Lycaenid Caterpillar Secretions Manipulate Attendant Ant Behavior

Abstract

Mutualistic interactions typically involve the exchange of different commodities between species. Nutritious secretions are produced by a number of insects and plants in exchange for services such as defense. These rewards are valuable metabolically and can be used to reinforce the behavior of symbiotic partners that can learn and remember them effectively. We show here novel effects of insect exocrine secretions produced by caterpillars in modulating the behavior of attendant ants in the food-for-defense interaction between lycaenid butterflies and ants. Reward secretions from the dorsal nectary organ (DNO) of Narathura japonica caterpillars function to reduce the locomotory activities of their attendant ants, Pristomyrmex punctatus workers. Moreover, workers that feed from caterpillar secretions are significantly more likely to show aggressive responses to eversion of the tentacle organs of the caterpillars. Analysis of the neurogenic amines in the brains of workers that consumed caterpillar secretions showed a significant decrease in levels of dopamine compared with controls. Experimental treatments in which reserpine, a known inhibitor of dopamine in Drosophila, was fed to workers similarly reduced their locomotory activity. We conclude that DNO secretions of lycaenid caterpillars can manipulate attendant ant behavior by altering dopaminergic regulation and increasing partner fidelity. Unless manipulated ants also receive a net nutritional benefit from DNO secretions, this suggests that similar reward-for-defense interactions that have been traditionally considered to be mutualisms may in fact be parasitic in nature.

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

“…Thus, the unambiguous identification of a manipulation event requires an understanding of the physiological and molecular mechanisms that cause these alterations. In other words, the observation of a manipulation effect does not suffice to characterize the manipulator as a parasite (Heil, 2015), because manipulation effects can also be exerted by mutualists (Wright et al, 2013;Heil et al, 2014;Hojo et al, 2015). Only the demonstration that a certain phenotypic alteration in the host is under the genetic control of the parasite and that it enhances the fitness of the parasite vi an enhancement of its transmission rate, while decreasing the fitness of the host, would provide clear evidence in favor of adaptive host manipulation.…”

Manipulators live better, but are they always parasites?

“…Strikingly, Hojo et al also reported an enhanced aggressiveness of manipulated ants. This behavioural change was associated with altered dopamine levels in the brains of the ants, albeit ants that had access to DNO secretions contained lower, rather than higher levels of dopamine [1]. The different directions in the changes in dopamine levels in manipulated mammals and ants clearly represent an interesting research subject per se.…”

“…In a new ground breaking study Hojo et al [1] report partner manipulation for an interaction that previously was considered to be a reward-for-defence mutualism. Lycaenid caterpillars secrete a metabolically valuable liquid from their dorsal nectary organ (DNO) and are tended by ants, which feed on this reward and defend the caterpillar against predators.…”

“…Recently, Hojo et al discovered that the DNO secretion decreases ant locomotion activity and increases the aggressiveness of the ants. Manipulated ants also were more likely to return to tend the caterpillar [1]. In simple terms, the caterpillar gains a reliable standing army of defending ants, whereas the ants pay the cost, because they become dependent.…”

“…In simple terms, the caterpillar gains a reliable standing army of defending ants, whereas the ants pay the cost, because they become dependent. The authors conclude that 'reward-for-defence interactions that have traditionally been considered to be mutualisms may in fact be parasitic in nature' [1].…”