title: Co-variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan-amphipod system.
abstract: Pomphorhynchus laevis, a fish acanthocephalan parasite, manipulates the behaviour of its gammarid intermediate host to increase its trophic transmission to the definitive host. However, the intensity of behavioural manipulation is variable between individual gammarids and between parasite populations. To elucidate causes of this variability, we compared the level of phototaxis alteration induced by different parasite sibships from one population, using experimental infections of Gammarus pulex by P. laevis. We used a naive gammarid population, and we carried out our experiments in two steps, during spring and winter. Moreover, we also investigated co-variation between phototaxis (at different stages of infection, 'young' and 'old cystacanth stage') and two other fitness-related traits, infectivity and development time. Three main parameters could explain the parasite intra-population variation in behavioural manipulation. The genetic variation, suggested by the differences between parasite families, was lower than the variation owing to an (unidentified) environmental factor. Moreover, a correlation was found between development rate and the intensity of behavioural change, the fastest growing parasites being unable to induce rapid phototaxis reversal. This suggests that parasites cannot optimize at the same time these two important parameters of their fitness, and this could explain a part of the variation observed in the wild.
authors.affiliation: Laboratoire Biogéosciences, UMR CNRS 5561, Equipe Ecologie Evolutive, Université de Bourgogne, Dijon, France.
authors.forename: N
authors.initials: N
authors.lastname: Franceschi
authors.affiliation: Laboratoire Biogéosciences, UMR CNRS 5561, Equipe Ecologie Evolutive, Université de Bourgogne, Dijon, France.
authors.forename: L
authors.initials: L
authors.lastname: Bollache
authors.forename: S
authors.initials: S
authors.lastname: Cornet
authors.affiliation: Laboratoire Biogéosciences, UMR CNRS 5561, Equipe Ecologie Evolutive, Université de Bourgogne, Dijon, France.
authors.forename: A
authors.initials: A
authors.lastname: Bauer
authors.affiliation: Laboratoire Biogéosciences, UMR CNRS 5561, Equipe Ecologie Evolutive, Université de Bourgogne, Dijon, France.
authors.forename: S
authors.initials: S
authors.lastname: Motreuil
authors.affiliation: Laboratoire Biogéosciences, UMR CNRS 5561, Equipe Ecologie Evolutive, Université de Bourgogne, Dijon, France.
authors.forename: T
authors.initials: T
authors.lastname: Rigaud
mesh_terms: D000049:Acanthocephala / Q000235:genetics / Q000254:growth & development* / Q000472:pathogenicity; D033304:Amphipoda / Q000469:parasitology*; D000818:Animals; D001522:Behavior, Animal; D005260:Female; D014644:Genetic Variation; D006790:Host-Parasite Interactions; D008297:Male
references.citation: Bauer, A., Trouvé, S., Grégoire, A., Bollache, L. & Cézilly, F. 2000. Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. Int. J. Parasitol. 30: 1453-1457.
references.citation: Benesh, D.P. 2010. What are the evolutionary constraints on larval growth in a trophically transmitted parasite? Oecologia 162: 599-608.
references.citation: Bethel, W.M. & Holmes, J.C. 1973. Altered evasive behaviour and response to light in amphipods harbouring acanthocephalan cystacanths. J. Parasitol. 59: 945-956.
references.citation: Blanford, S., Thomas, M.B., Pugh, C. & Pell, J.K. 2003. Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecol. Lett. 6: 2-5.
references.citation: Carius, H.J., Little, T.J. & Ebert, D. 2001. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55: 1136-1145.
references.citation: Cornet, S., Franceschi, N., Bollache, L., Rigaud, T. & Sorci, G. 2009. Variation and covariation in infectivity, virulence and immunodepression in the host-parasite association Gammarus pulex-Pomphorhynchus laevis. Proc. R. Soc. B 276: 4229-4236.
references.citation: Crompton, D.W.T. & Nickol, B.B. 1985. Biology of the Acanthocephala. Cambridge University Press, Cambridge.
references.citation: Davies, C.M., Webster, J.P. & Woolhouse, M.E.J. 2001. Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proc. R. Soc. Lond. B 268: 251-257.
references.citation: Dezfuli, B.S., Capuano, S., Pironi, F. & Mischiati, C. 1999. The origin and function of cement gland secretion in Pomphorhynchus laevis (Acanthocephala). Parasitology 119: 649-653.
references.citation: Ebert, D., Zschokke-Rohringer, C.D. & Carius, H.J. 2000. Dose effects and density dependent regulation of two microparasites of Daphnia magna. Oecologia 122: 200-209.
references.citation: Fels, D. 2005. The effect of food on microparasite transmission in the waterflea Daphnia magna. Oikos 109: 360-366.
references.citation: Fels, D. & Kaltz, O. 2006. Temperature-dependent transmission and latency of Holospora undalata, a micronucleus-specific parasite of the ciliate Paramecium caudatum. Proc. R. Soc. B 273: 1031-1038.
references.citation: Franceschi, N., Rigaud, T., Moret, Y., Hervant, F. & Bollache, L. 2007. Behavioural and physiological effects of the trophically transmitted cestode parasite, Cyathocephalus truncatus, on its intermediate host, Gammarus pulex. Parasitology 134: 1839-1847.
