Malaria is a vector-borne parasitic disease found in 91 countries with an estimated of 228 million cases occurred worldwide during 2018. The 93% (213 million) of those cases were reported in the African Region (WHO 2019). Six species of Plasmodium parasites can produce the disease but only P. falciparum and P. vivax are the predominant species globally. More than 40 species of Anopheles mosquitoes are important malaria vectors (Asley et al. 2018). Intrinsic (genetic background, parasite susceptibility) and extrinsic (feeding host preference, host diversity and availability, mosquito abundance) factors affect the capacity of mosquitoes to vector the disease (Macdonald 1952). Malaria is prevented by chemoprophylaxis, vaccination, bite-avoidance and vector-control measures. The mainstays of vector control are long-lasting insecticide (pyrethroid) treated nets and indoor residual spraying with insecticides (Asley et al. 2018). The widespread use of pyrethroid insecticides forced the emergence of insecticide resistance in malaria vectors reducing the insecticidal effect. Mosquitoes can modify their behaviour avoiding insecticide contact and so potentially reducing vector control tools efficacy. In this sense, Diop et al. (2020) investigated whether pre-exposure to an Insecticide-Treated Net (ITN) modulates the mosquito ability to take a blood meal in Anopheles gambiae. By means of video recording experiments the authors analyzed how the feeding/bitting behaviour was affected by kdr mutation genotypes (homozygous susceptible – SS-, heterozygotes -RS- and homozygous resistant -RR-) when exposed to two different insecticides (permethrin and deltamethrin). According to the results, the blood-feeding success did not differ between the three genotypes in the absence of insecticide exposure. However, authors observed differences in the feeding duration and blood meal size. In example, RR mosquitoes spent less time taking their blood meal than RS and SS. On the other hand, RS mosquitoes took higher blood volumes than RR females. These differences can affect the mosquito fitness by decreasing/increasing the likelihood to be killed by the host defensive behavior or increase the oogenesis so enhancing fecundity. Regarding the effect of exposition to insecticides authors detected a strong relationship between kdr genotype and Knock Down (KD) phenotype when mosquitoes were exposed to Permethrin. Previously, the authors have evidenced that RR mosquitoes prefer a host protected by a permethrin-treated net rather than an untreated net and that heterozygotes RS mosquitoes have a remarkable ability to find a hole into a bet net (Diop et al. 2015, Porciani et al. 2017). With data here obtained, they demonstrated that kdr homozygous resistant An. gambiae displayed enhanced feeding success when exposed to permethrin ITN. The changes observed in the feeding/biting mosquito behaviour can affect their fitness shaping the evolution of the insecticide resistance in mosquitoes’ natural populations. Moreover, this may also alter parasite transmission dynamics by modifying vector/host interactions and so vector capacity.

References

World Health Organization (2019). World malaria report 2019. Geneva: World Health Organization; 2019. ISBN 978-92-4-156572-1
Ashley EA, Pyae Phyo A, Woodrow CJ (2018). Malaria. Lancet. 391(10130):1608‐1621. doi: 10.1016/S0140-6736(18)30324-6
Macdonald G (1952). The analysis of equilibrium in malaria. Trop Dis Bull 49: 813-828.
Diop MM, Chandre F, Rossignol M, Porciani A, Château M, Moiroux N and Pennetier, C. (2020). Sub-lethal insecticide exposure affects host biting efficiency of Kdr-resistant Anopheles gambiae. bioRxiv 653980, ver. 4 peer-reviewed and recommended by PCI Zoology. doi: 10.1101/653980
Diop MM, Moiroux N, Chandre F, Martin-Herrou H, Milesi P, Boussari O, et al. (2015) Behavioral cost and overdominance in Anopheles gambiae. PLoS ONE. 10(4):e0121755. doi: 10.1371/journal.pone.0121755
Porciani A, Diop M, Moiroux N, Kadoke-Lambi T, Cohuet A, Chandre F, et al. (2017) Influence of pyrethroïd-treated bed net on host seeking behavior of Anopheles gambiae s.s. carrying the kdr allele. PLOS ONE. 12(7):e0164518. doi: 10.1371/journal.pone.0164518

Redistribution of domesticated and non domesticated species by humans profoundly affected earth biogeography and in return human activities. This process accelerated exponentially since human expansion out of Africa, leading to the modern global, highly connected and homogenized, agriculture and trade system (Mack et al. 2000, Jaksic and Castro 2021), that threatens biological diversity and genetic resources. To accompany quarantine and control effort, the reconstruction of invasion routes provides valuable information that help identifying critical nodes and edges in the global networks (Estoup and Guillemaud 2010, Cristescu 2015). Historical records and genetic markers are the two major sources of information of this corpus of knowledge on Anthropocene historical phylogeography. With the advances of molecular genetics tools, the genealogy of these introductions events could be revisited and empowered. Due to their idiosyncrasy and intimate association with the contingency of human trades and activities, understanding the invasion and domestication routes require particular statistical tools (Fraimout et al. 2017).

