Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-24T16:34:42.112Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproduction and caste ratios under stress in trematode colonies with a division of labour

Published online by Cambridge University Press:  27 February 2013

MELANIE M. LLOYD  and
ROBERT POULIN
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. Tel: +64 3 479 7986. Fax: +64 3 479 7584. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Trematodes form clonal colonies in their first intermediate host. Individuals are, depending on species, rediae or sporocysts (which asexually reproduce) and cercariae (which develop within rediae or sporocysts and infect the next host). Some species use a division of labour within colonies, with 2 distinct redial morphs: small rediae (non-reproducing) and large rediae (individuals which produce cercariae). The theory of optimal caste ratio predicts that the ratio of caste members (small to large rediae) responds to environmental variability. This was tested in Philophthalmus sp. colonies exposed to host starvation and competition with the trematode, Maritrema novaezealandensis. Philophthalmus sp. infected snails, with and without M. novaezealandensis, were subjected to food treatments. Reproductive output, number of rediae, and the ratio of small to large rediae were compared among treatments. Philophthalmus sp. colonies responded to host starvation and competition; reproductive output was higher in well-fed snails of both infection types compared with snails in lower food treatments and well-fed, single infected snails compared with well-fed double infected snails. Furthermore, the caste ratio in Philophthalmus sp. colonies was altered in response to competition. This is the first study showing caste ratio responses to environmental pressures in trematodes with a division of labour.

