The trade-off between the transmission of chemical cues and parasites: behavioral interactions between leaf-cutting ant workers of different age classes

ABSTRACT Social animals are faced with an intriguing dilemma. On the one hand, interactions between individuals are essential to exchange information and to promote cohesion, while on the other hand such interactions carry with them the risk of catching and transmitting parasites. This trade-off is particularly significant for social insects because low within-colony genetic diversity makes their colonies potentially vulnerable to parasites while frequent interactions are essential to the development of the colonial odor profile necessary for nestmate recognition. Here we investigate whether social interactions between young and old leaf-cutting ant workers show evidence of this trade-off. We find that old workers engage in more selfgrooming and mandibular scraping than young workers, both in keeping with old workers having been more exposed to parasites. In contrast, we find that young workers engaged in more allogrooming than old workers, which seems likely to have a different motivation possibly the transfer of recognition cues. Furthermore, young workers tended to engage in allogrooming with other young workers, although it was the old workers that were most active and with whom allogrooming would seem likely to optimize information or chemicals transfer. This suggests that young workers may be attempting to minimize the risk of parasite transmission during their social interactions. Although limited to behavioral data, these results hint that ant workers may be sensitive to the trade-off between the transmission of recognition cues and disease, and adjust their social interactions accordingly.

Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease.

The worldwide spread of diseases is considered a major threat to biodiversity and a possible driver of the decline of pollinator populations, particularly when novel species or strains of parasites emerge. Previous studies have suggested that populations of introduced European honeybee (Apis mellifera) and bumblebee species (Bombus terrestris and Bombus ruderatus) in Argentina share the neogregarine parasite Apicystis bombi with the native bumblebee (Bombus dahlbomii). In this study we investigated whether A. bombi is acting as an emergent parasite in the non-native populations. Specifically, we asked whether A. bombi, recently identified in Argentina, was introduced by European, non-native bees. Using ITS1 and ITS2 to assess the parasite's intraspecific genetic variation in bees from Argentina and Europe, we found a largely unstructured parasite population, with only 15% of the genetic variation being explained by geographic location. The most abundant haplotype in Argentina (found in all 9 specimens of non-native species) was identical to the most abundant haplotype in Europe (found in 6 out of 8 specimens). Similarly, there was no evidence of structuring by host species, with this factor explaining only 17% of the genetic variation. Interestingly, parasites in native Bombus ephippiatus from Mexico were genetically distant from the Argentine and European samples, suggesting that sufficient variability does exist in the ITS region to identify continent-level genetic structure in the parasite. Thus, the data suggest that A. bombi from Argentina and Europe share a common, relatively recent origin. Although our data did not provide information on the direction of transfer, the absence of genetic structure across space and host species suggests that A. bombi may be acting as an emergent infectious disease across bee taxa and continents.

Kin-informative recognition cues in ants.

Although social groups are characterized by cooperation, they are also often the scene of conflict. In non-clonal systems, the reproductive interests of group members will differ and individuals may benefit by exploiting the cooperative efforts of other group members. However, such selfish behaviour is thought to be rare in one of the classic examples of cooperation--social insect colonies--because the colony-level costs of individual selfishness select against cues that would allow workers to recognize their closest relatives. In accord with this, previous studies of wasps and ants have found little or no kin information in recognition cues. Here, we test the hypothesis that social insects do not have kin-informative recognition cues by investigating the recognition cues and relatedness of workers from four colonies of the ant Acromyrmex octospinosus. Contrary to the theoretical prediction, we show that the cuticular hydrocarbons of ant workers in all four colonies are informative enough to allow full-sisters to be distinguished from half-sisters with a high accuracy. These results contradict the hypothesis of non-heritable recognition cues and suggest that there is more potential for within-colony conflicts in genetically diverse societies than previously thought.

Adaptive social immunity in leaf-cutting ants.