Because it encompasses all these theoretical, ecological and economical implications, I am pleased to recommend the readers of PCI Zoology this article by Mallez et al. (2021) on pine wood nematode invasion route inference from genetic markers using Approximate Bayesian Computation (ABC) methods.

Economically and ecologically, this pest, is responsible for killing millions of pines worldwide each year. The results show these damages and the global genetic patterns are due to few events of successful introductions. The authors consider that this low probability of introductions success reinforces the idea that quarantine measures are efficient. This is illustrated in Europe where the pine-worm has been quarantined successfully in the Iberian Peninsula since 1999. Another relevant conclusion is that hybridization between invasive populations have not been observed and implied in the invasion process. Finally the present study reinforced the role of Asiatic bridgehead populations in invasion process including in Europe.

Methodologically, for the first time, ABC was applied to this species. A total of 310 individual sequences were added to the Mallez et al. (2015) microsatellite dataset. Fraimoult et al. (2017) showed the interest to apply random forest to improve scenario selection in ABC framework. This method, implemented in the DiYABC software (Collin et al. 2020) for invasion route scenario selection allows to handle more complex scenario alternatives and was used in this study. In this article by Mallez et al. (2021), you will also find a clear illustration of the step-by-step approach to select scenario using ABC techniques (Lombaert et al. 2014). The rationale is to reduce number of scenario to be tested by assuming that most recent invasions cannot be the source of the most ancient invasions and to use posterior results on most ancient routes as prior hypothesis to distinguish following invasions. The other simplification is to perform classical population genetic analysis to characterize genetic units and representative populations prior to invasion routes scenarios selection by ABC.

Yet, even when using the most advanced Bayesian inference methods, it is recognized by the authors that the method can be pushed to its statistical power limits. The method is appropriate when population show strong inter-population genetic structure. But the high number of differentiated populations in native area can be problematic since it is generally associated to incomplete sampling scheme. The hypothesis of ghost populations source allowed to bypass this difficulty, but the authors consider simulation studies are needed to assess the joint effect of genetic diversity and number of genetic markers on the inference results in such situation. Also the need to use a stepwise approach to reduce the number of scenario to test has to be considered with caution. Scenarios that are not selected but have non negligible posterior, cannot be ruled out in the constitution of next step scenarios hypotheses.

Due to its interest to understand this major facet of Anthropocene, reconstruction of invasion routes should be more considered as a guide to damper biological homogenization process.

References

Collin, F.-D., Durif, G., Raynal, L., Lombaert, E., Gautier, M., Vitalis, R., Marin, J.-M. and Estoup, A. (2020) Extending Approximate Bayesian Computation with Supervised Machine Learning to infer demographic history from genetic polymorphisms using DIYABC Random Forest. Authorea. doi: https://doi.org/10.22541/au.159480722.26357192

Cristescu, M.E. (2015) Genetic reconstructions of invasion history. Molecular Ecology, 24, 2212–2225. doi: https://doi.org/10.1111/mec.13117

Estoup, A. and Guillemaud, T., (2010) Reconstructing routes of invasion using genetic data: Why, how and so what? Molecular Ecology, 9, 4113-4130. doi: https://doi.org/10.1111/j.1365-294X.2010.04773.x

Fraimout, A., Debat, V., Fellous, S., Hufbauer, R.A., Foucaud, J., Pudlo, P., Marin, J.M., Price, D.K., Cattel, J., Chen, X., Deprá, M., Duyck, P.F., Guedot, C., Kenis, M., Kimura, M.T., Loeb, G., Loiseau, A., Martinez-Sañudo, I., Pascual, M., Richmond, M.P., Shearer, P., Singh, N., Tamura, K., Xuéreb, A., Zhang, J., Estoup, A. and Nielsen, R. (2017) Deciphering the routes of invasion of Drosophila suzukii by Means of ABC Random Forest. Molecular Biology and Evolution, 34, 980-996. doi: https://doi.org/10.1093/molbev/msx050

Jaksic, F.M. and Castro, S.A. (2021). Biological Invasions in the Anthropocene, in: Jaksic, F.M., Castro, S.A. (Eds.), Biological Invasions in the South American Anthropocene: Global Causes and Local Impacts. Springer International Publishing, Cham, pp. 19-47. doi: https://doi.org/10.1007/978-3-030-56379-0_2

