Recognition in a social symbiosis: chemical phenotypes and nestmate recognition behaviors of neotropical parabiotic ants.

Virginia J Emery,Neil D Tsutsui

doi:10.1371/journal.pone.0056492

Abstract

Social organisms rank among the most abundant and ecologically dominant species on Earth, in part due to exclusive recognition systems that allow cooperators to be distinguished from exploiters. Exploiters, such as social parasites, manipulate their hosts’ recognition systems, whereas cooperators are expected to minimize interference with their partner’s recognition abilities. Despite our wealth of knowledge about recognition in single-species social nests, less is known of the recognition systems in multi-species nests, particularly involving cooperators. One uncommon type of nesting symbiosis, called parabiosis, involves two species of ants sharing a nest and foraging trails in ostensible cooperation. Here, we investigated recognition cues (cuticular hydrocarbons) and recognition behaviors in the parabiotic mixed-species ant nests of Camponotus femoratus and Crematogaster levior in North-Eastern Amazonia. We found two sympatric, cryptic Cr. levior chemotypes in the population, with one type in each parabiotic colony. Although they share a nest, very few hydrocarbons were shared between Ca. femoratus and either Cr. levior chemotype. The Ca. femoratus hydrocarbons were also unusually long–chained branched alkenes and dienes, compounds not commonly found amongst ants. Despite minimal overlap in hydrocarbon profile, there was evidence of potential interspecific nestmate recognition –Cr. levior ants were more aggressive toward Ca. femoratus non-nestmates than Ca. femoratus nestmates. In contrast to the prediction that sharing a nest could weaken conspecific recognition, each parabiotic species also maintains its own aggressive recognition behaviors to exclude conspecific non-nestmates. This suggests that, despite cohabitation, parabiotic ants maintain their own species-specific colony odors and recognition mechanisms. It is possible that such social symbioses are enabled by the two species each using their own separate recognition cues, and that interspecific nestmate recognition may enable this multi-species cooperative nesting.

Highlights

Social organisms, ranging from microbes and insects to humans, dominate our planet
None of the nest cuticular hydrocarbon profiles appeared to be intermediate between Cr. levior Type A and Cr. levior Type B
The Cr. levior chemotypes overlapped in geographic distribution (Fig. 2), with one very distant nest (500 km away from main population, not shown in Fig. 2) sharing an almost identical cuticular hydrocarbons (CHCs) profile to Cr. levior Type B

Summary

Introduction

Social organisms, ranging from microbes and insects to humans, dominate our planet. The success of any society is contingent on the ability to recognize members and non-members, and to maintain an efficient recognition system in the face of exploiters who might manipulate it [1,2,3,4]. Optimal social recognition systems minimize both rejection errors (that falsely reject members) and acceptance errors (that falsely accept non-members) by increasing the reliability of signals used in the recognition system This can be done on the sender side, with more consistent relationships between cues and identity [5,6], or on the receiver side by honing sensory perception and decision rules used by receivers to evaluate cues and assign identity [7,8,9,10,11]. A common nest odor, (the ‘gestalt odor’), is maintained through frequent social interactions, such as allogrooming, during which odors are exchanged among the interacting individuals These interactions minimize recognition errors by homogenizing chemical cues across individuals [14,15,16,17]. Ant nestmate recognition systems are reliable because of the frequent mixing of recognition cues, and the constant updating of individual’s neural templates as colony odors shift [4]

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Results

Conclusion