Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T02:55:28.692Z Has data issue: false hasContentIssue false

Caste formation in larval Himasthla elongata (Trematoda) infecting common periwinkles Littorina littorea

Published online by Cambridge University Press:  02 April 2014

Sigrid S. Nielsen
Affiliation:
Department of Bioscience, Aarhus University, Ole Worms Allé 1, 8000 Aarhus C, Denmark
Malan Johansen
Affiliation:
Department of Bioscience, Aarhus University, Ole Worms Allé 1, 8000 Aarhus C, Denmark
Kim N. Mouritsen*
Affiliation:
Department of Bioscience, Aarhus University, Ole Worms Allé 1, 8000 Aarhus C, Denmark
*
Correspondence should be addressed to: K.N. Mouritsen, Department of Bioscience, Aarhus University, Ole Worms Allé 1, 8000 Aarhus C, Denmark email: [email protected]

Abstract

Reproductive division of labour is well-known in several animal groups but the ecological factors driving the evolution of such social organization are still being discussed. Recent studies have discovered social organization in four marine species of trematode parasites having two distinct castes specialized for reproduction and defence of the clonal intra-molluscan larval colony, respectively. Here, we provide novel evidence for social structure also in colonies of the trematode Himasthla elongata infecting the common periwinkle Littorina littorea. We found two types of rediae, the parthenogenetic larval offspring of the parasite: small non-reproductive rediae and considerably larger reproductive rediae. Both redial types possessed a digestive system, collar and posterior appendages and, hence, aside from dimensions, were morphologically similar. However, in vitro experiments showed that non-reproductive morphs attacked heterospecific competing parasites at a higher rate (2–3 fold) than reproductive morphs did. No within-colony antagonism was observed. In contrast to a previous study on a congeneric trematode species, our findings suggest a relatively weak caste formation in H. elongata, possibly resulting from a corresponding weaker level of interspecific competition.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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

Aoki, S. (1977) Colophina clematis (Homoptera, Pemphigidae), an aphid species with ‘soldiers’. Kontyu 45, 276282.Google Scholar
Bourke, A.F.G. (2011) The validity and value of inclusive fitness theory. Proceedings of the Royal Society of London, B 278, 33133320.Google Scholar
Crespi, B.J. (1994) Three conditions for the evolution of eusociality—are they sufficient? Insectes Sociaux 41, 395400.Google Scholar
Crespi, B.J. and Yanega, D. (1995) The definition of eusociality. Behavioural Ecology 6, 109115.Google Scholar
Esteban, J.G. and Muñoz-Antoli (2009) Echinostomes: systematics and life cycles. In Fried, B. and Toledo, R. (eds) The biology of echinostomes. Berlin: Springer, pp. 133.Google Scholar
Galaktionov, K.V. and Dobrovolskij, A.A. (2003) The biology and evolution of trematodes. Dordrecht: Kluwer Academic.Google Scholar
Hamilton, W.D. (1964) Genetical evolution of social behaviour. I and II. Journal of Theoretical Biology 7, 152.Google 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 of London, B 278, 656665.Google Scholar
Hughes, W.O.H., Oldroyd, B.P., Beekman, M. and Ratnieks, F.L.W. (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 12131216.Google Scholar
Hyman, I.H. (1967) The invertebrates: volume VI, mollusca I. New York: McGraw-Hill.Google Scholar
Kuris, A.M. (1990) Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. In Esch, G.W., Bush, A.O. and Aho, J.M. (eds) Parasite communities: patterns and processes. London: Chapmann and Hall, pp. 69100.Google Scholar
Lauckner, G. (1980) Diseases of mollusca: gastropoda. In Kinne, O. (ed.) Diseases of marine animals, Volume 1. Hamburg: Biologische Anstalt Helgoland, pp. 311424.Google Scholar
Lauckner, G. (1983) Diseases of mollusca: bivalvia. In Kinne, O. (ed.) Diseases of marine animals, Volume 2. Hamburg: Biologische Anstalt Helgoland, pp. 477962.Google Scholar
Leung, T.L.F. and Poulin, R. (2012) Small worms, big appetites: ratios of different functional morphs in relation to interspecific competition in trematode parasites. International Journal for Parasitology 41, 10631068.Google Scholar
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.Google Scholar
Miura, O. (2012) Social organization and caste formation in three additional parasitic flatworm species. Marine Ecology Progress Series 465, 119127.Google Scholar
Nowak, M.A., Tarnita, C.E. and Wilson, E.O. (2010) The evolution of eusociality. Nature 466, 10571062.Google Scholar
Poulin, R. and Mouritsen, K.N. (2003) Large-scale determinants of trematode infections in intertidal gastropods. Marine Ecology Progress Series 254, 187198.Google Scholar
Sousa, W.P. (1983) Host life history and the effect of parasitic castration on growth: a field study of Cerithidea californica Haldeman (Gastropoda: Prosobranchia) and its trematode parasites. Journal of Experimental Marine Biology and Ecology 73, 273296.Google Scholar
Sousa, W. (1993) Interspecifik antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs 63, 103128.Google Scholar
Stunkard, H.W. (1938) The morphology and life cycle of the trematode Himasthla quissetensis (Miller and Northup, 1926). Biological Bulletin. Marine Biological Laboratory, Woods Hole 75, 145164.Google Scholar
Stunkard, H.W. (1966) The morphology and life history of the digenetic trematode Himasthla littorinae sp. (Echinostomatidae). Journal of Parasitology 52, 367372.Google Scholar
Werding, B. (1969) Morphologie, entwicklung und ökologie digener trematoden-larven der strandschnecke Littorina littorea. Marine Biology 3, 306333.CrossRefGoogle Scholar
Wilson, E.O. (1971) The insect societies. Cambridge, MA: Belknap Press of Harvard University Press.Google Scholar