Alternative parasite development in transmission strategies: how time flies!
Among parasitic platyhelminths with complex life cycles, it has been well documented that transmission opportunities are the main forces shaping the diversity of life-history traits and parasite developmental strategies. While deviations in the development pathway usually involve shortening of life cycles, their extension may also occur following perception of remaining time by parasites. Polystoma gallieni, the monogenean parasite of Hyla meridionalis, is able to trigger two alternative developmental strategies depending on the physiological stage of the tadpoles upon which larvae attach. The distribution and reproductive outputs of both resulting phenotypes were surveyed to address questions about the dynamics of transmission in natural environments. Because modifications in the completion of life cycles can have drawbacks which may perturb the dynamic equilibrium of the resulting host-parasite systems, experimental infestations were also performed to assess parasite-parasite interactions. Our results suggest that the bladder adult phenotype, which involves transmission between frogs and tadpoles, is supplied secondarily by the branchial phenotype which involves transmission between tadpoles and metamorphs. They also support the occurrence of finely tuned trade-offs between hosts and parasites and highlight positive trends behind the extension of direct life cycles, in which host-derived signals account for the remaining time to achieve parasitic transmission.
Badets
M
M
UMR 5244 CNRS-UPVD, Biologie et Ecologie Tropicale et Méditerranéenne, Parasitologie Fonctionnelle et Evolutive, Université de Perpignan Via Domitia, Perpignan Cedex, France.
Morrison
C
C
Environment Futures Centre, School of Environment, Griffith University Gold Coast, QLD, Australia.|School of Earth and Environmental Sciences, University of Wollongong, Wollongong NSW, Australia.
Verneau
O
O
UMR 5244 CNRS-UPVD, Biologie et Ecologie Tropicale et Méditerranéenne, Parasitologie Fonctionnelle et Evolutive, Université de Perpignan Via Domitia, Perpignan Cedex, France.
D000818:Animals; D001001:Anura / Q000469:parasitology*; D001934:Branchial Region / Q000469:parasitology; D005260:Female; D005602:France / Q000453:epidemiology; D006374:Helminthiasis, Animal / Q000453:epidemiology / Q000635:transmission*; D006790:Host-Parasite Interactions; D007814:Larva / Q000469:parasitology; D008297:Male; D052287:Oviparity; D010641:Phenotype; D010986:Platyhelminths / Q000254:growth & development*; D011157:Population Dynamics; D001743:Urinary Bladder / Q000469:parasitology
Alberch, P. & Blanco, M.J. 1996. Evolutionary patterns in ontogenetic transformation: from laws to regularities. Int. J. Dev. Biol. 40: 845-858.
Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. 2009. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22: 245-259.
Badets, M. & Verneau, O. 2009. Origin and evolution of alternative developmental strategies in amphibious sarcopterygian parasites (Platyhelminthes, Monogenea, Polystomatidae). Org. Divers. Evol. 9: 155-164.
Badets, M., Boissier, J., Brémond, P. & Verneau, O. 2009. Polystoma gallieni: experimental evidence for chemical cues for developmental plasticity. Exp. Parasitol. 121: 163-166.
Benesh, D.P. 2010. Developmental inflexibility of larval tapeworms in response to resource variation. Int. J. Parasitol. 40: 487-497.
Combes, C. 1967. Recherches sur les formes néoténiques de Polystomatidae (Monogenea). Présence d’une forme néoténique chez Polystoma gallieni Price, 1938. Bull. Soc. Neuch. Sci. Nat. 90: 205-214.
Combes, C. 1968. Biologie, écologie des cycles et biogéographie de digènes et monogènes d’amphibiens dans l’est des Pyrénées. Mém. Mus. Natl. Hist. Nat., Sér. A Zool. 1: 1-195.
Combes, C. 1995. Interactions Durables - Ecologie et évolution du Parasitisme. Masson, Paris.
Combes, C. 2001. L’art d’être Parasite. Flammarion, Paris.
Cribb, T.H., Chisholm, L.A. & Bray, R.A. 2002. Diversity in Monogenea and Digenea: does lifestyle matter? Int. J. Parasitol. 32: 321-328.
Cribb, T.H., Bray, R.A., Olson, P.D. & Littlewood, D.T.J. 2003. Life cycle evolution in the digenean: a new perspective from phylogeny. Adv. Parasitol. 54: 197-254.
Debat, V. & David, P. 2001. Mapping phenotypes: canalization, plasticity and developmental stability. Trend Ecol. Evol. 16: 555-561.
Gallien, L. 1935. Recherches expérimentales sur le dimorphisme évolutif et la biologie de Polystoma integerrimum Fröhlich. Trav. Stat. Zool. Wimereux. 12: 1-181.
Haddad, C.F.B. & Prado, C.P.A. 2005. Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. Bioscience 55: 207-217.
IUCN. 2010. The IUCN Redlist of Endangered Species 2010. Available at: http://www.iucnredlist.org. Accessed May, 26 2010.
Jackson, J.A. & Tinsley, R.C. 2003. Density dependence of postlarval survivorship in primary infections of Protopolystoma xenopodis. J. Parasitol. 89: 958-960.
Kearn, G.C. 1994. Evolutionary expansion of the Monogenea. Int. J. Parasitol. 24: 1227-1271.
Koella, J.C., Agnew, P. & Michalakis, Y. 1998. Coevolutionary interactions between host life histories and parasite life cycles. Parasitology 116: S47-S55.
