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

ABSTRACT: 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.

SUBMITTER: Blacher P

PROVIDER: S-EPMC3878879 | biostudies-other | 2013

REPOSITORIES: biostudies-other

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

Blacher Pierre P Boreggio Laurie L Leroy Chloé C Devienne Paul P Châline Nicolas N Chameron Stéphane S

Frontiers in zoology 20131210 1

<h4>Background</h4>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 ...[more]

PMID: 24321042

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Project description:Co-evolution is a major driving force shaping the outcome of host-parasite interactions over time. After host shifts, the lack of co-evolution can have a drastic impact on novel host populations. Nevertheless, it is known that Western honey bee (Apismellifera) populations can cope with host-shifted ectoparasitic mites (Varroa destructor) by means of natural selection. However, adaptive phenotypic traits of the parasites and temporal variations in host resistance behavior are poorly understood. Here, we show that mites made adaptive shifts in reproductive strategy when associated with resistant hosts and that host resistance traits can change over time. In a fully-crossed field experiment, worker brood cells of local adapted and non-adapted (control) A.mellifera host colonies were infested with mites originating from both types of host colonies. Then, mite reproduction as well as recapping of cells and removal of infested brood (i.e., Varroa Sensitive Hygiene, VSH) by host workers were investigated and compared to data from the same groups of host colonies three years earlier. The data suggest adaptive shifts in mite reproductive strategies, because mites from adapted hosts have higher probabilities of reproduction, but lower fecundity, when infesting their associated hosts than mites in treated colonies. The results confirm that adapted hosts can reduce mite reproductive success. However, neither recapping of cells nor VSH were significantly expressed, even though the latter was significantly expressed in this adapted population three years earlier. This suggests temporal variation in the expression of adaptive host traits. It also appears as if mechanisms not investigated here were responsible for the reduced mite reproduction in the adapted hosts. In conclusion, a holistic view including mite adaptations and studies of the same parasite/host populations over time appears overdue to finally understand the mechanisms enabling survival of V.destructor-infested honey bee host colonies.

Dataset Information

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

Publications

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

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