Chemically armed mercenary ants protect fungus-farming societies

Abstract

The ants are extraordinary in having evolved many lineages that exploit closely related ant societies as social parasites, but social parasitism by distantly related ants is rare. Here we document the interaction dynamics among a Sericomyrmex fungus-growing ant host, a permanently associated parasitic guest ant of the genus Megalomyrmex, and a raiding agro-predator of the genus Gnamptogenys. We show experimentally that the guest ants protect their host colonies against agro-predator raids using alkaloid venom that is much more potent than the biting defenses of the host ants. Relatively few guest ants are sufficient to kill raiders that invariably exterminate host nests without a cohabiting guest ant colony. We also show that the odor of guest ants discourages raider scouts from recruiting nestmates to host colonies. Our results imply that Sericomyrmex fungus-growers obtain a net benefit from their costly guest ants behaving as a functional soldier caste to meet lethal threats from agro-predator raiders. The fundamentally different life histories of the agro-predators and guest ants appear to facilitate their coexistence in a negative frequency-dependent manner. Because a guest ant colony is committed for life to a single host colony, the guests would harm their own interests by not defending the host that they continue to exploit. This conditional mutualism is analogous to chronic sickle cell anemia enhancing the resistance to malaria and to episodes in human history when mercenary city defenders offered either net benefits or imposed net costs, depending on the level of threat from invading armies.

Keywords: Attini; Solenopsidini; evolutionary transition; symbiosis.

Fig. 1.

Subfamily and tribe-level tree after Brady et al. (8) indicating the different phylogenetic positions of the interacting ant species. (A) The fungus-growing ant host S. amabilis. (B) The guest ant social parasite M. symmetochus (in a stilted stance, emitting volatile alkaloids from its protruding sting). (C) The G. hartmani raiding agro-predator. M. symmetochus and G. hartmani have independently specialized on using S. amabilis fungus gardens and brood as food.

Fig. 2.

Defense efficiencies of host and guest ants. (A) The resulting mortality after a single G. hartmani agro-predator interacted with groups of two to eight S. amabilis host ants (blue Petri dish) or M. symmetochus guest ants (orange Petri dish) after 24 h. Defender category significantly affected G. hartmani worker mortality (binomial GLZ, LR χ²= 42.34, P < 0.0001), with S. amabilis effective in killing only when greatly outnumbering G. hartmani (blue dots) and M. symmetochus significantly more effective in killing regardless of their number (orange dots). (B) The overall mortality inflicted by the G. hartmani worker on host or guest ant defenders differed significantly (binomial GLZ, LR χ² = 18.84, P < 0.0001), with S. amabilis defenders (blue dots) taking proportionally much higher casualties. The proportional mortality of both defenders decreased significantly with an increasing number of defenders (binomial GLZ, LR χ² = 7.29, P = 0.0069), but this decrease did not differ between the defending species (interaction between number and species of defenders, binomial GLZ, LR χ² = 0.0996, P = 0.752). Ant drawings courtesy of Rozlyn Haley.

Fig. 3.

Host survival rates and raider mutilations. When threatened, M. symmetochus guest ants use toxic venom, whereas Sericomyrmex hosts mutilate intruders by removing appendages. (A) When 18 host ants were confronted with 2 intruding Gnamptogenys workers without (0) or with (3 or 6) Megalomyrmex guest ants, the proportion of S. amabilis deaths was decreased (binomial GLZ, LR χ² = 10.93, P = 0.0009). (B) The same increased number of guest ants was also associated with a reduced rate of extremity damage in G. hartmani workers (binomial GLZ, LR χ² = 14.18, P = 0.0002), consistent with the fact that the agro-predator raiders were no longer attacked by S. amabilis defenders because they were killed by guest ants rather than by physical mutilation by the host ants. Ant drawings courtesy of Rozlyn Haley.

Fig. 4.

A G. hartmani laboratory colony was given repeated choices between four pairs of S. amabilis host colonies with or without M. symmetochus guest ants (size-matched so that total number of ants, fungus garden volume, and nest box size were approximately equal). Gray bars represent the number of replicate trials for each pair, and dark-colored bars represent raids that were initiated after single G. hartmani scouts had inspected one or both of the maize separations with the experimental S. amabilis colonies. Recruited columns of raiding G. hartmani were preferentially directed toward S. amabilis colonies without guest ants (binomial GLZ, LR χ² = 18.12, P < 0.0001). Chemical structures (Upper Left) represent the M. symmetochus venom compounds (5Z,8E)-3-butyl-5-hexylpyrrolizidine and (5E,8E)-3-butyl-5-hexylpyrrolizidine, detected from air samples. Ant drawings courtesy of Rozlyn Haley.