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Social flatworms: the minor caste is adapted for attacking competing parasites

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Abstract

Recently, it has been hypothesized that some marine parasitic flatworms (trematoda) within their gastropod hosts form socially organized larval colonies divided into distinct castes adapted for defence and reproduction. However, the evidence in support for advanced division of labour in trematodes is challengeable and generally consistent with the traditional view of ordinary age-structured colonies. Using intramolluscan larval colonies of the trematode Himasthla elongata (Echinostomatidae) as study system, we demonstrate experimentally that contrary to reproducing colony members, non-reproducing larvae are anatomically and behaviourally adapted of defending the colony against competing parasites infecting the same host. We also show that co-infections are significantly less frequent in situ than expected by chance, which emphasizes the efficiency of the antagonistic activity of Himasthla colonies in eliminating competitors. Together, this brings novel and pivotal support to the view of adaptive cast formation in marine trematodes.

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References

  • Crespi BJ (1994) Three conditions for the evolution of eusociality: are they sufficient? Insect Soc 41:395–400

    Article  Google Scholar 

  • Crespi BJ, Yanega D (1995) The definition of eusociality. Behav Ecol 6:109–115

    Article  Google Scholar 

  • Curtis LA (2003) Tenure of individual larval trematode infections in an estuarine gastropod. J Mar Biol Assoc UK 83:1047–1051

    Article  Google Scholar 

  • Galaktionov KV, Dobrovolskij AA (2003) The biology and evolution of trematodes. Kluwer, Dordrecht

    Book  Google Scholar 

  • Gorbushin AM, Iakovleva NV (2008) The enigma of the haemogram “left-shift” in periwinkles infected with trematodes. Fish Shellfish Immun 24:745–751

    Article  CAS  Google Scholar 

  • Gorbushin AM, Shaposhnikova TG (2002) In vitro culture of the avian echinostome Himasthla elongata: from redia to marita. Exp Parasitol 101:234–239

    Article  CAS  Google Scholar 

  • Hamilton WD (1964) Genetical evolution of social behaviour. I and II. J Theo Biol 7:1–52

    Article  CAS  Google Scholar 

  • Hechinger RF, Wood AC, Kuris AM (2011) Social organization in a flatworm: trematode parasites form soldier and reproductive castes. Proc R Soc Lond B 278:656–665

    Article  Google Scholar 

  • Huxham M, Raffaelli D, Pike A (1993) The influence of Cryptocotyle lingua (Digenea: Plathyhelminthes) infections on the survival and fecundity of Littorina littorea (Gastropoda: Prosobranchia); an ecological approach. J Exp Mar Biol Ecol 168:223–238

    Article  Google Scholar 

  • Iakovleva NV, Shaposhnikova TG, Gorbushin AM (2006) Rediae of echinostomatid and heterophyid trematodes suppress phagocytosis of haemocytes in Littorina littorea (Gastropoda: Prosobranchia). Exp Parasitol 113:24–29

    Article  CAS  Google Scholar 

  • Kamiya T, Poulin R (2013) Caste ratios affect the reproductive output of social trematode colonies. J Evol Biol 26:509–516

    Article  CAS  Google Scholar 

  • Karvonen A, Rellstab C, Louhi K-R, Jokela J (2012) Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites. Proc R Soc Lond B 279:171–176

    Article  Google Scholar 

  • Kearn GC (1998) Parasitism and the platyhelminths. Springer, London

    Google Scholar 

  • Keeney DB, Boessenkool S, King TM, Leung TLF, Poulin R (2008) Effects of interspecific competition on asexual proliferation and clonal genetic diversity in larval trematode infections of snails. Parasitology 135:741–747

    Article  CAS  Google Scholar 

  • Kuris AM, Lafferty KD (1994) Community structure: larval trematodes in snail hosts. Annu Rev Ecol Syst 25:189–217

    Article  Google Scholar 

  • Lafferty KD, Sammond DT, Kuris AM (1994) Analysis of larval trematode communities. Ecology 75:2275–2285

