Ecology and Evolution of Communication in Social Insects

Leonhardt, Sara D.; Menzel, Florian; Nehring, Volker; Schmitt, Thomas

doi:10.1016/j.cell.2016.01.035

Cited by 312 publications

(303 citation statements)

References 85 publications

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“…Serving as intra-and interspecific recognition cues, it is likely that, similar to parabioses, insects adapt their CHC profiles to other biotic interactions, including predator-prey, parasitic or mutualistic relationships [17,61]. At the same time, ants need CHC profiles that can encode a multitude of information [4]. This may limit the evolution of very simple profiles or those dominated by n-alkanes, which are believed to convey little information [8].…”

Section: Resultsmentioning

confidence: 99%

How do cuticular hydrocarbons evolve? Physiological constraints and climatic and biotic selection pressures act on a complex functional trait

2017

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Cuticular hydrocarbons (CHCs) cover the cuticles of virtually all insects, serving as a waterproofing agent and as a communication signal. The causes for the high CHC variation between species, and the factors influencing CHC profiles, are scarcely understood. Here, we compare CHC profiles of ant species from seven biogeographic regions, searching for physiological constraints and for climatic and biotic selection pressures. Molecule length constrained CHC composition: long-chain profiles contained fewer linear alkanes, but more hydrocarbons with disruptive features in the molecule. This is probably owing to selection on the physiology to build a semi-fluid cuticular layer, which is necessary for waterproofing and communication. CHC composition also depended on the precipitation in the ants' habitats. Species from wet climates had more alkenes and fewer dimethyl alkanes than those from drier habitats, which can be explained by different waterproofing capacities of these compounds. By contrast, temperature did not affect CHC composition. Mutualistically associated (parabiotic) species possessed profiles highly distinct from non-associated species. Our study is, to our knowledge, the first to show systematic impacts of physiological, climatic and biotic factors on quantitative CHC composition across a global, multi-species dataset. We demonstrate how they jointly shape CHC profiles, and advance our understanding of the evolution of this complex functional trait in insects.

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Section: Resultsmentioning

confidence: 99%

How do cuticular hydrocarbons evolve? Physiological constraints and climatic and biotic selection pressures act on a complex functional trait

2017

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“…While species-specific compounds allow species recognition, colony-specific profiles are important for inbreeding avoidance [25]. Queens communicate their fertility through their CHC profile and/or glandular secretions [2]. Besides these functions, CHCs experience selection from social parasites [26,27], which are thought to be a major driver of recognition cue diversity [28,29].…”

Section: Introductionmentioning

confidence: 99%

“…Recognition cues are usually blended within a colony through trophallaxis and grooming, with the postpharyngeal gland serving as a reservoir, where CHCs obtained by grooming are mixed and re-distributed [5]. They are also affected by environmental factors such as nest material or food [6,7] and social parameters for instance queen signals, so that the colony odour is constantly updated [2].…”

Section: Introductionmentioning

confidence: 99%

“…Animals only benefit from altruistic behaviour when directed towards relatives [1]. In insects, especially in social ones, recognition and subsequent discrimination occurs through olfaction or contact chemoreception [2]. Besides their role as desiccation barriers, the low to non-volatile hydrocarbons on the insect's cuticle mediate chemical communication and form the basis for nest-mate, species, and sex recognition and fertility signalling [3].…”

Section: Introductionmentioning

confidence: 99%

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The influence of slavemaking lifestyle, caste and sex on chemical profiles in Temnothorax ants: insights into the evolution of cuticular hydrocarbons

Kleeberg¹,

Menzel²,

Foitzik³

2017

Proc. R. Soc. B.

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Chemical communication is central for the formation and maintenance of insect societies. Generally, social insects only allow nest-mates into their colony, which are recognized by their cuticular hydrocarbons (CHCs). Social parasites, which exploit insect societies, are selected to circumvent host recognition. Here, we studied whether chemical strategies to reduce recognition evolved convergently in slavemaking ants, and whether they extend to workers, queens and males alike. We studied CHCs of three social parasites and their related hosts to investigate whether the parasitic lifestyle selects for specific chemical traits that reduce host recognition. Slavemaker profiles were characterized by shorter-chained hydrocarbons and a shift from methyl-branched alkanes to n -alkanes, presumably to reduce recognition cue quantity. These shifts were consistent across independent origins of slavery and were found in isolated ants and those emerging in their mother colony. Lifestyle influenced profiles of workers most profoundly, with little effect on virgin queen profiles. We detected an across-species caste signal, with workers, for which nest-mate recognition is particularly important, carrying more and longer-chained hydrocarbons and males exhibiting a larger fraction of n -alkanes. This comprehensive study of CHCs across castes and species reveals how lifestyle-specific selection can result in convergent evolution of chemical phenotypes.

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“…Even though insects in particular rely predominantly on chemotactile sensing to detect harmful compounds (de Brito Sanchez et al, 2005;Falibene et al, 2015), recognize mates (Blomquist and Bagneres, 2010;Leonhardt et al, 2016;Wilson, 1971), differentiate between colony members and foreigners (Fletcher and Michener, 1987;Leonhardt et al, 2016;Wilson, 1971) or determine food quality (de Brito Sanchez, 2011;Ruedenauer et al, 2015), surprisingly little is known on the neuronal processing of chemotactile information or the contribution of different sensory modalities (i.e. tactile, gustatory and olfactory cues) in insects other than Drosophila (Masek and Keene, 2016;Singh, 1997;Zhang et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Separation of different pollen types by chemotactile sensing in Bombus terrestris.

Ruedenauer

Leonhardt

Schmalz

et al. 2017

Journal of Experimental Biology

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When tasting food, animals rely on chemical and tactile cues, which determine the animal's decision on whether to eat food. As food nutritional composition has enormous consequences for the survival of animals, food items should generally be tasted before they are eaten or collected for later consumption. Even though recent studies have confirmed the importance of, for example, gustatory cues, compared with olfaction only little is known about the representation of chemotactile stimuli at the receptor level (let alone higher brain centers) in animals other than vertebrates. To better understand how invertebrates may process chemotactile cues, we used bumblebees as a model species and combined electroantennographical (EAG) recordings with a novel technique for chemotactile antennal stimulation in bees. The recorded EAG responses to chemotactile stimulation clearly separated volatile compounds by both compound identity and concentration, and could be successfully applied to test the receptor activity evoked by different types of pollen. We found that two different pollen types (apple and almond; which were readily distinguished by bumblebees in a classical conditioning task) evoked significantly distinct neural activity already at the antennal receptor level. Our novel stimulation technique therefore enables investigation of chemotactile sensing, which is highly important for assessing food nutritional quality while foraging. It can further be applied to test other chemosensory behaviors, such as mate or nest mate recognition, or to investigate whether toxic substances, e.g. in pollen, affect neuronal separation of different food types.

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Ecology and Evolution of Communication in Social Insects

Cited by 312 publications

References 85 publications

How do cuticular hydrocarbons evolve? Physiological constraints and climatic and biotic selection pressures act on a complex functional trait

How do cuticular hydrocarbons evolve? Physiological constraints and climatic and biotic selection pressures act on a complex functional trait

The influence of slavemaking lifestyle, caste and sex on chemical profiles in Temnothorax ants: insights into the evolution of cuticular hydrocarbons

Separation of different pollen types by chemotactile sensing in Bombus terrestris.

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