Fertility Signaling and Partitioning of Reproduction in the Ant Neoponera apicalis.

All individuals in social insect colonies benefit from being informed about the presence and fertility state of reproducers. This allows the established reproductive individuals to maintain their reproductive monopoly without the need for physical control, and the non-reproductive individuals to make appropriate reproductive choices. Here, we studied whether fertility signaling is responsible for the partitioning of reproduction in the ant Neoponera apicalis. This species forms small colonies from one single-mated queen, with workers establishing reproductive hierarchies when hopelessly queenless. Previous studies identified putative fertility signals, particularly the hydrocarbon 13-methylpentacosane (13-MeC25), and have shown that precise status discrimination based on these signals could be involved in the regulation of reproductive activities. Here, we extend these findings and reveal that all individuals, be they queens or workers, differ in their cuticular hydrocarbon profile according to fertility state. Proportions of 13-MeC25 were a strong predictor of an individual's ovarian activity, and could, thus, advertise the established reproducer(s) in both queenright and queenless conditions. Furthermore, this compound might play a key role in the establishment of the reproductive hierarchy, since workers with low fertility at the onset of hierarchy formation already have relatively high amounts of 13-MeC25. Dyadic encounters showed that individuals with experimentally increased amounts of 13-MeC25 triggered less agonistic interactions from top rankers, in accord with them "advertising" higher status. Thus, these bioassays supported the use of 13-MeC25 by competing ants. This simple recognition system potentially allows permanent regulation of partitioning of reproduction in this species.

Specific recognition of reproductive parasite workers by nest-entrance guards in the bumble bee Bombus terrestris.

BACKGROUND: The impact of social parasites on their hosts' fitness is a strong selective pressure that can lead to the evolution of adapted defence strategies. Guarding the nest to prevent the intrusion of parasites is a widespread response of host species. If absolute rejection of strangers provides the best protection against parasites, more fine-tuned strategies can prove more adaptive. Guarding is indeed costly and not all strangers constitute a real threat. That is particularly true for worker reproductive parasitism in social insects since only a fraction of non-nestmate visitors, the fertile ones, can readily engage in parasitic reproduction. Guards should thus be more restrictive towards fertile than sterile non-nestmate workers. We here tested this hypothesis by examining the reaction of nest-entrance guards towards nestmate and non-nestmate workers with varying fertility levels in the bumble bee Bombus terrestris. Because social recognition in social insects mainly relies on cuticular lipids (CLs), chemical analysis was also conducted to examine whether workers' CLs could convey the relevant information upon which guards could base their decision. We thus aimed to determine whether an adapted defensive strategy to worker reproductive parasitism has evolved in B. terrestris colonies. RESULTS: Chemical analysis revealed that the cuticular chemical profiles of workers encode information about both their colony membership and their current fertility, therefore providing potential recognition cues for a suitable adjustment of the guards' defensive decisions. We found that guards were similarly tolerant towards sterile non-nestmate workers than towards nestmate workers. However, as predicted, guards responded more aggressively towards fertile non-nestmates. CONCLUSION: Our results show that B. terrestris guards discriminate non-nestmates that differ in their reproductive potential and respond more strongly to the individuals that are a greatest threat for the colony. Cuticular hydrocarbons are the probable cues underlying the specific recognition of reproductive parasites, with the specific profile of highly fertile bees eliciting the agonistic response when combined with non-colony membership information. Our study therefore provides a first piece of empirical evidence supporting the hypothesis that an adapted defensive strategy against worker reproductive parasitism exists in B. terrestris colonies.

Drifting behaviour as an alternative reproductive strategy for social insect workers.

