Convergent evolution of the Dufour’s gland secretion as a propaganda substance in the slave-making ant genera Protomognathus and Harpagoxenus

Abstract

Slave-making ants are social parasites which exploit the workforce of heterospecific slaves for their own reproduction, and to this end they have developed a variety of morphological and behavioural adaptations. Furthermore, social parasites utilize the chemical communication system of their hosts by breaking their nestmate recognition code, and some slave-maker species additionally employ semiochemicals as weapons during colony foundation and slaveraiding. Here, we demonstrate the use of such a 'propaganda allomone' by the North American myrmicine slave-maker Protomognathus americanus. This substance is produced in the Dufour's gland and may be employed during slave raids to elicit panic among defending host workers. Slave-maker Dufour's gland secretions evoked agitation and heightened levels of activity among host workers when applied directly on a host nest, and strong aggressive responses of nestmates when applied onto a host worker. Although the hosts own Dufour's gland secretion also elicits intra-colonial fights, no support for the hypothesis was found that the slave-maker propaganda substance mimics a fertility signal of the host, as the chemical profile of the gland secretions is highly divergent between the two species. Preliminary results on the chemical composition of the secretion obtained by gas chromatography indicate that the propaganda substance of P. americanus differs from that of the related European slavemaker Harpagoxenus sublaevis, and is thus likely to represent an independent evolutionary development.

Function of the Dufour’s gland in solitary and social Hymenoptera

“…Such compounds may also act as a repellent and thereby facilitate usurpation of a host colony (Ruano et al 2005). Another function of Dufour's gland in slave making ants is to act as a source of propaganda substances that elicit panic among defending host workers, thereby increasing the efficiency of slave capturing raids (Brandt et al 2006). Dufour's gland compounds have also been found to act as sex pheromones, and can also be involved in the calling behavior exhibited by females, whereby virgin gynes place themselves in strategic positions outside their nests and "call" for mates by releasing sex pheromones (Hölldobler and Wust 1973, Hölldobler and Wilson 1990, Ayasse et al 2001).…”

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

“…All of them raid host colonies for slaves, but their fighting strategies differ [31,[39][40][41]. Temnothorax americanus, the oldest slavemaker in this clade, shows little evidence of chemical mimicry [30,41], but uses the Dufour's gland secretion to divert host aggression [42,43]. Temnothorax duloticus on the contrary, efficiently uses its sting [39].…”

The placid slavemaker: avoiding detection and conflict as an alternative, peaceful raiding strategy

“…Chemical manipulation of host behavior is a fourth and commonly used strategy by which parasites use offensive chemicals to disrupt the host defense systems. While entering host colonies, social parasites use substances released from the Dufour's, the Pygidial, or the Poison gland, which serve as manipulative alarm signals or chemical weapons (Lenoir et al 2001) and as appeasement substances to circumvent aggressive escalations, such as attacks directed toward the social parasite (Mori et al 2000;Brandt et al 2006) Slavemaking ants are social parasites that have to successfully invade host colonies recurrently during their life cycle, in contrast to many other social parasites, such as the workerless inquilines, that do so only once in their life. Most slavemakers are obligate parasites that are contingent on their slave workforce, which oversees colony maintenance including caring for the parasites' offspring.…”