The intricate relationships between parasites and their hosts often involve a choreography of behavioral changes, with parasites manipulating their hosts in a way that enhances - or seemingly enhances – their transmission (Hughes et al., 2012; Moore, 2002; Poulin, 2010). Host manipulation is increasingly acknowledged as a pervasive adaptive transmission strategy employed by parasites, and as such is one of the most remarkable manifestations of the extended phenotype (Dawkins, 1982).

In this laboratory study, Rigaud et al. (2023) delved into the time course of antipredator behavioral modifications induced by the acanthocephalan Pomphorhynchus laevis in its amphipod intermediate host Gammarus pulex. This system has a good foundation of prior knowledge (Bakker et al., 2017; Fayard et al., 2020; Perrot-Minnot et al., 2023), nicely drawn upon for the present work. This parasite orchestrates a switch from predation suppression, during the noninfective phase, to predation enhancement upon maturation. Specifically, G. pulex infected with the non-infective acanthella stage of the parasite can exhibit increased refuge use and reduced activity compared to uninfected individuals (Dianne et al., 2011, 2014), leading to decreased predation by trout (Dianne et al., 2011). In contrast, upon reaching the infective cystacanth stage, the parasite can enhance the susceptibility of its host to trout predation (Dianne et al., 2011).

The present work aimed to understand the temporal sequence of these behavioral changes across the entire ontogeny of the parasite. The results confirmed the protective role of P. laevis during the acanthella stage, wherein infected amphipods exhibited heightened refuge use. This protective manipulation, however, became significant only later in the parasite's ontogeny, suggesting a delayed investment strategy, possibly influenced by the extended developmental time of P. laevis. The protective component wanes upon reaching the cystacanth stage, transitioning into an exposure strategy, aligning with theoretical predictions and previous empirical work (Dianne et al., 2011; Parker et al., 2009). The switch was behavior-specific. Unlike the protective behavior, a decline in the amphipod activity rate manifested early in the acanthella stage and persisted throughout development, suggesting potential benefits of reduced activity for the parasite across multiple stages. Furthermore, the findings challenge previous assumptions regarding the condition-dependency of manipulation, revealing that the parasite-induced behavioral changes predominantly occurred in the presence of cues signaling potential predators. Finally, while amphipods infected with acanthella stages displayed survival rates comparable to their uninfected counterparts, increased mortality was observed in those infected with cystacanth stages.

Understanding the temporal sequence of host behavioral changes is crucial for deciphering whether it is adaptive to the parasite or not. This study stands out for its meticulous examination of multiple behaviors over the entire ontogeny of the parasite highlighting the complexity and condition-dependent nature of manipulation. The protective-then-expose strategy emerges as a dynamic process, finely tuned to the developmental stages of the parasite and the ecological challenges faced by the host. The delayed emergence of protective behaviors suggests a strategic investment by the parasite, with implications for the host's survival and the parasite's transmission success. The differential impact of infection on refuge use and activity rate further emphasizes the need for a multidimensional approach in studying parasitic manipulation (Fayard et al., 2020). This complexity demands further exploration, particularly in deciphering how trophically-transmitted parasites shape the behavioral landscape of their intermediate hosts and its temporal dynamic (Herbison, 2017; Perrot-Minnot & Cézilly, 2013).  As we discover the many subtleties of these parasitic manipulations, new avenues of research are unfolding, promising a deeper understanding of the ecology and evolution of host-parasite interactions.

References

Bakker, T. C. M., Frommen, J. G., & Thünken, T. (2017). Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology, 123(11), 779–784. https://doi.org/10.1111/eth.12660

Dawkins, R. (1982). The extended phenotype: The long reach of the gene (Reprinted). Oxford University Press.

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Gaillard, M., Léger, E., & Rigaud, T. (2011). Protection first then facilitation: A manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution, 65(9), 2692–2698. https://doi.org/10.1111/j.1558-5646.2011.01330.x

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Guvenatam, A., & Rigaud, T. (2014). Parasite-induced alteration of plastic response to predation threat: Increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. International Journal for Parasitology, 44(3–4), 211–216. https://doi.org/10.1016/j.ijpara.2013.11.001

Fayard, M., Dechaume‐Moncharmont, F., Wattier, R., & Perrot‐Minnot, M. (2020). Magnitude and direction of parasite‐induced phenotypic alterations: A meta‐analysis in acanthocephalans. Biological Reviews, 95(5), 1233–1251. https://doi.org/10.1111/brv.12606

Herbison, R. E. H. (2017). Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation. Frontiers in Ecology and Evolution, 5, 102. https://doi.org/10.3389/fevo.2017.00102

Hughes, D. P., Brodeur, J., & Thomas, F. (2012). Host manipulation by parasites. Oxford university press.

