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Multi-clone infections and the impact of intraspecific competition on trematode colonies with a division of labour

Published online by Cambridge University Press:  22 October 2013

MELANIE M. LLOYD*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
ROBERT POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
*Corresponding author: Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand. E-mail: [email protected]

Summary

A division of labour occurs in colonies of the trematode Philophthalmus sp. within their first intermediate hosts. Two castes exist: one which reproduces and one which does not reproduce. It has been hypothesized that the benefit of the non-reproductive caste is in competitive interactions. Evidence for this from past experiments with Philophthalmus sp. colonies has been contradictory: the non-reproductive caste appears to benefit the colony in some way but not necessarily by combating interspecific competitors. The aims of this study were to consider intraspecific competition as a possible cause of the division of labour in Philophthalmus sp. colonies. Results show that mixed genotype infections occur in Philophthalmus sp. infected hosts and thus intraspecific competition is likely. Furthermore, the total number of individuals per colony is reduced in mixed genotype infections, indicating that intraspecific competition reduces colony fitness. However, the results do not indicate that the division of labour in Philophthalmus sp. plays a role in competitive interactions as the ratio of small, non-reproductive to large, reproductive individuals is unaffected by the presence of intraspecific competition. This is the first study to identify and quantify intraspecific competition in Philophthalmus sp., and to assess its selective role in this species’ division of labour.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Dabo, A., Durand, P., Morand, S., Diakite, M., Langand, J., Imbert-Establet, D., Doumbo, O. and Jourdane, J. (1997). Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali. Acta Tropica 66, 1526. doi: http://dx.doi.org/10.1016/S0001-706X(97)00670-0.Google Scholar
Davies, C. M., Fairbrother, E. and Webster, J. P. (2002). Mixed strain Schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 3138.Google Scholar
Galaktionov, K. V. and Dobrovolskij, A. A. (2003). The Biology and Evolution of Trematodes. Kluwer Academic Publishers, Amsterdam, the Netherlands.CrossRefGoogle Scholar
Harvey, J. A., Corley, L. S. and Strand, M. R. (2000). Competition induces adaptive shifts in caste ratios of a polyembryonic wasp. Nature 406, 183186.CrossRefGoogle ScholarPubMed
Hechinger, R. F., Wood, A. C. and Kuris, A. M. (2011). Social organization in a flatworm: trematode parasites form soldier and reproductive castes. Proceedings of the Royal Society B, Biological Sciences 278, 656665. doi: 10.1098/rspb.2010.1753.Google Scholar
Hothorn, T., Bretz, F. and Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal 50, 346363.Google Scholar
Johnston, A. B. and Wilson, E. O. (1985). Correlates of variation in the major minor ratio of the ant, Pheidole dentata (Hymenoptera: Formicidae). Annals of the Entomological Society of America 78, 811.Google Scholar
Kamiya, T. and Poulin, R. (2013 a). Behavioural plasticity of social trematodes depends upon social context. Biology Letters 9. doi: 10.1098/rsbl.2012.1027 1744-957X.Google Scholar
Kamiya, T. and Poulin, R. (2013 b). Caste ratios affect the reproductive output of social trematode colonies. Journal of Evolutionary Biology 26, 509516.Google Scholar
Karvonen, A., Rellstab, C., Louhi, K.-R. and Jokela, J. (2012). Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites. Proceedings of the Royal Society B, Biological Sciences 279, 171176.Google Scholar
Keeney, D. B., Waters, J. M. and Poulin, R. (2007). Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Molecular Ecology 16, 431439. doi: MEC3143 [pii] 10.1111/j.1365-294X.2006.03143.x.Google Scholar
Keeney, D. B., Boessenkool, S., King, T. M., Leung, T. L. and Poulin, R. (2008). Effects of interspecific competition on asexual proliferation and clonal genetic diversity in larval trematode infections of snails. Parasitology 135, 741747. doi: 10.1017/S0031182008004435.CrossRefGoogle ScholarPubMed
Keeney, D. B., King, T. M., Rowe, D. L. and Poulin, R. (2009). Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites. Molecular Ecology 18, 45914603. doi: MEC4388 [pii] 10.1111/j.1365-294X.2009.04388.x.Google Scholar
Kuris, A. M. and Lafferty, K. D. (1994). Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189217. doi: 10.1146/annurev.es.25.110194.001201.CrossRefGoogle Scholar
Lafferty, K. D., Sammond, D. T. and Kuris, A. M. (1994). Analysis of larval trematode communities. Ecology 75, 22752285.CrossRefGoogle Scholar