    Article  Google Scholar 

  • Leung TLF, Poulin R (2011) Small worms, big appetites: ratios of different functional morphs in relation to interspecific competition in trematode parasites. Int J Parasitol 41:1063–1068

    Article  Google Scholar 

  • Lloyd MM, Poulin R (2012) Fitness benefits of a division of labour in parasitic trematode colonies with and without competition. Int J Parasitol 42:939–946

    Article  Google Scholar 

  • Lloyd MM, Poulin R (2013) Reproduction and caste ratios under stress in trematode colonies with a division of labour. Parasitology 140:939–946

    Article  Google Scholar 

  • Lloyd MM, Poulin R (2014a) Multi-clone infections and the impact of intraspecific competition on trematode colonies with a division of labour. Parasitology 141:304–310

    Article  Google Scholar 

  • Lloyd MM, Poulin R (2014b) Geographic variation in caste ratio of trematode colonies with a division of labour reflects local adaptation. Parasitol Res 113:2593–2602

    Article  Google Scholar 

  • Loker ES (1994) On being a parasite in an invertebrate host: a short survival course. J Parasitol 80:728–747

    Article  CAS  Google Scholar 

  • Miura O (2012) Social organization and caste formation in three additional parasitic flatworm species. Mar Ecol Prog Ser 465:119–127

    Article  Google Scholar 

  • Nielsen SS, Johansen M, Mouritsen KN (2014) Caste formation in larval Himasthla elongata (Trematoda) infecting common periwinkles Littorina littorea. J Mar Biol Assoc UK 94:917–923

    Article  Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton

    Google Scholar 

  • Passara L, Ronchin E, Kaufmann B, Keller L (1996) Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379:630–631

    Article  Google Scholar 

  • Pechenik JA (2010) Biology of the invertebrates, 6th edn. McGraw-Hill, New York

    Google Scholar 

  • Pinheiro J, Maldonado Júnior A, Attias M, Lanfredi RM (2004) Morphology of the rediae Echinostoma paraensei (Trematoda: Echonostomatidae) from its intermediate host Lymnaea columella (Mollusca, Gastropoda). Parasitol Res 93:171–177

    Article  CAS  Google Scholar 

  • Podvyaznaya IM, Galaktionov KV (2014) Trematode reproduction in the molluscan host: an ultrastructural study of the germinal mass in the rediae of Himasthla elongata (Mehlis, 1831) (Digenea: Echinostomatidae). Parasitol Res 113:1215–1224

    Article  Google Scholar 

  • Seid MA, Traniello JFA (2006) Age-related repertoire expansion and division of labor in Pheidole dentata (Hymnoptera : Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav Ecol Sociobiol 60:631–644

    Article  Google Scholar 

  • Sousa W (1993) Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecol Monograph 63:103–128

    Article  Google Scholar 

  • Tian L, Zhou X (2014) The soldiers in societies: defence, regulation, and evolution. Int J Biol Sci 10:296–308

    Article  Google Scholar 

  • Torres VO, Montagna TS, Raizer J, Antonialli-Junior WF (2012) Division of labor in colonies of the eusocial wasp, Mischocyttarus consimilis. J Insect Sci 12:1–15

    Article  Google Scholar 

  • Werding B (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Mar Biol 3:306–333

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, New York, pp 4–6

    Google Scholar 

  • Zdarska Z, Nasincova V, Valkuonova J (1988) Multiviliate sensory endings in the rediae of Echinostoma revolutum (Trematoda, Echinostomatidae). Folia Parasitol 35:17–20

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Bioscience, Aquatic Biology, Aarhus University, Ole Worms Allé 1, DK-8000, Aarhus C, Denmark

    Kim N. Mouritsen & Frej J. Halvorsen

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  1. Kim N. Mouritsen
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  2. Frej J. Halvorsen
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Correspondence to Kim N. Mouritsen.

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Communicated by T. Reusch.

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Mouritsen, K.N., Halvorsen, F.J. Social flatworms: the minor caste is adapted for attacking competing parasites. Mar Biol 162, 1503–1509 (2015). https://doi.org/10.1007/s00227-015-2686-9

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  • DOI: https://doi.org/10.1007/s00227-015-2686-9

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