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Stage-dependent behavioural changes but early castration induced by the acanthocephalan parasite Polymorphus minutus in its Gammarus pulex intermediate host


Multidimensionality in parasite-induced phenotypic alterations (PIPA) has been observed in a large number of host–parasite associations, particularly in parasites with complex life cycles. However, it is still unclear whether such a syndrome is due to the successive activation of independent PIPAs, or results from the synchronous disruption of a single mechanism. The aim of the present study was to investigate the onset and progression of two PIPAs (a behavioural alteration: reversion of geotaxis, and castration) occurring in the crustacean amphipod Gammarus pulex infected with the acanthocephalan Polymorphus minutus, at different parasite developmental stages. Modifications of geotaxis in hosts differed according to the parasite developmental stage. Whereas the cystacanth stage induced a negative geotaxis (exposing the gammarid to predation by birds, the definitive hosts), the acanthella stage, not yet infective for the definitive host, induced a stronger positive geotaxis (presumably protecting gammarids from bird predation). In contrast, castration was almost total at the acanthella stage, with no significant variation in the intensity according to parasite maturation. Finally, no significant correlation was found between the intensity of behavioural changes and the intensity of castration. We discuss our results in relation with current views on the evolution of multidimensionality in PIPA.

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*Corresponding author: Laboratoire Biogéosciences, Université Bourgogne Franche-Comté, UMR CNRS 6282, Equipe Ecologie Evolutive, 6 boulevard Gabriel, 21000 Dijon, France. E-mail:
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Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution 29, 335352.
Bauer, A., Haine, E. R., Perrot-Minnot, M.-J. and Rigaud, T. (2005). The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli . Journal of Zoology 267, 3943.
Bethel, W. M. and Holmes, J. C. (1973). Altered evasive behavior and response to light in amphipods harboring acanthocephalan cyctacanths. Journal of Parasitology 59, 945956.
Bethel, W. M. and Holmes, J. C. (1974). Correlation of development of altered evasive behavior in Gammarus lactustris (Amphipoda) harboring cystacanths of Polymorphus paradoxus (Acanthocephala) with the infectivity to the definitive host. Journal of Parasitology 60, 272274.
Bierbower, S. M. and Sparkes, T. C. (2007). Parasite-related pairing success in an intermediate host, Caecidotea intermedius (Isopoda): effects of male behavior and reproductive physiology. Journal of Parasitology 93, 445449.
Bollache, L., Gambade, G. and Cézilly, F. (2001). The effects of two acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on pairing success in male Gammarus pulex (Crustacea: Amphipoda). Behavioral Ecology and Sociobiology 49, 296303.
Bollache, L., Rigaud, T. and Cézilly, F. (2002). Effects of two acanthocephalan parasites on the fecundity and pairing status of female Gammarus pulex (Crustacea: Amphipoda). Journal of Invertebrate Pathology 79, 102110.
Brown-Peterson, N. J., Manning, C. S., Denslow, N. D. and Brouwer, M. (2011). Impacts of cyclic hypoxia on reproductive and gene expression patterns in the grass shrimp: field versus laboratory comparison. Aquatic Sciences 73, 127141.
Byers, J. (2013). Modeling and regression analysis of semiochemical dose-response curves of insect antennal reception and behavior. Journal of Chemical Ecology 39, 10811089.
Carmichael, L. M., Moore, J. and Louis, B. and Bjostad, L. B. (1993). Parasitism and decreased response to sex pheromones in male Periplaneta Americana (Dictyoptera: Blattidae). Journal of Insect Behavior 6, 2532.
Cézilly, F. and Perrot-Minnot, M.-J. (2010). Interpreting multidimensionality in parasite-induced phenotypic alterations: panselectionism versus parsimony. Oikos 119, 12241229.
Cézilly, F., Grégoire, A. and Bertin, A. (2000). Conflict between co-occurring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex . Parasitology 120, 625630.
Cézilly, F., Thomas, F., Médoc, V. and Perrot-Minnot, M.-J. (2010). Host-manipulation by parasites with complex life cycles: adaptive or not? Trends in Parasitology 26, 311317.
Cézilly, F., Favrat, A. and Perrot-Minnot, M.-J. (2013). Multidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects. Journal of Experimental Biology 216, 2735.
Conlan, K. E. (1991). Precopulatory mating-behaviour and sexual dimorphism in the amphipod Crustacea. Hydrobiologia 223, 255282.
Cothran, R. D. and Jeyasingh, P. D. (2010). Condition dependence of a sexually selected trait in a crustacean species complex: importance of the ecological context. Evolution 64, 25352546.
Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Elsa, L. and 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, 26922698.
Franceschi, N., Bauer, A., Bollache, L. and Rigaud, T. (2008). The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. International Journal for Parasitology 38, 11611170.