Restricted reproduction is traditionally posited as the defining feature of eusocial insect workers. The discovery of worker reproduction in foreign colonies challenges this view and suggests that workers' potential to pursue selfish interests may be higher than previously believed. However, whether such reproductive behaviour truly relies on a reproductive decision is still unknown. Workers' reproductive decisions thus need to be investigated to assess the extent of workers' reproductive options. Here, we show in the bumblebee Bombus terrestris that drifting is a distinct strategy by which fertile workers circumvent competition in their nest and reproduce in foreign colonies. By monitoring workers' movements between colonies, we show that drifting is a remarkably dynamic behaviour, widely expressed by both fertile and infertile workers. We demonstrate that a high fertility is, however, central in determining the propensity of workers to enter foreign colonies as well as their subsequent reproduction in host colonies. Moreover, our study shows that the drifting of fertile workers reflects complex decision-making processes associated with in-nest reproductive competition. This novel finding therefore adds to our modern conception of cooperation by showing the previously overlooked importance of alternative strategies which enable workers to assert their reproductive interests.

Social context and reproductive potential affect worker reproductive decisions in a eusocial insect.

Context-dependent decision-making conditions individual plasticity and is an integrant part of alternative reproductive strategies. In eusocial Hymenoptera (ants, bees and wasps), the discovery of worker reproductive parasitism recently challenged the view of workers as a homogeneous collective entity and stressed the need to consider them as autonomous units capable of elaborate choices which influence their fitness returns. The reproductive decisions of individual workers thus need to be investigated and taken into account to understand the regulation of reproduction in insect societies. However, we know virtually nothing about the proximate mechanisms at the basis of worker reproductive decisions. Here, we test the hypothesis that the capacity of workers to reproduce in foreign colonies lies in their ability to react differently according to the colonial context and whether this reaction is influenced by a particular internal state. Using the bumble bee Bombus terrestris, we show that workers exhibit an extremely high reproductive plasticity which is conditioned by the social context they experience. Fertile workers reintroduced into their mother colony reverted to sterility, as expected. On the contrary, a high level of ovary activity persisted in fertile workers introduced into a foreign nest, and this despite more frequent direct contacts with the queen and the brood than control workers. Foreign workers' reproductive decisions were not affected by the resident queen, their level of fertility being similar whether or not the queen was removed from the host colony. Workers' physiological state at the time of introduction is also of crucial importance, since infertile workers failed to develop a reproductive phenotype in a foreign nest. Therefore, both internal and environmental factors appear to condition individual reproductive strategies in this species, suggesting that more complex decision-making mechanisms are involved in the regulation of worker reproduction than previously thought.

Do host species evolve a specific response to slave-making ants?

BACKGROUND: Social parasitism is an important selective pressure for social insect species. It is particularly the case for the hosts of dulotic (so called slave-making) ants, which pillage the brood of host colonies to increase the worker force of their own colony. Such raids can have an important impact on the fitness of the host nest. An arms race which can lead to geographic variation in host defenses is thus expected between hosts and parasites. In this study we tested whether the presence of a social parasite (the dulotic ant Myrmoxenus ravouxi) within an ant community correlated with a specific behavioral defense strategy of local host or non-host populations of Temnothorax ants. Social recognition often leads to more or less pronounced agonistic interactions between non-nestmates ants. Here, we monitored agonistic behaviors to assess whether ants discriminate social parasites from other ants. It is now well-known that ants essentially rely on cuticular hydrocarbons to discriminate nestmates from aliens. If host species have evolved a specific recognition mechanism for their parasite, we hypothesize that the differences in behavioral responses would not be fully explained simply by quantitative dissimilarity in cuticular hydrocarbon profiles, but should also involve a qualitative response due to the detection of particular compounds. We scaled the behavioral results according to the quantitative chemical distance between host and parasite colonies to test this hypothesis. RESULTS: Cuticular hydrocarbon profiles were distinct between species, but host species did not show a clearly higher aggression rate towards the parasite than toward non-parasite intruders, unless the degree of response was scaled by the chemical distance between intruders and recipient colonies. By doing so, we show that workers of the host and of a non-host species in the parasitized site displayed more agonistic behaviors (bites and ejections) towards parasite than toward non-parasite intruders. CONCLUSIONS: We used two different analyses of our behavioral data (standardized with the chemical distance between colonies or not) to test our hypothesis. Standardized data show behavioral differences which could indicate qualitative and specific parasite recognition. We finally stress the importance of considering the whole set of potentially interacting species to understand the coevolution between social parasites and their hosts.