Moore, J. (2002). Parasites and the behavior of animals. Oxford University Press.

Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K., & Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution, 63(2), 448–458. https://doi.org/10.1111/j.1558-5646.2008.00565.x

Perrot-Minnot, M.-J., & Cézilly, F. (2013). Investigating candidate neuromodulatory systems underlying parasitic manipulation: Concepts, limitations and prospects. Journal of Experimental Biology, 216(1), 134–141. https://doi.org/10.1242/jeb.074146

Perrot-Minnot, M.-J., Cozzarolo, C.-S., Amin, O., Barčák, D., Bauer, A., Filipović Marijić, V., García-Varela, M., Servando Hernández-Orts, J., Yen Le, T. T., Nachev, M., Orosová, M., Rigaud, T., Šariri, S., Wattier, R., Reyda, F., & Sures, B. (2023). Hooking the scientific community on thorny-headed worms: Interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite, 30, 23. https://doi.org/10.1051/parasite/2023026

Poulin, R. (2010). Parasite Manipulation of Host Behavior. In Advances in the Study of Behavior (Vol. 41, pp. 151–186). Elsevier. https://doi.org/10.1016/S0065-3454(10)41005-0

Rigaud, T., Balourdet, A., & Bauer, A. (2023). Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: The switch in manipulation according to parasite developmental stage differs between behaviors. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2023.04.25.538244

Whiteflies are serious global pests that feed on phloem sap of many agricultural crop plants. Like other phloem feeders, whiteflies rely on a primary-symbiont to supply their poor, sugar-based diet. Over time, the genomes of primary-symbionts become degraded, and they are either been replaced or complemented by co-hosted secondary-symbionts (McCutcheon and Moran 2012). In Bemisia tabaci species complex, the primary-symbiont is Candidatus Portiera aleyrodidarium, with seven secondary-symbionts that have been described to date. The prevalence and dynamics of these secondary-symbionts have been studied in various whitefly populations and genetic groups around the world, and certain combinations are determined under specific biotic and environmental factors (Zchori-Fein et al. 2014).

To understand the potential metabolic or other interactions of various secondary-symbionts with Ca. Portiera aleyrodidarium and the hosts, Mouton et al. used metabarcoding approach and diagnostic PCR confirmation, to describe symbiont compositions in a collection of whiteflies from eight populations with four genetic groups in Burkina Faso. They found that one of the previously recorded secondary-symbiont from Asian whitefly populations, Candidatus Hemipteriphilus asiaticus, is also found in the tested African whiteflies. The newly identified Ca. Hemipteriphilus asiaticus forms a different strain than the ones described in Asia, and is found in high prevalence in six of the tested populations and in three genetic groups. They also showed that Portiera densities are not affected by the presence of Ca. Hemipteriphilus asiaticus. The authors suggest that based on its high prevalence, Ca. Hemipteriphilus asiaticus may benefit certain whitefly populations, however, there is no attempt to test this assumption or to relate it to environmental factors, or to identify the source of introduction.

Mouton et al. bring new perspectives to the study of complex hemipteran symbioses, emphasizing the need to use both unbiased approaches such as metabarcoding, together with a priori methods such as PCR, in order to receive a complete description of symbiont population structures. Their findings are awaiting future screens for this secondary-symbiont, as well as its functional genomics and experimental manipulations to clarify its role. Discoveries on whitefly-symbionts delicate interactions are required to develop alternative control strategies for this worldly devastating pest.

References

McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nature Reviews Microbiology, 10, 13–26. https://doi.org/10.1038/nrmicro2670

Mouton L, Henri H, Romba R, Belgaidi Z, Gnankiné O, Vavre F (2022) Analyses of symbiotic bacterial communities in the plant pest Bemisia tabaci reveal high prevalence of Candidatus Hemipteriphilus asiaticus on the African continent. bioRxiv, 2021.10.06.463217, ver. 3 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.10.06.463217

Zchori-Fein E, Lahav T, Freilich S (2014) Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Frontiers in Microbiology, 5. https://doi.org/10.3389/fmicb.2014.00310