Gopko, M., Mikheev, V. N. and Taskinen, J. (2015). Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis. Behavioral Ecology and Sociobiology 69, 17231730.
Hall, S. R., Becker, C. and Cáceres, C. E. (2007). Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47, 295309.
Hammerschmidt, K., Koch, K., Milinski, M., Chubb, J. C. and Parker, G. A. (2009). When to go: optimization of host switching in parasites with complex life cycles. Evolution 63, 19761986.
Hindsbo, O. (1972). Effects of Polymorphus (Acanthocephala) on colour and behaviour of Gammarus lacustris . Nature 238, 333.
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363368.
Hurd, H. (2009). Evolutionary drivers of parasite-induced changes in insect life-history traits: from theory to underlying mechanisms. Advances in Parasitology 68, 85110.
Jacquin, L., Mori, Q., Pause, M., Steffen, M. and Médoc, V. (2014). Non-specific manipulation of gammarid behaviour by P. minutus parasite enhances their predation by definitive bird hosts. Plos ONE 9, e101684.
Jensen, K. H., Little, T., Skorping, A. and Ebert, D. (2006). Empirical support for optimal virulence in a castrating parasite. Plos Biology 4, e197.
Kennedy, C. R. (2006). Ecology of the Acanthocephala. Cambridge University Press, Cambridge, UK.
Lafferty, K. D. and Kuris, A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564572.
Lai, K. P., Li, J. W., Chan, C. Y. S, Chan, T. F., Yuen, K. W. Y. and Chiu, J. M. Y. (2016). Transcriptomic alterations in Daphnia magna embryos from mothers exposed to hypoxia. Aquatic Toxicology 177, 454463.
Lau, C. E., Sun, L., Wang, K., Simpao, A. and Falk, J. L. (2000). Oral cocaine pharmacokinetics and pharmacodynamics in a cumulative-dose regimen: pharmacokinetic-pharmacodynamic modeling of concurrent operant and spontaneous behavior within an operant context. Journal of Pharmacology and Experimental Therapeutics 295, 634643.
Lemaître, J. -F., Rigaud, T., Cornet, S. and Bollache, L. (2009). Sperm depletion, male mating behaviour and reproductive ‘time-out’ in Gammarus pulex (Crustacea, Amphipoda). Animal Behaviour 77, 4954.
Levri, E. D. (1998). The influence of non-host predators on parasite-induced behavioral changes in a freshwater snail. Oikos 81, 531537.
Li, T. and Brouwer, M. (2013). Field study of cyclic hypoxic effects on gene expression in grass shrimp hepatopancreas. Comparative Biochemistry and Physiology, Part D 8, 309316.
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, Oxford.
Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K. and Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution 63, 448458.
Perrot-Minnot, M.-J., Madaleno, M., Balourdet, A. and Cézilly, F. (2012). Host manipulation revisited: no evidence for a causal link between altered photophobia and increased trophic transmission of amphipods infected with acanthocephalans. Functional Ecology 26, 10071014.
Perrot-Minnot, M.-J., Maddaleno, M. and Cézilly, F. (2016). Parasite-induced inversion of geotaxis in a freshwater amphipod: a role for anaerobic metabolism? Functional Ecology 30, 780788.
Poulin, R. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. In Advances in the Study of Behavior, Vol. 41 (ed. Brockmann, H. J., Roper, T. J., Naguib, M., WynneEdwards, K. E., Mitani, J. C. and Simmons, L. W.), pp. 151186. Academic Press, Burlington.
Rabhi, K. K., Esancy, K., Voisin, A., Crespin, L., Le Corre, J., Tricoire-Leignel, H., Anton, S. and Gadenne, C. (2014). Unexpected effects of low doses of a neonicotinoid insecticide on behavioral responses to sex pheromone in a pest insect. PLoS ONE 9, e114411.
Rauque, C. A. and Semenas, L. (2009). Effects of two acanthocephalan species on the reproduction of Hyalella patagonica (Amphipoda, Hyalellidae) in an Andean Patagonian Lake (Argentina). Journal of Invertebrate Pathology 100, 3539.
Sparkes, T. C., Weil, K. A., Renwick, D. T. and Talkington, J. A. (2006). Development-related effects of an acanthocephalan parasite on pairing success of its intermediate host. Animal Behaviour 71, 439448.
Sutcliffe, D. W. (1992). Reproduction in Gammarus (Crustacea, Amphipoda): basic processes. Freshwater Forum 2, 102128.
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185199.
Thomas, F., Poulin, R. and Brodeur, J. (2010). Host manipulation by parasites: a multidimensional phenomenon. Oikos 119, 12171223.
Weinreich, F., Benesh, D. P. and Milinski, M. (2013). Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective. Parasitology 140, 129135.
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