Nestmate recognition in social insects: overcoming physiological constraints with collective decision making

Abstract

Social insects rank among the most abundant and influential terrestrial organisms. The key to their success is their ability to form tightly knit social groups that perform work cooperatively, and effectively exclude non-members from the colony. An extensive body of research, both empirical and theoretical, has explored how optimal acceptance thresholds could evolve in individuals, driven by the twin costs of inappropriately rejecting true nestmates and erroneously accepting individuals from foreign colonies. Here, in contrast, we use agent-based modeling to show that strong nestmate recognition by individuals is often unnecessary. Instead, highly effective nestmate recognition can arise as a colony-level property from a collective of individually poor recognizers. Essentially, although an intruder can get by one defender when their odor cues are similar, it is nearly impossible to get past many defenders if there is the slightest difference in cues. The results of our models match observed rejection rates in studies of ants, wasps, and bees. We also show that previous research in support of the optimal threshold theory approach to the problem of nestmate recognition can be alternatively viewed as evidence in favor of the collective formation of a selectively permeable barrier that allows in nestmates (at a significant cost) while rejecting non-nestmates. Finally, this work shows that nestmate recognition has a stronger task allocation component than previously thought, as colonies can nearly always achieve perfect nestmate recognition if it is cost effective for them to do so at the colony level. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-010-1094-x) contains supplementary material, which is available to authorized users.

Fig. 1

Conceptual model for the trade-off between the prevalence of true and false rejections based on the limited olfactory acuity of individual workers. Any perceived worker with a template cue dissimilarity value to the right of the acceptance threshed is rejected, while those to the left are accepted. Imperfect discrimination ability on the part of the worker is proposed to generate an error window (within which odor differences cannot be distinguished). Depending on the width of this window, and the placement of the acceptance threshold, this window can generate a trade-off between acceptance and rejection errors. In order to account for studies showing no false rejections, the acceptance level must be set far to the right of the nestmate distribution, necessitating a large number of false acceptances of non-nestmates

Fig. 2

Ultimate acceptance probability for non-nestmates having encountered variable numbers of nestmates with a fixed probability of rejection per encounter. The acceptance probability for a given number of encounters is simply the per-encounter rejection rate raised to the number of interactions. For low probabilities of acceptance per encounter, the overall acceptance rate quickly falls to nearly zero, while a much slower rate of decay is exhibited by higher per-encounter probabilities

Fig. 3

Results of an agent-based model simulating the time to rejection for invading non-nestmates in a colony without explicit guards. Density of workers within the nest strongly determines encounter rate, which in turn underlies the ultimate probability of rejection. Simulated workers have a 10% probability (mean with individual variation amongst workers) of rejecting non-nestmates per encounter

Fig. 4

Ultimate acceptance rate for varying numbers of interactions with a fixed probability of rejection per encounter. Even the slightest probabilities of rejecting nestmates (0.5%) leads to rejection after 100–200 encounters. Thus, in large colonies, even slight probabilities of rejection would lead to continual fighting. A precondition of sociality may therefore be setting the acceptance threshold such that nestmate rejection does not occur

Fig. 5

Probability of ultimate acceptance and time to entry for 10 nestmates and 5 non-nestmates attempting to enter a honey bee nest with guards. When non-nestmate and nestmate per-encounter rejection rates are strongly dissimilar (80% and 20% in present case), it is possible for a colony to ensure next to no admittance of non-nestmates by regulating the number of guards at the entrance. This comes at a price, however, as increasing numbers of guards increase the time to admittance for nestmates

Fig. 6

Simulation of colony defense during a period of robbing. A feedback mechanism, based on the recruitment of guards via alarm pheromone, is shown to be capable of collectively regulating nestmate recognition. Simulations start with two guards; 20 invaders and 60 nestmates arrive per minute. At hour 2, the invader arrival rate is increased to 80 per minute for 2 h. Mean per minute acceptance rates are shown. The acceptance rate for invaders is relatively high for a few minutes before additional guards have been recruited, at which time it falls drastically. When the invader arrival rate is increased, acceptance rate increases briefly before returning to below 1 per minute

Fig. 7

Mean (±sd) numbers of guards, foragers, and invaders at the entrance over time for the same simulations shown in Fig. 6. The number of guards quickly rises, before reaching a stable level. When the number of invaders increases, the number of guards rises weakly. However, the number of foragers waiting to get into the nest strongly rises when the number of guards is increased