Kok, D.J. 1990. Polystoma umthakathi (Monogenea): establishment, mortality and reproduction of neotenic parasites in experimentally infected Natalobatrachus bonebergi tadpoles. S. Afr. J. Zool. 25: 26-30.
Kok, D.J. & Du Preez, L.H. 1989. Polystoma australis (Monogenea): development and reproduction in neotenic parasites. S. Afr. J. Zool. 24: 225-230.
Kok, D.J. & Du Preez, L.H. 1998. The relative importance of bladder versus neotenic stages of Polystoma marmorati and P. umthakathi in natural frog populations in South Africa. J. Helminthol. 72: 117-121.
Lagrue, C. & Poulin, R. 2007. Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? J. Evol. Biol. 20: 1189-1195.
Lagrue, C. & Poulin, R. 2009. Life cycle abbreviation in trematode parasites and the developmental time hypothesis: is the clock ticking? J. Evol. Biol. 22: 1727-1738.
Lefebvre, F. & Poulin, R. 2005a. Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes. J. Helminthol. 79: 47-53.
Lefebvre, F. & Poulin, R. 2005b. Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate host. Parasitology 130: 587-605.
Maeder, A.-M. 1973. Monogènes et Trématodes parasites d’Amphibiens en Côte d’Ivoire. Rev. Suisse Zool. 80: 267-322.
Michaud, M., Milinski, M., Parker, G.A. & Chubb, J.C. 2006. Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evol. Ecol. 20: 39-57.
Murith, D. 1979. Identité des larves de polystomes (Monogenea) parasites du têtard de Dicroglossus occipitalis (Günther) en Côte-d’Ivoire. Z. Parasitenkd. 59: 187-194.
Murith, D. 1981. Examples of the close relationship between the mode of transmission of some parasites and the niche of the host amphibian. Ital. J. Zool. 15: 359-365.
Murith, D., Vaucher, C. & Combes, C. 1977. Coexistence de la néoténie et du cycle interne chez un Polystomatidae (Monogenea). C. R. Acad. Sci. Gen., Paris 284: 187-190.
Murith, D., Miremad-Gassmann, M. & Vaucher, C. 1978. Contribution à l’étude des polystomes d’amphibiens du Cameroun. Rev. Suisse Zool. 85: 681-698.
Parker, G.A., Chubb, J.C., Ball, M.A. & Roberts, G.N. 2003. Evolution of complex life cycles in helminth parasites. Nature 425: 480-484.
Piersma, T. & Drent, J. 2003. Phenotypic flexiibility and the evolution of organismal design. Trends Ecol. Evol. 18: 228-233.
Pigliucci, M. 2005. Evolution of phenotypic plasticity: where are we going now? Trends Ecol. Evol. 20: 481-486.
Poulin, R. 1996. The evolution of life history strategies in parasitic animals. Adv. Parasitol. 37: 107-134.
Poulin, R. & Cribb, T.H. 2002. Trematode life cycles: short is sweet? Trends Parasitol. 18: 176-183.
Poulin, R. & Lefebvre, F. 2006. Alternative life-history and transmission strategies in a parasite: first come, first served? Parasitology 132: 135-141.
Rohde, K. 1994. The origins of parasitism in the Platyhelminthes. Int. J. Parasitol. 24: 1099-1115.
Thomas, F., Brown, S.P., Sukhdeo, M. & Renaud, F. 2002. Understanding parasite strategies: a state-dependent approach? Trends Parasitol. 18: 387-391.
Tinsley, R.C. 1990. Host behaviour and opportunism in parasites life cycles. In: Parasitism and Host Behaviour (C.J. Barnard & J.M. Behnke, eds), pp. 158-192. Taylor & Francis, London, UK.
Tinsley, R.C. 1993. The population biology of polystomatid monogeneans. Bull. Fr. Pêche Piscic. 328: 120-136.
Tinsley, R.C. 1999. Parasite adaptations to extreme conditions in a desert environment. Parasitology 119: 31-56.
Tinsley, R.C. 2004. Platyhelminth parasite reproduction: some general principles derived from monogenans. Can. J. Zool. 82: 270-291.
Tinsley, R.C. & Jackson, J.A. 2002. Host factors limiting monogenean infections: a case study. Int. J. Parasitol. 32: 353-365.
Verneau, O. 2004. Origine et évolution des monogènes Polystomatidae, parasites d’amphibiens et de chéloniens d’eau douce. HDR Thesis, Perpignan.
Verneau, O., Bentz, S., Sinnappah, N.D., Du Preez, L., Whittington, I. & Combes, C. 2002. A view of early vertebrate evolution inferred from the phylogeny of polystome parasites (Monogenea : Polystomatidae). Proc. R. Soc. Lond. B Biol. Sci. 269: 535-543.
Via, S., Gomulkiewicz, R., De Jong, G., Scheiner, S.M., Schlichting, C.D. & Van Tienderen, P.H. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10: 212-217.
West-Eberhard, M.J. 1989. Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20: 249-278.
Whittington, I.D. 1997. Reproduction and host-location among the parasitic Platyhelminthes. Int. J. Parasitol. 27: 705-714.
Williams, J.B. 1961. The dimorphism of Polystoma integerrimum (Frölich) Rudolphi and its bearing on relationships within the Polystomatidae: Part III. J. Helminthol. 35: 181-202.