Social insects have evolved a suite of sophisticated defences against parasites. In addition to the individual physiological immune response, social insects also express 'social immunity' consisting of group-level defences and behaviours that include allogrooming. Here we investigate whether the social immune response of the leaf-cutting ant Acromyrmex echinatior reacts adaptively to the virulent fungal parasite, Metarhizium anisopliae. We 'immunized' mini-nests of the ants by exposing them twice to the parasite and then compared their social immune response with that of naive mini-nests that had not been experimentally exposed to the parasite. Ants allogroomed individuals exposed to the parasite, doing this both for those freshly treated with the parasite, which were infectious but not yet infected, and for those treated 2 days previously, which were already infected but no longer infectious. We found that ants exposed to the parasite received more allogrooming in immunized mini-nests than in naive mini-nests. This increased the survival of the freshly treated ants, but not those that were already infected. The results thus indicate that the social immune response of this leaf-cutting ant is adaptive, with the group exhibiting a greater and more effective response to a parasite that it has previously been exposed to.

Genetic polymorphism in leaf-cutting ants is phenotypically plastic.

Advanced societies owe their success to an efficient division of labour that, in some social insects, is based on specialized worker phenotypes. The system of caste determination in such species is therefore critical. Here, we examine in a leaf-cutting ant (Acromyrmex echinatior) how a recently discovered genetic influence on caste determination interacts with the social environment. By removing most of one phenotype (large workers; LW) from test colonies, we increased the stimulus for larvae to develop into this caste, while for control colonies we removed a representative sample of all workers so that the stimulus was unchanged. We established the relative tendencies of genotypes to develop into LW by genotyping workers before and after the manipulation. In the control colonies, genotypes were similarly represented in the large worker caste before and after worker removal. In the test colonies, however, this relationship was significantly weaker, demonstrating that the change in environmental stimuli had altered the caste propensity of at least some genotypes. The results indicate that the genetic influence on worker caste determination acts via genotypes differing in their response thresholds to environmental cues and can be conceptualized as a set of overlapping reaction norms. A plastic genetic influence on division of labour has thus evolved convergently in two distantly related polyandrous taxa, the leaf-cutting ants and the honeybees, suggesting that it may be a common, potentially adaptive, property of complex, genetically diverse societies.

Genetic diversity and disease resistance in leaf-cutting ant societies.

Multiple mating by females (polyandry) remains hard to explain because, while it has substantial costs, clear benefits have remained elusive. The problem is acute in the social insects because polyandry is probably particularly costly for females and most material benefits of the behavior are unlikely to apply. It has been suggested that a fitness benefit may arise from the more genetically diverse worker force that a polyandrous queen will produce. One leading hypothesis is that the increased genetic diversity of workers will improve a colony's resistance to disease. We investigated this hypothesis using a polyandrous leaf-cutting ant and a virulent fungal parasite as our model system. At high doses of the parasite most patrilines within colonies were similarly susceptible, but a few showed greater resistance. At a low dose of the parasite there was more variation between patrilines in their resistance to the parasite. Such genetic variation is a key prerequisite for polyandry to result in increased disease resistance of colonies. The relatedness of two hosts did not appear to affect the transmission of the parasite between them, but this was most likely because the parasite tested was a virulent generalist that is adapted to transmit between distantly related hosts. The resistance to the parasite was compared between small groups of ants of either high or low genetic diversity. No difference was found at high doses of the parasite, but a significant improvement in resistance in high genetic diversity groups was found at a low dose of the parasite. That there is genetic variation for disease resistance means that there is the potential for polyandry to produce more disease-resistant colonies. That this genetic variation can improve the resistance of groups even under the limited conditions tested suggests that polyandry may indeed produce colonies with improved resistance to disease.

Ant parasite queens revert to mating singly.

Multiple mating (polyandry) is widespread among animal groups, particularly insects. But the factors that maintain it and underlie its evolution are hard to verify because benefits and costs are not easily quantified and they tend to be similar in related species. Here we compare the mating strategies of the leaf-cutting ant Acromyrmex echinatior and its recently derived social parasite Acromyrmex insinuator, which is also its closest relative. We find that although the host queens mate with up to a dozen different males, the social parasite mates only singly. This rapid and surprising reversion to single mating in a socially parasitic ant indicates that the costs of polyandry are probably specific to a free-living lifestyle.