Lombaert, E., Guillemaud, T., Lundgren, J., Koch, R., Facon, B., Grez, A., Loomans, A., Malausa, T., Nedved, O., Rhule, E., Staverlokk, A., Steenberg, T. and Estoup, A. (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: The case of the Asian ladybird Harmonia axyridis. Molecular Ecology, 23, 5979-5997. doi: https://doi.org/10.1111/mec.12989

Mack, R.N., Simberloff, D., Lonsdale, M.W., Evans, H., Clout, M., Bazzaz, F.A. (2000) Biotic Invasions : Causes , Epidemiology , Global Consequences , and Control. Ecological Applications, 10, 689-710. doi: https://doi.org/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2

Mallez, S., Castagnone, C., Lombaert, E., Castagnone-Sereno, P. and Guillemaud, T. (2021) Inference of the worldwide invasion routes of the pinewood nematode Bursaphelenchus xylophilus using approximate Bayesian computation analysis. bioRxiv, 452326, ver. 6 peer-reviewed and recommended by Peer community in Zoology. doi: https://doi.org/10.1101/452326

Ticks are notorious vectors of diseases in humans and other vertebrates. Much effort has been expended to understand tick diversity and ecology with the aim of managing their populations to alleviate the misery they bring. Further, the fundamental question of whether ticks are usually host generalists or host specialists has been debated at length and is important both for understanding the mechanisms of their diversification as well as for focusing control of ticks [1].

One elegant resolution of this question is to consider most tick species to be global generalists but local specialists [1]. This is well illustrated in a series of studies of the seabird tick, Ixodes uriae, which is comprised of host-specific races that show genetic [2], morphological [3] and host performance [4] differences associated with the seabirds they feed on. Such a pattern has clear ramifications for sympatric speciation; however, the factors that potentially act to drive these differences have remained elusive.

Dupraz et al. [5] have now made intriguing and important steps toward bridging the gap between demonstrating local patterns of tick host association and understanding the physiological mechanisms that may facilitate such divergences. They collected I. uriae ticks from the nests of two seabirds – Atlantic puffins and common guillemots – on the north side of Iceland. Four populations of ticks were sampled, with one island providing both puffin ticks and guillemot ticks, to give two tick populations from each of the two seabird host species. They then washed the ticks in solvent and analyzed the dissolved cuticular hydrocarbons (CHCs) using GC mass spectrometry, revealing 22 different hydrocarbon compounds common to most of these samples. CHCs are known to be important across arthropods for a variety of functions ranging from reducing water loss to facilitating communication and recognition between individuals with species.

Dupraz et al. [5] found three hydrocarbons that distinguished puffin ticks most consistently from guillemot ticks. A cross-validation test for host type also assigned 75% of the tick pools to the seabird host of origin. However, with these limited sample sizes, statistical analysis revealed no significant difference in CHC profiles between the host types, although a tendency was evident. Nonetheless, this study revealed a number of potentially diagnostic CHCs for tick host type, as well as some that may be more diagnostic of locations. This provides a fascinating and actionable foundation for further work using additional sites and host types, as well as an entry point into discerning the mechanisms at play in producing the diversity, complexity and adaptability that make ticks such medical menaces.

References

[1]  McCoy, K.D., Léger, E., Dietrich, M., 2013. Host specialization in ticks and transmission of tick-borne diseases: a review. Front. Cell. Infect. Microbiol. 3. https://doi.org/10.3389/fcimb.2013.00057

[2]  McCoy, K.D., Chapuis, E., Tirard, C., Boulinier, T., Michalakis, Y., Bohec, C.L., Maho, Y.L., Gauthier-Clerc, M., 2005. Recurrent evolution of host-specialized races in a globally distributed parasite. Proc. R. Soc. B Biol. Sci. 272, 2389–2395. https://doi.org/10.1098/rspb.2005.3230

[3]  Dietrich, M., Beati, L., Elguero, E., Boulinier, T., McCoy, K.D., 2013. Body size and shape evolution in host races of the tick Ixodes uriae. Biol. J. Linn. Soc. 108, 323–334. https://doi.org/10.1111/j.1095-8312.2012.02021.x

[4]  Dietrich, M., Lobato, E., Boulinier, T., McCoy, K.D., 2014. An experimental test of host specialization in a ubiquitous polar ectoparasite: a role for adaptation? J. Anim. Ecol. 83, 576–587. https://doi.org/10.1111/1365-2656.12170

[5] Dupraz, M., Leroy, C., Thórarinsson, T. L., d’Ettorre, P. and McCoy, K. D. (2022) Within and among population differences in cuticular hydrocarbons in the seabird tick Ixodes uriae. bioRxiv, 2022.01.21.477272, ver. 5 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2022.01.21.477272

Insects exhibit a great diversity of life-history traits that often vary not only between species but also between populations of the same species (Flatt and Heyland, 2011). A better understanding of the variation in these traits can be of paramount importance when it comes to species of economic and agricultural interest (Wilby and Thomas, 2002). In particular, the control of the development and expansion of agricultural pests generally requires a good understanding of the parameters that favour the reproduction of these pests and/or the reproduction of the species used to control them (Bianchi et al., 2013; Gäde and Goldsworthy, 2003).

