Immune Defense in Leaf-Cutting Ants: A Cross-Fostering Approach (original) (raw)

Covariation between colony social structure and immune defences of workers in the ant Formica selysi

Insectes Sociaux, 2010

Several ant species vary in the number of queens per colony, yet the causes and consequences of this variation remain poorly understood. In previous experiments, we found that Formica selysi workers originating from multiple-queen (=polygyne) colonies had a lower resistance to a fungal pathogen than workers originating from single-queen (=monogyne) colonies. In contrast, group diversity improved disease resistance in experimental colonies. This discrepancy between field and experimental colonies suggested that variation in social structure in the field had antagonistic effects on worker resistance, possibly through a down-regulation of the immune system balancing the positive effect of genetic diversity. Here, we examined if workers originating from field colonies with alternative social structure differed in three major components of their immune system. We found that workers from polygyne colonies had a lower bacterial growth inhibitory activity than workers from monogyne colonies. In contrast, workers from the two types of colonies did not differ significantly in bacterial cell wall lytic activity and prophenoloxidase activity. Overall, the presence of multiple queens in a colony correlated with a slight reduction in one inducible component of the immune system of individual workers. This reduced level of immune defence might explain the lower resistance of workers originating from polygyne colonies despite the positive effect of genetic diversity. More generally, these results indicate that social changes at the group level can modulate individual immune defences.

Immune-priming in ant larvae: social immunity does not undermine individual immunity

Biology Letters, 2013

Social insects deploy numerous strategies against pathogens including behavioural, biochemical and immunological responses. While past research has revealed that adult social insects can generate immunity, few studies have focused on the immune function during an insect's early life stages. We hypothesized that larvae of the black carpenter ant Camponotus pennsylvanicus vaccinated with heat-killed Serratia marcescens should be less susceptible to a challenge with an active and otherwise lethal dose of the bacterium. We compared the in vivo benefits of prior vaccination of young larvae relative to naive and ringer injected controls. Regardless of colony of origin, survival parameters of vaccinated individuals following a challenge were significantly higher than those of the other two treatments. Results support the hypothesis that ant larvae exhibit immune-priming. Based on these results, we can infer that brood care by workers does not eliminate the need for individual-level imm...

Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus

Biology Letters, 2010

In social insects, group behaviour can increase disease resistance among nest-mates and generate social prophylaxis. Stomodeal trophallaxis, or mutual feeding through regurgitation, may boost colony-level immunocompetence. We provide evidence for increased trophallactic behaviour among immunized workers of the carpenter ant Camponotus pennsylvanicus , which, together with increased antimicrobial activity of the regurgitate droplet, help explain the improved survival of droplet recipient ants relative to controls following an immune challenge. We have identified a protein related to cathepsin D, a lysosomal protease, as a potential contributor to the antimicrobial activity. The combined behavioural and immunological responses to infection in these ants probably represent an effective mechanism underlying the social facilitation of disease resistance, which could potentially produce socially mediated colony-wide prophylaxis. The externalization and sharing of an individual's immun...

Foster carers influence brood pathogen resistance in ants

Proceedings. Biological sciences / The Royal Society, 2014

Social organisms face a high risk of epidemics, and respond to this threat by combining efficient individual and collective defences against pathogens. An intriguing and little studied feature of social animals is that individual pathogen resistance may depend not only on genetic or maternal factors, but also on the social environment during development. Here, we used a cross-fostering experiment to investigate whether the pathogen resistance of individual ant workers was shaped by their own colony of origin or by the colony of origin of their carers. The origin of care-giving workers significantly influenced the ability of newly eclosed cross-fostered Formica selysi workers to resist the fungal entomopathogen Beauveria bassiana. In particular, carers that were more resistant to the fungal entomopathogen reared more resistant workers. This effect occurred in the absence of post-infection social interactions, such as trophallaxis and allogrooming. The colony of origin of eggs signifi...

Inbreeding and caste-specific variation in immune defence in the ant Formica exsecta

Behavioral Ecology and Sociobiology, 2011

Social insects are a widespread and ecologically dominant group. Reproductive division of labour among the females in the colonies is a key trait for their success, but at the same time, it creates dense aggregations of relatives which may promote the spread of disease in the colonies. Hence, the appropriate regulation of immune defence is crucial for the well-being of a colony. Inbreeding may disturb this process through reduced resistance or by impairing the colony's ability to regulate the responses. We tested the effect of inbreeding and the within-colony differences in the encapsulation response between the two female castes of the ant Formica exsecta. New reproductive females (gynes) born in more inbred colonies, and being more inbred themselves, showed an elevated immune response whereas inbreeding had no effect on worker response. Furthermore, the immune response exhibited by gynes was lower than that of workers and was not dependent on their body size whereas the worker response increased with body size. The elevated response is likely to reflect genetic stress caused by inbreeding, which in turn may compromise colony founding and longevity. Indeed, eliciting a high immune response in itself might not be adaptive. Our results show that the regulation of the expression of immunity differs between female castes despite their similar genetic make-up.

