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Social Structure and Genetic Distance Mediate Nestmate Recognition and Aggressiveness in the Facultative Polygynous Ant Pheidole pallidula.

ABSTRACT: In social insects, the evolutionary stability of cooperation depends on the privileged relationships between individuals of the social group, which is facilitated by the recognition of relatives. Nestmate recognition is based on genetically determined cues and/or environmentally derived chemical components present on the cuticle of individuals. Here, we studied nestmate recognition in the ant Pheidole pallidula, a species where both single-queen (monogyne) and multiple-queen (polygyne) colonies co-occur in the same population. We combined geographical, genetic and chemical analyses to disentangle the factors influencing the level of intraspecific aggressiveness. We show that encounters between workers from neighbouring colonies (i.e., nests less than 5 m away) are on average less aggressive than those between workers from more distant colonies. Aggressive behaviour is associated with the level of genetic difference: workers from monogyne colonies are more aggressive than workers from polygyne colonies, and the intensity of aggressiveness is positively associated with the genetic distance between colonies. Since the genetic distance is correlated with the spatial distance between pairs of colonies, the lower level of aggression toward neighbours may result from their higher relatedness. In contrast, the analysis of overall cuticular hydrocarbon profiles shows that aggressive behaviour is associated neither with the chemical diversity of colonies, nor with the chemical distances between them. When considering methyl-branched alkanes only, however, chemical distances differed between monogyne and polygyne colonies and were significantly associated with aggressiveness. Altogether, these results show that the social structure of colonies and the genetic distances between colonies are two major factors influencing the intensity of agonistic behaviours in the ant P. pallidula.

SUBMITTER: Fournier D

PROVIDER: S-EPMC4886963 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Project description:The importance of early experience in animals' life is unquestionable, and imprinting-like phenomena may shape important aspects of behaviour. Early learning typically occurs during a sensitive period, which restricts crucial processes of information storage to a specific developmental phase. The characteristics of the sensitive period have been largely investigated in vertebrates, because of their complexity and plasticity, both in behaviour and neurophysiology, but early learning occurs also in invertebrates. In social insects, early learning appears to influence important social behaviours such as nestmate recognition. Yet, the mechanisms underlying recognition systems are not fully understood. It is currently believed that Polistes social wasps are able to discriminate nestmates from non-nestmates following the perception of olfactory cues present on the paper of their nest, which are learned during a strict sensitive period, immediately after emergence. Here, through differential odour experience experiments, we show that workers of Polistes dominula develop correct nestmate recognition abilities soon after emergence even in absence of what have been so far considered the necessary cues (the chemicals spread on nest paper). P. dominula workers were exposed for the first four days of adult life to paper fragments from their nest, or from a foreign conspecific nest or to a neutral condition. Wasps were then transferred to their original nests where recognition abilities were tested. Our results show that wasps do not alter their recognition ability if exposed only to nest material, or in absence of nest material, during the early phase of adult life. It thus appears that the nest paper is not used as a source of recognition cues to be learned in a specific time window, although we discuss possible alternative explanations. Our study provides a novel perspective for the study of the ontogeny of nestmate recognition in Polistes wasps and in other social insects.

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Social Structure and Genetic Distance Mediate Nestmate Recognition and Aggressiveness in the Facultative Polygynous Ant Pheidole pallidula.

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