Periodic Reporting for period 4 - EPIDEMIC (Experimental Epidemiology in Ant Societies)
Periodo di rendicontazione: 2024-08-01 al 2026-01-31
Many infectious diseases spread through social contact. The way individuals organise themselves in groups can strongly influence how quickly infections spread and who gets infected. However, in most animal and human societies, it is extremely difficult to determine whether differences in infection risk are caused by behaviour itself, or by other factors such as age, genetics, or prior exposure to pathogens. This limits our ability to predict disease outbreaks and to understand how social systems evolve to cope with infection risk.
The ERC project EPIDEMIC addressed this challenge by developing an experimental approach to epidemiology in social insect societies. The project used the clonal raider ant (Ooceraea biroi), a species in which replicate colonies of precisely determined size, genetic, and demographic composition can easily be created. This unique feature makes it possible to isolate the effects of various factors (behaviour, genetics, age) from each other. The overall objectives of EPIDEMIC were 1) to measure how individual behaviour is linked to infection risk and immune function. 2) to create experimental social networks with predictable differences in transmission risk. 3) To experimentally test how infections spread through controlled social networks.
Over the course of the project, EPIDEMIC demonstrated that behavioural organisation alone is sufficient to generate systematic differences in infection risk. Even in colonies composed of genetically identical individuals, workers that performed tasks outside the nest were more likely to become infected than those that remained inside.Contrary to a long-standing hypothesis, the project found no evidence that individuals facing higher infection risk invest more in baseline immune defences. This refines our understanding of how immunity is organised in social systems. Based on adapted experimental approaches we successfully tested key predictions about how social structure influences disease spread.
In conclusion, EPIDEMIC established a new experimental framework for studying disease transmission in social groups. By providing causal evidence that behavioural organisation shapes infection risk, the project advances our understanding of how social systems influence the dynamics of infectious disease, knowledge that is relevant not only for understanding animal societies but also for improving predictive approaches in epidemiology more broadly.
The ERC project EPIDEMIC addressed this challenge by developing an experimental approach to epidemiology in social insect societies. The project used the clonal raider ant (Ooceraea biroi), a species in which replicate colonies of precisely determined size, genetic, and demographic composition can easily be created. This unique feature makes it possible to isolate the effects of various factors (behaviour, genetics, age) from each other. The overall objectives of EPIDEMIC were 1) to measure how individual behaviour is linked to infection risk and immune function. 2) to create experimental social networks with predictable differences in transmission risk. 3) To experimentally test how infections spread through controlled social networks.
Over the course of the project, EPIDEMIC demonstrated that behavioural organisation alone is sufficient to generate systematic differences in infection risk. Even in colonies composed of genetically identical individuals, workers that performed tasks outside the nest were more likely to become infected than those that remained inside.Contrary to a long-standing hypothesis, the project found no evidence that individuals facing higher infection risk invest more in baseline immune defences. This refines our understanding of how immunity is organised in social systems. Based on adapted experimental approaches we successfully tested key predictions about how social structure influences disease spread.
In conclusion, EPIDEMIC established a new experimental framework for studying disease transmission in social groups. By providing causal evidence that behavioural organisation shapes infection risk, the project advances our understanding of how social systems influence the dynamics of infectious disease, knowledge that is relevant not only for understanding animal societies but also for improving predictive approaches in epidemiology more broadly.
We experimentally manipulated two key aspects of colony composition, genetic structure and age structure, to generate replicate social networks predicted to differ in transmission risk. These experiments demonstrated that workers of different genotypes exhibit consistent behavioural differences that translate into measurable variation in network topology. Similarly, colonies composed of workers of different ages showed systematic differences in spatial organization and interaction patterns. In parallel, a peer-reviewed study (Jud et al., Proc. R. Soc. B) showed that colony genotype composition can shape behavioural dynamics and colony-level cycles, providing complementary evidence that collective organisation is predictable and experimentally tractable in O. biroi. To complement the empirical work, a computational pipeline was developed to simulate disease spread on temporal networks derived from automated behavioural tracking data.
To test whether individuals facing higher infection risk invest more in constitutive immune defences, we used O. biroi to decouple behavioural role from genotype and age. As a foundation, we annotated the immune gene repertoire of O. biroi from the genome by homology, identifying 256 candidate immune-related genes. We then combined fine-scale automated behavioural tracking with three complementary measures of baseline immune investment: immune-related gene expression quantified by transcriptomics, antibacterial activity measured in lysates, and survival following experimental pathogen exposure. Contrary to a long-standing hypothesis, we found no evidence that individuals engaging more strongly in high-exposure (forager-like) behaviours show higher constitutive immune investment; instead, baseline immune measures were largely uniform across behavioural phenotypes (see Li et al., 2025).