references.citation: Franceschi, N., Bauer, A., Bollache, L. & Rigaud, T. 2008. The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. Int. J. Parasitol. 38: 1161-1170.
references.citation: Franceschi, N., Cornet, S., Bollache, L., Dechaume-Moncharmont, F.X., Bauer, A., Motreuil, S. & Rigaud, T. 2010. Variation between populations and local adaptation in an acanthocephalan-induced parasite manipulation. Evolution 64: 2417-2430.
references.citation: Gandon, S. 2004. Evolution of multihost parasites. Evolution 58: 455-469.
references.citation: Hammerschmidt, K. & Kurtz, J. 2005. Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle. Proc. R. Soc. Lond. B 272: 2511-2518.
references.citation: Hammerschmidt, K., Koch, K., Milinski, M., Chubb, J.C. & Parker, G.A. 2009. When to go: optimization of host switching in parasites with complex life cycles. Evolution 63: 1976-1986.
references.citation: Incani, R.N., Morales, G. & Cesari, I.M. 2001. Parasite and vertebrate host genetic heterogeneity determine the outcome of infection by Schistosoma mansoni. Parasitol. Res. 87: 131-137.
references.citation: Jokela, J., Taskinen, J., Mutikainen, P. & Kopp, K. 2005. Virulence of parasites in hosts under environmental stress: experiments with anoxia and starvation. Oikos 108: 156-164.
references.citation: Kaldonski, N., Perrot-Minnot, M.J. & Cézilly, F. 2007. Differential influence of two acanthocephalan parasites on the antipredator behaviour of their common intermediate host. Anim. Behav. 74: 1311-1317.
references.citation: Kaltz, O. & Shykoff J, A. 2002. Within- and among population variation in infectivity, latency and spore production in a host-pathogen system. J. Evol. Biol. 15: 850-860.
references.citation: Kennedy, C.R. 2006. Ecology of the Acanthocephala. Cambridge University Press, Cambridge.
references.citation: Kraaijeveld, A.R., Van Alphen, J.J.M. & Godfray, H.C.J. 1998. The coevolution of host resistance and parasitoid virulence. Parasitology 116: S29-S45.
references.citation: Lafferty, K.D. 1999. The evolution of trophic transmission. Parasitol. Today 15: 111-115.
references.citation: Lagrue, C., Kaldonski, N., Perrot-Minnot, M.J., Motreuil, S. & Bollache, L. 2007. Modification of hosts’ behaviour by a parasite: field evidence for adaptive manipulation. Ecology 88: 2839-2847.
references.citation: Leung, T.L.F., Keeney, D.B. & Poulin, R. 2010. Genetics, intensity-dependence and host manipulation in the trematode Curtuteria australis: following the strategies of others? Oikos 119: 393-400.
references.citation: Lively, C.M. 1989. Adaptation by a parasitic trematode to local-populations of its snail host. Evolution 43: 1663-1671.
references.citation: Lucas, M.C. & Batley, E. 1996. Seasonal movements and behaviour of adult barbel Barbus barbus, a riverine cyprinid fish: implications for river management. J. Appl. Ecol. 33: 1345-1358.
references.citation: Mitchell, S.E., Rogers, E.S., Little, T.J. & Read, A.F. 2005. Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59: 70-80.
references.citation: Moore, J. 2002. Parasites and the behaviour of animals. Oxford University Press, Oxford.
references.citation: Penttinen, O.P. & Holopainen, I.J. 1992. Seasonal feeding-activity and ontogenic dietary shifts in crucian carp, Carassius carassius. Environ. Biol. Fishes 33: 215-221.
references.citation: Perrot-Minnot, M.J. 2004. Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). Int. J. Parasitol. 34: 45-54.
references.citation: Poulin, R. 1994. The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109: S109-S118.
references.citation: Poulin, R. 2006. Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. Int. J. Parasitol. 36: 877-885.
references.citation: Poulin, R., Curtis, M.A. & Rau, M.E. 1992. Effects of Eubothrium salvelini (Cestoda) on the behaviour of Cyclops vernalis (Copepoda) and its susceptibility to fish predators. Parasitology 105: 265-271.
references.citation: Roff, D.A. 1997. Evolutionary quantitative genetics. Chapman & Hall, New York.
references.citation: De Roode, J.C., Gold, L.R. & Altizer, S. 2007. Virulence determinants in a natural butterfly-parasite system. Parasitology 134: 657-668.
references.citation: Stearns, S.C. 1992. The evolution of life histories. Oxford University Press, Oxford.
references.citation: Tain, L., Perrot-Minnot, M.J. & Cezilly, F. 2006. Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proc. R. Soc B 273: 3039-3045.
references.citation: Thomas, F. & Poulin, R. 1998. Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116: 431-436.
references.citation: Thomas, F., Adamo, S. & Moore, J. 2005. Parasitic manipulation: where are we and where should we go? Behav. Processes 68: 185-199.
references.citation: Webster, J.P. 2005. Parasitic manipulation: where else should we go? Behav. Processes 68: 275-277.