Behavior altering parasites are found world-wide. They come from a wide array of taxonomic groups – fungi, single-celled protists, a variety of worms, and even the familiar arthropods. They can target any type of animal, some are specialists that only affect a single species, others can be found in hundreds or even thousands of species. In just the six parasites covered in this blog series we see many different methods of manipulation. Paragordius tricuspidatus – the hairworm that causes crickets to jump into water and drown – may manipulate neurogenesis (the formation of new cells) and amino acid levels in its host [1]. The zebrafish parasite Pseudoloma neurophilia (a fungus) and the ant parasites of the Dicrocoelium genus (trematodes) both cause pressure on nerve cells that could lead to behavioral changes [2][3]. Pandora formicae and Ophiocordyceps unilateralis are two ant-controlling fungi that use chemical signals to control the whims of their hosts [4][5]. Similarly, the spider-parasitic wasps of the genus Polysphincta might use their own growth hormones to trigger a beneficial behavioral change in their hosts [6]. Toxoplasma gondii – the protist that most notably affects cats, rats, and humans – turns the host’s immune system against itself in a chain reaction that leads to neurotransmitter imbalances and a wide array of changes in the brain of the host [7]. Even the motivations of the parasites differ. Some of them are just trying to find their next host – usually a larger animal in which they can reproduce. In this category, we find Dicrocoelium spp., T. gondii, and many others, such as the snail-infecting flatworm, Leucochloridium paradoxum [8]. Others just want to grow up and be freed into the perfect environment to spend the rest of their life, like the water-dwelling P. tricuspidatus, the fungus P. formicae, or the juvenile Polysphincta wasps. Closely schooling zebrafish are easier targets for P. neurophilia, so this anxiety-inducing parasite has a clear evolutionary benefit from its behavior altering ways.
There are, of course, similarities as well. Many of these parasites spend their early life stages manipulating hosts, but stop their behavior-changing ways once they reach a reproductive stage. The one exception in our selection is P. neurophilia, which completes its life cycle entirely within the zebrafish host. Other than the wasps, they are all endoparasites – they live inside their hosts. They target either neurons, neurotransmitters, or hormones – the physiological basis of action or feeling as we currently understand it.
So what exactly is the point? Why do we study parasites that bother bugs and snails and fish? Why does it matter how they’re different or the same or what chemicals they use? You could say it’s just curiosity – they’re interesting and a little scary, and we want to understand the world around us. You could also say it’s precaution, since Toxoplasma gondii shows us that we are far from immune to the effects of outside forces in our brains. We have a lot to learn about the brain, motivation, and thought, and looking into the minds of these animals and the way they can be changed gives us insight into some of the mechanisms the body has to facilitate planning, action, and decision making to the degree that they appear in these models.
Sorry for the lack of jokes this week, guess I’m pretty bugged out about this all. I’m not fishing for sympathy though, in fact it’s been pretty fungi. I wouldn’t protist writing about even more parasites if I had to. I can’t worm my way out of this one…there’s no puns for wasps.
[1] Thomas, F., Ulitsky, P., Augier, R., Dusticier, N., Samuel, D., Strambi, C., … Cayre, M. (2003). Biochemical and histological changes in the brain of the cricket Nemobius sylvestris infected by the manipulative parasite Paragordius tricuspidatus (Nematomorpha). International Journal for Parasitology, 33(4), 435–443. https://doi.org/10.1016/S0020-7519(03)00014-6
[2] Spagnoli, S. T., Xue, L., Murray, K. N., Chow, F., & Kent, M. L. (2015). Pseudoloma neurophilia: a retrospective and descriptive study of nervous system and muscle infections, with new implications for pathogenesis and behavioral phenotypes. Zebrafish, 12(2), 189-201. https://doi.org/10.1089/zeb.2014.1055
[3] 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. https://doi.org/10.1007/BF00931990
[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. https://doi.org/10.1016/j.jip.2015.05.001
[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. https://doi.org/10.1038/s41598-017-12863-w
[6] Kloss, T. G., Gonzaga, M. O., de Oliveira, L. L., & Sperber, C. F. (2017). Proximate mechanism of behavioral manipulation of an orb-weaver spider host by a parasitoid wasp. PLoS ONE, 12(2), 1–11. https://doi.org/10.1371/journal.pone.0171336
[7] Ihara, F., Nishimura, M., Muroi, Y., Mahmoud, M. E., Yokoyama, N., Nagamune, K., & Nishikawa, Y. (2016). Toxoplasma gondii Infection in Mice Impairs Long-Term Fear Memory Consolidation through Dysfunction of the Cortex and Amygdala. Infection and Immunity, 84(10), 2861–2870. https://doi.org/10.1128/IAI.00217-16
[8] Wesolowska, W., & Wesolowski, T. (2014). Do Leucochloridium sporocysts manipulate the behaviour of their snail hosts? Journal of Zoology, 292(3), 151–155. https://doi.org/10.1111/jzo.12094