Leung, T. L. F. and Poulin, R. (2011). Small worms, big appetites: ratios of different functional morphs in relation to interspecific competition in trematode parasites. International Journal for Parasitology 41, 10631068. doi: 10.1016/j.ijpara.2011.05.001.Google Scholar
Lloyd, M. M. and Poulin, R. (2011). In vitro culture of marine trematodes from their snail first intermediate host. Experimental Parasitology 129, 101106. doi: 10.1016/j.exppara.2011.07.009.CrossRefGoogle ScholarPubMed
Lloyd, M. M. and Poulin, R. (2012). Fitness benefits of a division of labour in parasitic trematode colonies with and without competition. International Journal for Parasitology 42, 939946. doi: 10.1016/j.ijpara.2012.07.010.Google Scholar
Lloyd, M. M. and Poulin, R. (2013). Reproduction and caste ratios under stress in trematode colonies with a division of labour. Parasitology 140: 825832. doi: 10.1017/S0031182012002235.Google Scholar
Louhi, K. R., Karvonen, A., Rellstab, C., Louhi, R. and Jokela, J. (2013). Prevalence of infection as a predictor of multiple genotype infection frequency in parasites with multiple host life cycles. Journal of Animal Ecology 82, 191200.Google Scholar
Martorelli, S. R., Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Description and proposed life cycle of Maritrema novaezealandensis n. sp (Microphallidae) parasitic in red-billed gulls, Larus novaehollandiae scopulinus, from Otago Harbour, South Island, New Zealand. Journal of Parasitology 90, 272277. doi: 10.1645/GE-3254.Google Scholar
Martorelli, S. R., Poulin, R. and Mouritsen, K. N. (2006). A new cercaria and metacercaria of Acanthoparyphium (Echinostomatidae) found in an intertidal snail Zeacumantus subcarinatus (Batillaridae) from New Zealand. Parasitology International 55, 163167.Google Scholar
Martorelli, S. R., Fredensborg, B. L., Leung, T. L. F. and Poulin, R. (2008). Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). New Zealand Journal of Zoology 35, 7384. doi: 10.1080/03014220809510104.CrossRefGoogle Scholar
Minchella, D. J., Sollenberger, K. M. and Desouza, C. P. (1995). Distribution of schistosome genetic diversity within molluscan intermediate hosts. Parasitology 111, 217220.Google Scholar
Miura, O. (2012). Social organization and caste formation in three additional parasitic flatworm species. Marine Ecology Progress Series 465, 119127.CrossRefGoogle Scholar
Miura, O., Kuris, A. M., Torchin, M. E., Hechinger, R. F., Dunham, E. J. and Chiba, S. (2005). Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793801. doi: http://dx.doi.org/10.1016/j.ijpara.2005.02.014.Google Scholar
Neal, A. T. and Poulin, R. (2012). Substratum preference of Philophthalmus sp. cercariae for cyst formation under natural and experimental conditions. Journal of Parasitology 98, 293298. doi: 10.1645/jp-ge-2969.Google Scholar
Oster, G. F. and Wilson, E. O. (1978). Caste and Ecology in the Social Insects. Princeton University Press, Princeton, NJ, USA.Google ScholarPubMed
Passera, L., Roncin, E., Kaufmann, B. and Keller, L. (1996). Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379, 630631. doi: 10.1038/379630a0.Google Scholar
Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122, S3S11.Google Scholar
R Development Core Team (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rauch, G., Kalbe, M. and Reusch, T. B. H. (2005). How a complex life cycle can improve a parasite's sex life. Journal of Evolutionary Biology 18, 10691075. doi: 10.1111/j.1420-9101.2005.00895.x.Google Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 10991102. doi: 10.1126/science.1059410.Google Scholar
Sire, C., Durand, P., Pointier, J. P. and Theron, A. (1999). Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers. Journal of Parasitology 85, 436441.Google Scholar
Sousa, W. P. (1992). Interspecific interactions among larval trematode parasites of freshwater and marine snails. American Zoologist 32, 583592.Google Scholar
Theron, A., Sire, C., Rognon, A., Prugnolle, F. and Durand, P. (2004). Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts. Parasitology 129, 571585. doi: 10.1017/S0031182004005943.Google Scholar
Thorne, B. L., Breisch, N. L. and Muscedere, M. L. (2003). Evolution of eusociality and the soldier caste in termites: influence of intraspecific competition and accelerated inheritance. Proceedings of the National Academy of Sciences USA 100, 1280812813. doi: 10.1073/pnas.2133530100.Google Scholar
Turnbull, C., Caravan, H., Chapman, T., Nipperess, D., Dennison, S., Schwarz, M. and Beattie, A. (2012). Antifungal activity in thrips soldiers suggests a dual role for this caste. Biology Letters 8, 526529. doi: 10.1098/rsbl.2012.0184.Google Scholar
Wong, N. and Lee, C.-Y. (2010). Intra- and interspecific agonistic behavior of the subterranean termite Microcerotermes crassus (Isoptera: Termitidae). Journal of Economic Entomology 103, 17541760. doi: 10.1603/ec10060.CrossRefGoogle ScholarPubMed
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