We also investigated how immune activation alters social organisation and the distribution of immune function within colonies. The core component of this work demonstrated that experimentally immune-challenged individuals occupy a more central position in the colony’s interaction network, rather than being avoided (Alciatore et al., 2021). This finding provided experimental evidence that immune status reshapes social networks in ways that are directly relevant for disease transmission.
Beyond this original objective, additional experiments testing immune priming revealed that prior exposure to live bacterial pathogens can enhance survival upon secondary exposure in O. biroi, and that this protection can be transmitted to nestmates. Additional experiments examined how bacterial infections affect social behaviour towards adults and larvae. To test predictions from network epidemiology by monitoring parasite transmission across experimental contact networks we established Diploscapter nematodes as a natural parasite system of ants and developed protocols for experimental infection.
Experiments combining behavioural tracking, infection assays, transcriptomics, and chemical analyses demonstrated that 1) Diploscapter parasitizes a specific gland in the ant head and affects host survival and physiology; 2) Differences in infection risk arise from behavioural variation alone: foragers become infected earlier and carry higher parasite loads than genetically identical nurses, and 3) Infection feeds back on social organization by reducing activity and increasing spatial overlap among colony members.
These results provide direct causal evidence that behavioural organization structures infection risk and that infection in turn reshapes social networks. The establishment of Diploscapter as an experimentally tractable parasite system represents a significant methodological advance for the study of transmission in ant societies.
The results of EPIDEMIC have been disseminated through several open-access, peer-reviewed publications and conference presentations, and further manuscripts are under preparation. Several events such as the Long Night of the Sciences were used to disseminate the findings to a lay public. The automated tracking infrastructure, new infection protocols developed during the project, and computational pipelines now form a durable experimental platform for future studies of epidemiology and other forms of biological transmission.
To test whether individuals facing higher infection risk invest more in constitutive immune defences, we used O. biroi to decouple behavioural role from genotype and age. As a foundation, we annotated the immune gene repertoire of O. biroi from the genome by homology, identifying 256 candidate immune-related genes. We then combined fine-scale automated behavioural tracking with three complementary measures of baseline immune investment: immune-related gene expression quantified by transcriptomics, antibacterial activity measured in lysates, and survival following experimental pathogen exposure. Contrary to a long-standing hypothesis, we found no evidence that individuals engaging more strongly in high-exposure (forager-like) behaviours show higher constitutive immune investment; instead, baseline immune measures were largely uniform across behavioural phenotypes (see Li et al., 2025).
We also investigated how immune activation alters social organisation and the distribution of immune function within colonies. The core component of this work demonstrated that experimentally immune-challenged individuals occupy a more central position in the colony’s interaction network, rather than being avoided (Alciatore et al., 2021). This finding provided experimental evidence that immune status reshapes social networks in ways that are directly relevant for disease transmission.
Beyond this original objective, additional experiments testing immune priming revealed that prior exposure to live bacterial pathogens can enhance survival upon secondary exposure in O. biroi, and that this protection can be transmitted to nestmates. Additional experiments examined how bacterial infections affect social behaviour towards adults and larvae. To test predictions from network epidemiology by monitoring parasite transmission across experimental contact networks we established Diploscapter nematodes as a natural parasite system of ants and developed protocols for experimental infection.
Experiments combining behavioural tracking, infection assays, transcriptomics, and chemical analyses demonstrated that 1) Diploscapter parasitizes a specific gland in the ant head and affects host survival and physiology; 2) Differences in infection risk arise from behavioural variation alone: foragers become infected earlier and carry higher parasite loads than genetically identical nurses, and 3) Infection feeds back on social organization by reducing activity and increasing spatial overlap among colony members.
These results provide direct causal evidence that behavioural organization structures infection risk and that infection in turn reshapes social networks. The establishment of Diploscapter as an experimentally tractable parasite system represents a significant methodological advance for the study of transmission in ant societies.
The results of EPIDEMIC have been disseminated through several open-access, peer-reviewed publications and conference presentations, and further manuscripts are under preparation. Several events such as the Long Night of the Sciences were used to disseminate the findings to a lay public. The automated tracking infrastructure, new infection protocols developed during the project, and computational pipelines now form a durable experimental platform for future studies of epidemiology and other forms of biological transmission.
At project start, empirical tests of network epidemiology were limited by three major constraints: lack of experimental control over social networks, lack of high-throughput behavioural monitoring, and lack of natural parasite systems with sustained transmission. EPIDEMIC addressed all three.
Conceptually, the project provides one of the first causal demonstrations that behavioural individuality alone generates structured infection risk in social groups, and it refines prevailing hypotheses regarding immune division of labour. The feedback between infection and social organization further advances the integration of behavioural ecology with epidemiological theory.
Conceptually, the project provides one of the first causal demonstrations that behavioural individuality alone generates structured infection risk in social groups, and it refines prevailing hypotheses regarding immune division of labour. The feedback between infection and social organization further advances the integration of behavioural ecology with epidemiological theory.