Chemical cues and how ants use them for recognizing colony members
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The most sophisticated form of altruism is found in eusocial insects, with workers usually sacrificing their own reproduction in order to support their mother (queen) in raising offspring (workers, virgin queens and males). Altruistic acts ultimately increase the workers’ indirect fitness, but only when directed towards relatives. Indeed, individuals from the same colony (nestmates) are usually all related and workers rigorously defend their colony against individuals from foreign con- and heterospecific colonies (non-nestmates). Ants are amazingly fast and accurate in discrimination of non-nestmates, however, in rare cases social parasites sneak into and live within a host colony exploiting its resources. Recognition of nestmates and discrimination from non-nestmates is based on mixtures of low-volatile components present on each individuals’ exoskeleton (cuticular hydrocarbons: CHCs). CHC profiles are species-specific and CHC profiles of individuals from neighboring conspecific colonies usually only differ in the quantitative ratios of CHCs. The individuals’ CHC profiles are further influenced by environmental factors and a frequent exchange of CHCs between nestmates results in a uniformation of CHC profiles of nestmates. However, inter-individual, task-specific differences in CHC profiles remain. The neuronal basis of nestmate recognition is unknown, but it is generally assumed that the nestmate recognition process is based on a process of label-template matching where the CHC profile of an encountered ant (label) is compared with a neural representation of the own colony odor (template). When label and template match, the encounter ant is recognized as nestmate and when they mismatch, the encounter ant is recognized as non-nestmate. An encounter of non-nestmates often results in aggression. Importantly, since the CHC profiles change over time due to environmental influences, the template needs to be up- dated. In this thesis, I investigated different levels of nestmate recognition in ants. Specifically, I focused on which CHCs are produced, how CHC profiles are perceived, how the behavioral response is influenced by experience, and how CHC profiles are encoded and decoded in the brain.
In chapter 1, I investigate a host-social parasite system, where a social parasitic ant (Megalomyrmex symmetochus) parasitizes a colony of a fungus-growing ant (Sericomyrmex amabilis). I show that the CHC profiles of the two species are distinct and the parasite shares only a single hydrocarbon with its host. Furthermore, the parasite has fewer CHCs and in an overall lower quantity than its host, suggesting that the parasite uses a ’chemical insignificant’ strategy. My behavioral experiments provide evidence that colonies both with and without parasites discriminate between nestmates and conspecific non-nestmates and that parasites are not ‘chemically hidden’ but are in fact detected and attacked by host ants that are not familiar with parasites. Furthermore, I find that volatile chemicals emitted by the parasites likely induce submission responses in host ants. The results show that parasites do not need to match the label of their host, but use volatile chemicals in order to manipulate members of the host colony.
In chapter 2, I investigate in carpenter ants (Camponotus floridanus) how specific manipulations of CHC profiles of individuals originating from the same source colony influence their nestmate recognition. I provide evidence that ants can adjust to novel CHC profiles, while the previous CHC profiles are still accepted as nestmate. Furthermore, I find that not only an addition but also a lack of a hydrocarbon can lead to a discrimination as non-nestmate and I provide the first evidence that ants can form novel templates for nestmates.
In chapter 3, I investigate the influence of recent presence of nestmates (social context) on the propensity of aggression response towards non-nestmates in the territorial red wood ant, Formica rufa. When kept in a group of nestmates, workers showed a high probability of aggression against non-nestmates whereas the lack of social context reduces the workers’ probability of aggression against non-nestmates. Thus, social context is necessary to maintain or induce a physiological state in workers that allows aggression response against non-nestmates. Furthermore, my results suggest that the nestmate recognition system can be utilized at remote sites for an adaptive and flexible tuning of the response against competitors.
For chapter 4, I collected data on the encoding of colony odors in the first olfactory neuropil in the brain of ants (C. floridanus) using functional imaging at high-speed and standard frame recording of calcium signals, and I developed a method for simultaneously monitoring the behavioral response of a mounted ant while measuring calcium signals. The data set of this investigation is not complete and therefore this part has to be considered as pilot study for future experiments.
The four studies, compiled in my thesis revealed novel insights to several aspects of nestmate recognition in ants: Nestmate recognition depends on previous experience of individuals, and ants can store multiple templates for different nestmate labels and can discriminate them from similar non-nestmate labels. Furthermore, the behavioral response towards conspecific non-nestmates depends on recent social contact with nestmates. My data also shed light into host-parasite relationships and broadens our understanding on how parasites circumvent the nestmate recognition system of their host. Additionally, I provide a new, testable hypothesis on how nestmate recognition is implemented in the ant brain. Taken together, my studies provide solid bases for future experiments on the proximate mechanisms of nestmate recognition, learning and classification of labels and modulation of decision-making through changes of an individual’s internal state.