Immune response affects ant trophallactic behaviour

2008

Sociality is associated with many benefits that have favoured its evolution in social insects. However, sociability also presents disadvantages like crowding of large numbers of individuals, which may favour the spread of infections within colonies. Adaptations allowing social insects to prevent and/or control pathogen infections range from behavioural responses to physiological ones including their immune systems. In a state of infection, social interactions with nestmates should be altered in a way which might prevent its spreading. We simulated a microbial infection in workers of the ant Camponotus fellah by the administration of peptidoglycan (PGN) and then quantified their immune response and social interactions. PGN injections as well as control injections of Ringer solution elicited similar production of antibacterial compounds, during 1-4 days after. However, injections of PGN reduced the ability of encapsulation of a nylon implant compared to Ringer controls. The immune challenged workers did not decrease the level of interactions with their nestmates. On the contrary, they devoted more time to trophallaxis. These results are discussed in relation to ant life history traits.

Immune priming and pathogen resistance in ant queens

Ecology and evolution, 2014

Growing empirical evidence indicates that invertebrates become more resistant to a pathogen following initial exposure to a nonlethal dose; yet the generality, mechanisms, and adaptive value of such immune priming are still under debate. Because life-history theory predicts that immune priming and large investment in immunity should be more frequent in long-lived species, we here tested for immune priming and pathogen resistance in ant queens, which have extraordinarily long life span. We exposed virgin and mated queens of Lasius niger and Formica selysi to a low dose of the entomopathogenic fungus Beauveria bassiana, before challenging them with a high dose of the same pathogen. We found evidence for immune priming in naturally mated queens of L. niger. In contrast, we found no sign of priming in virgin queens of L. niger, nor in virgin or experimentally mated queens of F. selysi, which indicates that immune priming in ant queens varies according to mating status and mating conditi...

Effects of the social environment on the survival and fungal resistance of ant brood

Behavioral Ecology and Sociobiology, 2012

The phenotype of social animals can be influenced by genetic, maternal and environmental effects, which include social interactions during development. In social insects, the social environment and genetic origin of brood can each influence a whole suite of traits, from individual size to caste differentiation. Here, we investigate to which degree the social environment during development affects the survival and fungal resistance of ant brood of known maternal origin. We manipulated one component of the social environment, the worker/brood ratio, of brood originating from single queens of Formica selysi. We monitored the survival of brood and measured the head size and ability to resist the entomopathogenic fungus Beauveria bassiana of the resulting callow workers. The worker/brood ratio and origin of eggs affected the survival and maturation time of the brood and the size of the resulting callow workers. The survival of the callow workers varied greatly according to their origin, both in controls and when challenged with B. bassiana. However, there was no interaction between the fungal challenge and either the worker/brood ratio or origin of eggs, suggesting that these factors did not affect parasite resistance in the conditions tested. Overall, the social conditions during brood rearing and the origin of eggs had a strong impact on brood traits that are important for fitness. We detected a surprisingly large amount of variation among queens in the survival of their brood reared in standard queenless conditions, which calls for further studies on genetic, maternal and social effects influencing brood development in the social insects.

ANTIMICROBIAL DEFENSE SHOWS AN ABRUPT EVOLUTIONARY TRANSITION IN THE FUNGUS-GROWING ANTS

Evolution, 2008

Understanding the relative evolutionary importance of parasites to different host taxa is problematic because the expression of disease and resistance are often confounded by factors such as host age and condition. The antibiotic-producing metapleural glands of ants are a potentially useful exception to this rule because they are a key first-line defense that are fixed in size in adults. Here we conduct a comparative analysis of the size of the gland reservoir across the fungus-growing ants (tribe Attini). Most attines have singly mated queens, but in two derived genera, the leaf-cutting ants, the queens are multiply mated, which is hypothesized to have evolved to improve colony-level disease resistance. We found that, relative to body size, the gland reservoirs of most attines are similar in size but that those of the leaf-cutting ants are significantly larger. In contrast, the size of the reservoir did not relate with the evolutionary transition from lower to higher attines and correlated at most only slightly with colony size. The results thus suggest that the relationship between leaf-cutting ants and their parasites is distinctly different from that for other attine ants, in accord with the hypothesis that multiple mating by queens evolved to improve colony-level disease resistance.