Parasitoid wasps of the genus Trichogramma are a classic example of insects involved in pest control (Smith, 1996). This genus comprises over 200 species worldwide, which have been used to control populations of a wide range of lepidopteran pests since the 1900s (Flanders, 1930; Hassan, 1993). Despite its common use, the egg-laying preference of this genus is only partially known. For example, all Trichogramma species are often thought to have positive phototaxis (or negative geotaxis) (e.g. Brower & Cline, 1984; van Atta et al., 2015), but comprehensive studies simultaneously testing this (or other) parameter among Trichogramma species and populations remain rare.

This is exactly the aim of the present study (Burte et al., 2021). Using a new experimental approach based on automatic image analysis, the authors compared the photo- and geo-tactic oviposition preference among 5 Trichogramma species from 25 populations. Their results first confirm that most Trichogramma species and populations prefer light to shade, and higher to lower positions for oviposition. Interestingly, they also reveal that the levels of preference for light and gravity show inter- and intraspecific variation (probably due to local adaptation to different strata) and that both preferences tend to relax over time.

Overall, this study provides important information for improving the use of Trichogramma species as biological agents. For example, it may help to establish breeding lines adapted to the microhabitat and/or growing parts of plants on which agricultural pests lay eggs most. Similarly, it suggests that the use of multiple strains with different microhabitat selection preferences could lead to better coverage of host plants, as well as a reduction in intraspecific competition in the preferred parts. Finally, this study provides a new methodology to efficiently and automatically study oviposition preferences in Trichogramma, which could be used in other insects with a particularly small size.

References

Bianchi, F. J. J. A., Schellhorn, N. A. and Cunningham, S. A. (2013). Habitat functionality for the ecosystem service of pest control: reproduction and feeding sites of pests and natural enemies. Agricultural and Forest Entomology, 15, 12–23. https://doi.org/10.1111/j.1461-9563.2012.00586.x

Burte V., Perez G., Ayed F., Groussier G., Mailleret L, van Oudenhove L. and Calcagno V. (2021). Up and to the light: intra- and interspecific variability of photo-and geo-tactic oviposition preferences in genus Trichogramma. bioRxiv, 2021.03.30.437671, ver. 4 peer-reviewed and recommended by PCI Zoology. https://doi.org/10.1101/2021.03.30.437671

Brower, J. H. and Cline, L. D. (1984). Response of Trichogramma pretiosum and T. evanescens to Whitelight, Blacklight or NoLight Suction Traps. The Florida Entomologist, 67, 262–268. https://doi.org/10.2307/3493947

Flanders, S. E. (1930). Mass production of egg parasites of the genus Trichogramma. Hilgardia, 4, 465–501. https://doi.org/10.3733/hilg.v04n16p465

Flatt, T. and Heyland, A. (2011). Mechanisms of life history evolution: the genetics and physiology of life history traits and trade-offs. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199568765.001.0001

Gäde, G. and Goldsworthy, G. J. (2003). Insect peptide hormones: a selective review of their physiology and potential application for pest control. Pest Management Science, 59, 1063–1075. https://doi.org/10.1002/ps.755

Hassan, S. A. (1993). The mass rearing and utilization of Trichogramma to control lepidopterous pests: Achievements and outlook. Pesticide Science, 37, 387–391. https://doi.org/10.1002/ps.2780370412

Smith, S. M. (1996). Biological Control with Trichogramma : Advances, Successes, and Potential of Their Use. Annual Review of Entomology, 41, 375–406. https://doi.org/10.1146/annurev.en.41.010196.002111

van Atta, K. J., Potter, K. A. and Woods, H. A. (2015). Effects of UV-B on Environmental Preference and Egg Parasitization by Trichogramma Wasps (Hymenoptera: Trichogrammatidae). Journal of Entomological Science, 50, 318–325. https://doi.org/10.18474/JES15-09.1

Wilby, A. and Thomas, M. B. (2002). Natural enemy diversity and pest control: patterns of pest emergence with agricultural intensification. Ecology Letters, 5, 353–360. https://doi.org/10.1046/j.1461-0248.2002.00331.x

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