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NEUPERT, Stefanie, 2018. Chemical cues and how ants use them for recognizing colony members [Dissertation]. Konstanz: University of KonstanzBibTex
@phdthesis{Neupert2018Chemi-43633, year={2018}, title={Chemical cues and how ants use them for recognizing colony members}, author={Neupert, Stefanie}, address={Konstanz}, school={Universität Konstanz} }
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Indeed, individuals from the same colony (nestmates) are usually all related and workers rigorously defend their colony against individuals from foreign con- and heterospecific colonies (non-nestmates). Ants are amazingly fast and accurate in discrimination of non-nestmates, however, in rare cases social parasites sneak into and live within a host colony exploiting its resources. Recognition of nestmates and discrimination from non-nestmates is based on mixtures of low-volatile components present on each individuals’ exoskeleton (cuticular hydrocarbons: CHCs). CHC profiles are species-specific and CHC profiles of individuals from neighboring conspecific colonies usually only differ in the quantitative ratios of CHCs. The individuals’ CHC profiles are further influenced by environmental factors and a frequent exchange of CHCs between nestmates results in a uniformation of CHC profiles of nestmates. However, inter-individual, task-specific differences in CHC profiles remain. The neuronal basis of nestmate recognition is unknown, but it is generally assumed that the nestmate recognition process is based on a process of label-template matching where the CHC profile of an encountered ant (label) is compared with a neural representation of the own colony odor (template). When label and template match, the encounter ant is recognized as nestmate and when they mismatch, the encounter ant is recognized as non-nestmate. An encounter of non-nestmates often results in aggression. Importantly, since the CHC profiles change over time due to environmental influences, the template needs to be up- dated. In this thesis, I investigated different levels of nestmate recognition in ants. Specifically, I focused on which CHCs are produced, how CHC profiles are perceived, how the behavioral response is influenced by experience, and how CHC profiles are encoded and decoded in the brain.<br />In chapter 1, I investigate a host-social parasite system, where a social parasitic ant (Megalomyrmex symmetochus) parasitizes a colony of a fungus-growing ant (Sericomyrmex amabilis). I show that the CHC profiles of the two species are distinct and the parasite shares only a single hydrocarbon with its host. Furthermore, the parasite has fewer CHCs and in an overall lower quantity than its host, suggesting that the parasite uses a ’chemical insignificant’ strategy. My behavioral experiments provide evidence that colonies both with and without parasites discriminate between nestmates and conspecific non-nestmates and that parasites are not ‘chemically hidden’ but are in fact detected and attacked by host ants that are not familiar with parasites. Furthermore, I find that volatile chemicals emitted by the parasites likely induce submission responses in host ants. The results show that parasites do not need to match the label of their host, but use volatile chemicals in order to manipulate members of the host colony.<br />In chapter 2, I investigate in carpenter ants (Camponotus floridanus) how specific manipulations of CHC profiles of individuals originating from the same source colony influence their nestmate recognition. I provide evidence that ants can adjust to novel CHC profiles, while the previous CHC profiles are still accepted as nestmate. Furthermore, I find that not only an addition but also a lack of a hydrocarbon can lead to a discrimination as non-nestmate and I provide the first evidence that ants can form novel templates for nestmates.<br />In chapter 3, I investigate the influence of recent presence of nestmates (social context) on the propensity of aggression response towards non-nestmates in the territorial red wood ant, Formica rufa. When kept in a group of nestmates, workers showed a high probability of aggression against non-nestmates whereas the lack of social context reduces the workers’ probability of aggression against non-nestmates. Thus, social context is necessary to maintain or induce a physiological state in workers that allows aggression response against non-nestmates. Furthermore, my results suggest that the nestmate recognition system can be utilized at remote sites for an adaptive and flexible tuning of the response against competitors.<br />For chapter 4, I collected data on the encoding of colony odors in the first olfactory neuropil in the brain of ants (C. floridanus) using functional imaging at high-speed and standard frame recording of calcium signals, and I developed a method for simultaneously monitoring the behavioral response of a mounted ant while measuring calcium signals. The data set of this investigation is not complete and therefore this part has to be considered as pilot study for future experiments.<br />The four studies, compiled in my thesis revealed novel insights to several aspects of nestmate recognition in ants: Nestmate recognition depends on previous experience of individuals, and ants can store multiple templates for different nestmate labels and can discriminate them from similar non-nestmate labels. Furthermore, the behavioral response towards conspecific non-nestmates depends on recent social contact with nestmates. My data also shed light into host-parasite relationships and broadens our understanding on how parasites circumvent the nestmate recognition system of their host. Additionally, I provide a new, testable hypothesis on how nestmate recognition is implemented in the ant brain. 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