Double Trouble Creature Feature: Two F-Ant-astic Manipulators

This week, we have a whole host of parasites, but only one host – wood ants belonging to the genus Formica. This unfortunate group of ants is prey to not one, but two groups of behavior altering parasites. Both types of infection result in similar behaviors: the affected ants climb up to the top of plants and hang out in broad daylight, sometimes clamping down with their mandibles to hold themselves in place. The weirdest part? The parasites aren’t even in the same kingdom!

Dicrocoelium is a genus of trematodes (a clade of parasitic flatworms) that start out life as larvae in the digestive tract of a terrestrial snail. Once they develop into their juvenile stage, the snail’s immune system kicks in, and they are excreted in balls of slime. When the ants come in contact with this snail slime, they also get a dose of worms [1]. The juvenile worms make their way into the ant’s brain, with different species targeting different regions of the cerebrum. The particular placement of the worm seems to affect the particular behavior evoked in the host. One species, D. hospes, is usually found in the region of the brain associated with decoding sensory input from the antennae. Ants infected with this parasite go out after dark and loiter in tight groups at the top of leaves and stems, perfectly motionless until morning (when the sun comes up, they and the parasite both want to get out of there to avoid desiccation in the heat). Another species behaves a little differently. It targets the subesophagial ganglion – an area used to control the mouth and neck muscles – near the mandibular nerve. Appropriately, this species of parasite makes use of the ant’s chomping ability, causing it to clamp down with its mandibles once it has climbed up a plant. In all species of Dicrocoelium, the end goal is the gut of an herbivore. The infected ants waiting at the top of leaves or grass are more likely to be grazed upon by cows, sheep, or other animals in which the parasite can reach its adult form, lay eggs, and start the cycle again [2].

D. hospes in an ant brain, on the antennal lobes, arrows pointing to worms. (Romig et al, 1980)

Pandora formicae, a fungus belonging to the order Entomophthorales, has similar results – infected ants climb up high stalks of grass or other plants and cling on using a combination of grasping with their mandibles and feet, and being fixed in place by rhizoids (root-like growths) produced by the parasite. The benefit of this behavior is a little different, since Formica ants are the end-goal hosts of this fungus. The movement to a higher altitude (and often a warmer area than the ant usually spends time in) may increase the spread of P. formicae spores, allowing the next generation to populate a new round of hosts [3]. The fungus has a wide variety of genes specialized to facilitate this infection – ranging from ones that produce chitin-dissolving proteins to break through the ants’ hard exoskeletons, to ones that cause rapid growth once the host has died [4]. So far, chemicals used to manipulate hosts haven’t been identified in this species, though we can speculate that the mechanisms could be similar to the behaviorally (though not phylogenetically) alike Ophiocordyceps [5].

P. formicae infected ant cadaver A) before and B) after the sporulation. (Malagocka et al, 2015)

Two species showing the same type of manipulation despite about 1.5 billion years of evolution separating them may seem odd, but it simply shows the power of convergent evolution, and how effective highly specialized parasitism can be as a life strategy. It also shows exactly how much we have left to learn about the mechanisms with which pathogens like these manipulate their hosts. At least we can see that even in this modern era, ant parasitism can bring families – or, you know, kingdoms – together.

[1] Tarry, D. W. (1969). Dicrocoelium dendriticum: The Life Cycle in Britain. Journal of Helminthology, 43(3–4), 403–416.
[2] Romig, T., Lucius, R., & Frank, W. (1980). Cerebral larvae in the second intermediate host of Dicrocoelium dendriticum (Rudolphi, 1819) and Dicrocoelium hospes looss, 1907 (Trematodes, Dicrocoeliidae). Zeitschrift For Parasitenkunde Parasitology Research, 63(3), 277–286.
[3] Małagocka, J., Jensen, A. B., & Eilenberg, J. (2017). Pandora formicae, a specialist ant pathogenic fungus: New insights into biology and taxonomy. Journal of Invertebrate Pathology, 143, 108–114.
[4] Małagocka, J., Grell, M. N., Lange, L., Eilenberg, J., & Jensen, A. B. (2015). Transcriptome of an entomophthoralean fungus (Pandora formicae) shows molecular machinery adjusted for successful host exploitation and transmission. Journal of Invertebrate Pathology, 128, 47–56.
[5] de Bekker C., Ohm R. A., Evans H. C., Brachmann A., Hughes D. P. (2017). Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins. Sci Rep. 2017;7(1):12508.

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