity can be detected may depend on the behavioural type of the receiver, but this has not been systematically explored in social insects. Therefore, the project ‘Identity Code’ tried to bridge this gap with an interdisciplinary and integrated approach.
Highlights of the main results achieved by the ‘Identity Code’ project:
- Context dependent behavioural strategies
Worker carpenter ant that are sick (experimentally induced sickness), become unsociable, in the sense that they are more aggressive towards foreigner ants (similarly to humans); moreover they leave the natal nest in order to avoid social contact with their healthy nestmates, thus preventing disease-spreading (Bos et al 2012a). In a different but comparable situation, young virgin queens of leaf-cutter ants that fail to mate and disperse, assume worker roles (brood care, colony defense) to help their natal colony to grow and reproduce (Nehring et al 2012). These two examples show that despite behavioural types and roles are constant by definition, natural selection provides individuals with adaptive behavioural flexibility.
- Communication of queen identity and regulation of reproduction
The ant queen typically has the monopoly of reproduction and she need to signal to her workers that she is healthy and productive, for workers will only help queens that assure their procreative role, which increases their indirect fitness (reproductive success). The queen signal is a pheromone, which chemically regulate worker reproduction. This signal has been identified for the first time in the back garden ant (Holman et al 2010). We also discovered that queens might be inhibited by their own pheromone, so that regulation of productivity works via negative feedback 5Holman et al 2013a). Moreover, this pheromone is evolutionary conserved among the ant genus Lasius. This is the first known case of universal queen pheromone (Holman et al 2013b).
- Perception of biologically relevant chemical compounds and learning abilities
To understand the chemical communication code of ants it is necessary to explore their perceptual and learning abilities. We made the first innovative steps to unravel the mechanisms used by ants to communicate social identity by characterizing perceptual similarity of cuticular hydrocarbons (Bos et al 2012b, 2013), learning and memory abilities (Guerrieri et al 2011), and the link between sucrose responsiveness, learning success and task specialization (Perez et al. 2013).
The results highlighted here, together with the others achievements of the project ‘Identity Code’, give a substantial and novel contribution to our understanding of the organization of societies and the pivotal role of individual identity in social interactions.
o Bos N. & d’Ettorre P. (2012) Recognition of social identity in ants. Frontiers in Psychology 3: 83
o Bos N., Lefèvre T., Bruun-Jensen A., d’Ettorre P. (2012a) Sick ants become unsociable. J Evol Biol 25, 342-
o Bos N., Dreier S., Jørgensen C.G. Nielsen J., Guerrieri F.J. d’Ettorre P. (2012b) Learning and perceptual similarity among cuticular hydrocarbons in ants. J Insect Physiol, 58,138-46.
o Bos N., d’Ettorre P., Guerrieri F.J. (2013). Chemical structure of odorants and perceptual similarity in ants. Journal of Experimental Biology (online early).
o d’Ettorre P., Moore, A.J. (2008) Chemical communication and the coordination of social interactions in insects. In: d’Ettorre, P., Hughes, D.P. (eds) Sociobiology of communication. Oxford University Press, Oxford, pp. 81-96.
o d’Ettorre P.,Lenoir, A. (2010) Nestmate recognition. In: Lach, L., Parr, C., Abbott, K. (eds) Ant Ecology. Oxford University Press, Oxford, pp 194-209.
o d’Ettorre P. (2013). Learning and Recognition of Identity in Ants. In: Menzel R., Benjamin P.R. (eds) Invertebrate Learning and Memory, Elsevier, San Diego: Academic Press, pp. 501-513. ISBN: 978-0-12-415823-8
o Guerrieri F.J. d’Ettorre P. , Devaud J-M & Giurfa M. (2011) Long-term olfactory memories are stabilised via protein synthesis in Camponotus fellah ants. J Exp Biol 214, 3300-3304
o Holman L., Jørgensen C.G. Nielsen J., d’Ettorre P. (2010) Identification of an ant queen pheromone regulating worker sterility. Proceedings Royal Society London B, 277: 3793-3800.
o Holman L., Leroy C., Jørgensen C.G. Nielsen J., d’Ettorre P. (2013a). Are queen ants inhibited by their own pheromone? Regulation of productivity via negative feedback. Behavioural Ecology, 24: 380-385.
o Holman L., Lanfear R., d’Ettorre P. (2013b). The evolution of queen pheromones in the ant genus Lasius. Journal of Evolutionary Biology (online early).
o Nehring V., Boomsma J.J. d’Ettorre P. (2012) Wingless virgin queens assume helper roles in Acromyrmex leaf-cutting ants. Current Biology 22, R671-673.
o Perez M., Rolland U., Giurfa M., d’Ettorre P. (2013). Sucrose responsiveness, learning success, and task specialization in ants. Learning & Memory (in press).
o van Zweden, J.S. d’Ettorre P.,(2010) The role of hydrocarbons in nestmate recognition. In: Blomquist, G.C. Bagnères, A.-G. (eds) Insect Hydrocarbons: Biology, Biochemistry and Chemical Ecology. Cambridge University Press, Cambridge, pp 222-243.