Keywords

host dietcompetitioncolony reproductive successPhilophthalmus sp.Zeacumantus subcarinatusMaritrema novaezealandensis
Type
Research Article
Information
Parasitology , Volume 140 , Issue 7 , June 2013 , pp. 825 - 832
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bates, D., Maechler, M. and Bolker, B. (2011). Linear mixed-effects models using S4 classes. Available at http://cran.R-project.org/package=lme4Google Scholar
Bedhomme, S., Agnew, P., Sidobre, C. and Michalakis, Y. (2004). Virulence reaction norms across a food gradient. Proceedings of the Royal Society B: Biological Sciences 271, 739–744. doi: 10.1098/rspb.2003.2657.CrossRefGoogle ScholarPubMed
Blackman, R. L. (1979). Stability and variation in aphid clonal lineages. Biological Journal of the Linnean Society 11, 259–277. doi: 10.1111/j.1095-8312.1979.tb00038.x.CrossRefGoogle Scholar
Brusca, R. C. and Brusca, G. J. (2003). Invertebrates, 2nd Edn. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Calabi, P. and Traniello, J. F. A. (1989). Social organization in the ant Pheidole dentata. Behavioral Ecology and Sociobiology 24, 69–78. doi: 10.1007/bf00299638.CrossRefGoogle Scholar
Coors, A. and De Meester, L. (2011). Fitness and virulence of a bacterial endoparasite in an environmentally stressed crustacean host. Parasitology 138, 122–131. doi: 10.1017/S0031182010000995.CrossRefGoogle Scholar
Craig, S., Slobodkin, L., Wray, G. and Biermann, C. (1997). The ‘paradox’ of polyembryony: a review of the cases and a hypothesis for its evolution. Evolutionary Ecology 11, 127–143. doi: 10.1023/a:1018443714917.CrossRefGoogle Scholar
Ebert, D., Zschokke-Rohringer, C. D. and Carius, H. J. (2000). Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122, 200–209. doi: 10.1007/pl00008847.CrossRefGoogle ScholarPubMed
Fellous, S. and Koella, J. C. (2010). Cost of co-infection controlled by infectious dose combinations and food availability. Oecologia 162, 935–940.CrossRefGoogle ScholarPubMed
Galaktionov, K. V. and Dobrovolskij, A. A. (2003). The Biology and Evolution of Trematodes. Kluwer Academic Publishers, Dordrecht, the Netherlands.CrossRefGoogle Scholar
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, 656–665. doi: 10.1098/rspb.2010.1753.CrossRefGoogle Scholar
Hendrickson, M. A. and Curtis, L. A. (2002). Infrapopulation sizes of co-occurring trematodes in the snail Ilyanassa obsoleta. Journal of Parasitology 88, 884–889. doi: 10.1645/0022-3395(2002)088[0884:isocot]2.0.co;2.CrossRefGoogle ScholarPubMed
Herbers, J. M. (1980). On caste ratios in ant colonies: population responses to changing environments. Evolution 34, 575–585.CrossRefGoogle ScholarPubMed
Jokela, J., Taskinen, J., Mutikainen, P. and Kopp, K. (2005). Virulence of parasites in hosts under environmental stress: experiments with anoxia and starvation. Oikos 108, 156–164. doi: 10.1111/j.0030-1299.2005.13185.x.CrossRefGoogle Scholar
Keas, B. E. and Esch, G. W. (1997). The effect of diet and reproductive maturity on the growth and reproduction of Helisoma anceps (Pulmonata) infected by Halipegus occidualis (Trematoda). Journal of Parasitology 83, 96–104.CrossRefGoogle ScholarPubMed
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, 741–747. doi: 10.1017/S0031182008004435.CrossRefGoogle ScholarPubMed
Kendall, S. B. (1949). Nutritional factors affecting the rate of development of Fasciola hepatica in Limnaea truncatula. Journal of Helminthology 23, 179–190. doi: 10.1017/S0022149X00032491.CrossRefGoogle Scholar
Krist, A. C., Jokela, J., Wiehn, J. and Lively, C. M. (2004). Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail–trematode interaction. Journal of Evolutionary Biology 17, 33–40. doi: 10.1046/j.1420-9101.2003.00661.x.CrossRefGoogle Scholar
Latshaw, D. J. (1991). Nutrition – mechanisms of immunosuppression. Veterinary Immunology and Immunopathology 30, 111–120. doi: 10.1016/0165-2427(91)90012-2.CrossRefGoogle ScholarPubMed
Lei, F. and Poulin, R. (2011). Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Marine Biology 158, 995–1003. doi: 10.1007/s00227-011-1625-7.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, 1063–1068. doi: 10.1016/j.ijpara.2011.05.001.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, 939–946. doi: 10.1016/j.ijpara.2012.07.010.CrossRefGoogle ScholarPubMed
Lloyd, S. (1995). Environmental influences on host immunity. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfeld, B. T. and Dobson, A. P.), pp. 327–361. Cambridge University Press, Cambridge, UK.CrossRefGoogle 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 Harbor, South Island, New Zealand. Journal of Parasitology 90, 272–277. doi: 10.1645/GE-3254.CrossRefGoogle 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, 73–84. doi: 10.1080/03014220809510104.CrossRefGoogle Scholar
McClatchie, S. (1979). Grazing of Zeacumantus subcarinatus (Gastropoda) on Ulva lactuca. Mauri Ora 7, 39–45.Google Scholar
McGlynn, T. (2010). Polygyny in thief ants responds to competition and nest limitation but not food resources. Insectes Sociaux 57, 23–28. doi: 10.1007/s00040-009-0045-x.CrossRefGoogle Scholar
McGlynn, T. and Owen, J. (2002). Food supplementation alters caste allocation in a natural population of Pheidole flavens, a dimorphic leaf-litter dwelling ant. Insectes Sociaux 49, 8–14. doi: 10.1007/s00040-002-8270-6.CrossRefGoogle Scholar
Miura, O. (2012). Social organization and caste formation in three additional parasitic flatworm species. Marine Ecology Progress Series 465, 119–127.CrossRefGoogle 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, 293–298. doi: 10.1645/jp-ge-2969.CrossRefGoogle ScholarPubMed
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. (1977). Production des soldats dans les sociétés sortant d'hibernation chez la fourmi Pheidole pallidula (Nyl.) (Formicidae, Myrmicinae). Insectes Sociaux 24, 131–146. doi: 10.1007/BF02227167.CrossRefGoogle Scholar
Passera, L., Roncin, E., Kaufmann, B. and Keller, L. (1996). Increased soldier production in ant colonies exposed to intraspecific competition. Nature, London 379, 630–631. doi: 10.1038/379630a0.CrossRefGoogle Scholar
Poulin, R. (1996). Evolution of life history strategies in parasitic animals. Advances in Parasitology 37, 107–134.CrossRefGoogle ScholarPubMed
Poulin, R. (2001). Interactions between species and the structure of helminth communities. Parasitology 122, S3–S11.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Pruett, S. B., Ensley, D. K. and Crittenden, P. L. (1993). The role of chemical induced stress responses in immunosuppression: a review of quantitative associations and cause effect relationships between chemical induced stress responses and immunosuppression. Journal of Toxicology and Environmental Health, Part A Current Issues 39, 163–192. doi: 10.1080/15287399309531744.CrossRefGoogle ScholarPubMed
R Development Core Team (2011). R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Ratnieks, F. L. W., Foster, K. R. and Wenseleers, T. (2011). Darwin's special difficulty: the evolution of ‘neuter insects’ and current theory. Behavioral Ecology and Sociobiology 65, 481–492. doi: 10.1007/s00265-010-1124-8.CrossRefGoogle Scholar
Rondelaud, D., Belfaiza, M., Vignoles, P., Moncef, M. and Dreyfuss, G. (2009). Redial generations of Fasciola hepatica: a review. Journal of Helminthology 83, 245–254. doi: 10.1017/S0022149X09222528.CrossRefGoogle ScholarPubMed
Saarinen, M. and Taskinen, J. (2005). Long-lasting effect of stress on susceptibility of a freshwater clam to copepod parasitism. Parasitology 130, 523–529. doi: 10.1017/S0031182004006869.CrossRefGoogle ScholarPubMed
Sandland, G. J. and Minchella, D. J. (2003). Effects of diet and Echinostoma revolutum infection on energy allocation patterns in juvenile Lymnaea elodes snails. Oecologia 134, 479–486. doi: 10.1007/s00442-002-1127-x.CrossRefGoogle ScholarPubMed
Seeley, T. D. (1995). The Wisdom of the Hive. The Social Physiology of Honey Bee Colonies. Harvard University Press, Cambridge, MA, USA.CrossRefGoogle Scholar
Seppälä, O., Liljeroos, K., Karvonen, A. and Jokela, J. (2008). Host condition as a constraint for parasite reproduction. Oikos 117, 749–753. doi: 10.1111/j.2008.0030-1299.16396.x.CrossRefGoogle Scholar
Shostak, A. W. and Dick, T. A. (1986). Effect of food intake by Cyclops biscuspidatus thomasi (Copepoda) on growth of proceroids of Triaenophorus crassus (Pseudophyllidea) and on host fecundity. American Midland Naturalist 115, 225–233.CrossRefGoogle Scholar
Sousa, W. P. (1992). Interspecific interactions among larval trematode parasites of freshwater and marine snails. American Zoologist 32, 583–592.CrossRefGoogle Scholar
Walker, J. and Stamps, J. (1986). A test of optimal caste ratio theory using the ant Camponotus (Colobopsis) impressus. Ecology 67, 1052–1062.CrossRefGoogle Scholar
West, A. F. (1961). Studies on the biology of Philophthalmus gralli Mathis and Leger, 1910 (Trematoda: Digenea). American Midland Naturalist 66, 363–383.CrossRefGoogle Scholar
Supplementary material: File

Lloyd Supplementay Material

Tables 1-2

Download Lloyd Supplementay Material(File)
File 13.6 KB