Alarm pheromone processing in the ant brain: an evolutionary perspective

Abstract

Social insects exhibit sophisticated communication by means of pheromones, one example of which is the use of alarm pheromones to alert nestmates for colony defense. We review recent advances in the understanding of the processing of alarm pheromone information in the ant brain. We found that information about formic acid and n-undecane, alarm pheromone components, is processed in a set of specific glomeruli in the antennal lobe of the ant Camponotus obscuripes. Alarm pheromone information is then transmitted, via projection neurons (PNs), to the lateral horn and the calyces of the mushroom body of the protocerebrum. In the lateral horn, we found a specific area where terminal boutons of alarm pheromone-sensitive PNs are more densely distributed than in the rest of the lateral horn. Some neurons in the protocerebrum responded specifically to formic acid or n-undecane and they may participate in the control of behavioral responses to each pheromone component. Other neurons, especially those originating from the mushroom body lobe, responded also to non-pheromonal odors and may play roles in integration of pheromonal and non-pheromonal signals. We found that a class of neurons receive inputs in the lateral horn and the mushroom body lobe and terminate in a variety of premotor areas. These neurons may participate in the control of aggressive behavior, which is sensitized by alarm pheromones and is triggered by non-pheromonal sensory stimuli associated with a potential enemy. We propose that the alarm pheromone processing system has evolved by differentiation of a part of general odor processing system.

Keywords: aggression; antennal lobe; communication; evolution; mushroom body; pheromone; social insect.

Figure 1

Three-dimensional reconstructions of major neuropils of the ant brain viewed ventrally (A) and dorsally (B). The protocerebrum (green) consists of the mushroom body, the lateral PR (l pr) that includes the lateral horn (l ho), the ventro-lateral PR (v-l pr), the medial and dorsal PR (m pr and d pr), the lateral accessory lobe (lal) and the central complex (cc: khaki). The mushroom body consists of calyces (ca: blue), the pedunculus (ped: light blue) and the vertical and medial lobes (v lob, m lob: light blue, broken line). The medulla (med: yellow) and the lobula (lo: light yellow) are the second and third optic neuropils. The deutocerebrum consists of the antennal lobe (a lob: orange) and the dorsal lobe (d lob: magenta). Scale bar = 100 μm. Modified from Yamagata et al. (2007).

Figure 2

An alarm pheromone-sensitive uniglomerular PN. (A) Reconstruction of an alarm pheromone-sensitive PN from confocal sections viewed ventrally. The soma is located at the medial cell cluster of the deutocerebrum. The dendritic arbors cover the AS1 glomerulus in the antennal lobe (a lob). The axon ascends through the medial anteno-cerebral tract and terminates in the lip region of the calyces (ca) and the lateral horn (l ho). me: medulla, ped: pedunculus. (B) Responses of the PN to formic acid. 10% formic acid indicates that it was diluted to 1/10 by distilled water. Modified from Yamagata et al. (2006).

Figure 3

Three-dimensional reconstruction of the antennal lobe of the ant, viewed ventrally (A) and horizontally (B). Five glomeruli (blue spheroids, AS1-AS5) from which alarm pheromone-sensitive uniglomerular PNs originated are mapped into the reconstructed antennal lobe (red). f+ and u+ indicate that the PN originating from that glomerulus was sensitive to formic acid and n-undecane, respectively. Alarm pheromone-sensitive multiglomerular PNs had dendrites in some of the AS glomeruli as well as in a number of glomeruli in the dorsalmost part (yellow) of the ventral glomerular cluster. Modified from Yamagata et al. (2006).

Figure 4

A model of alarm pheromone processing system in the ant brain. Organization of the alarm pheromone processing system in the worker of the ant C. obscuripes is schematically compared with the general odor processing system and sex-pheromone processing system of other insects, such as moths, cockroaches, honeybees and fruit-flies. There is segregated, yet partially overlapped, representation of alarm pheromone information in the primary (antennal lobe) and a secondary (lateral horn) olfactory center. This is in contrast to segregated representations of sex-pheromone information. For details, see text.

Figure 5

Schematic model of processing pathways for alarm pheromone signals in the ant brain. The pathways are based on observations of 63 pheromone-sensitive interneurons. Visual pathways to the dorsal protocerebrum and to the lateral accessory lobe and mechanosensory pathway to the dorsal lobe are based on our unpublished observations. sg: subesophageal ganglion; tg: thoracic ganglia; ag: abdominal ganglia. For other abbreviations, see legend of Figure 1. *l pr in this figure indicates the lateral protocerebrum excluding the lateral horn. The distinction of sensory, association, premotor and motor areas is based on studies of basic organizations of the cockroach brain (Okada et al., 2003). To facilitate interpretation of data, we classified behavioral responses into (1) initial preparatory phase of alarm behavior, (2) alarm behavior and (3) aggression against a potential enemy, as reviewed by Blum (1985) and Vander Meer and Alonso (1998). Modified from Yamagata et al. (2007).

Figure 6

Pheromone-sensitive wide-field protocerebral neuron. (A) Reconstruction of the neuron from confocal sections viewed ventrally. The soma is located at the boundary between the protocerebrum and the antennal lobe (a lob). The dendrites cover the vertical lobe (v lob), the medial protocerebrum (m pr) and a part of the lateral horn (l ho) and the lateral accessory lobe (lal). The axon takes a circular route around the pedunculus (ped) and extends terminal arbors in the lateral protocerebrum (l pr) and the dorsal protocerebrum (d pr). One axon descends toward the subesophageal ganglion (arrow). For other abbreviations, see legend of Figure 1. Scale bar = 100 μm. (B) Responses to formic acid, 1-hexanol and banana odor. Application of formic acid evoked excitatory response. 1-Hexanol evoked bi-phasic responses, and banana odor elicited a brief spike discharge. Modified from Yamagata et al. (2007).