Abstract
Phenotypic diversification among colony members often leads to formation of physical castes which are morphologically specialised for particular tasks within the colony. The relative abundance of these castes and their body sizes represent two key aspects of the demography of a colony that may reflect the colony’s needs and conditions, and ultimately influence its survival and reproductive success. In a recently discovered social trematode, Philophthalmus sp., which exhibits a reproductive division of labour, the role of competition and colony composition in shaping reproductive success and behaviour of colony members has been documented. As body size variation within physical castes often influences colony efficiency, we investigated how the growth of reproductive and non-reproductive morphs of Philophthalmus sp. responds to competitive pressure, and to other attributes of colony demography such as colony size and composition. Our survey of a natural population and in vitro experiments demonstrate that the growth of reproductive colony members reflects the interaction between colony composition and the presence of a competitor, while the non-reproductive members simply grow larger in the presence of the intra-host competitor, Maritrema novaezealandensis. Furthermore, the close association between the volume and reproductive capacity of the reproductive members corroborates an adaptive value of colony member size in determining the fitness of the trematode colony as a whole. The present study is the first to demonstrate a fitness consequence, and identify the determinants, of the growth of colony members in social trematodes.
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References
Ayre DJ, Grosberg RK (1996) Effects of social organization on inter-clonal dominance relationships in the sea anemone Anthopleura elegantissima. Anim Behav 51:1233–1245
Bates AE, Leiterer F, Wiedeback ML, Poulin R (2011) Parasitized snails take the heat: a case of host manipulation? Oecologia 167:613–621
Belfaiza M, Abrous M, Rondelaud D, Moncef M, Dreyfuss G (2004a) The use of Tetraphyll as food for snails increases the intensity of cercarial shedding in Galba truncatula infected with Fasciola hepatica. Parasitol Res 94:86–90
Belfaiza M, Rondelaud D, Moncef M, Dreyfuss G (2004b) Fasciola hepatica: the effect of food quality on the development of redial generations in Galba truncatula infected with allopatric miracidia. Parasitol Res 92:12–17
Couvillon MJ, Dornhaus A (2009) Location, location, location: larvae position inside the nest is correlated with adult body size in worker bumble-bees (Bombus impatiens). Proc R Soc Lond B Bio 276:2411–2418
Davidson DW (1978) Size variability in worker caste of a social insect (Veromessor pergandei mayr) as a function of competitive environment. Am Nat 112:523–532
Duffy JE (1996) Eusociality in a coral-reef shrimp. Nature 381:512–514
Hasegawa E (1997) The optimal caste ratio in polymorphic ants: estimation and empirical evidence. Am Nat 149:706–722
Hechinger RF, Wood AC, Kuris AM (2011) Social organization in a flatworm: trematode parasites form soldier and reproductive castes. Proc R Soc Lond B Bio 278:656–665
Ishikawa Y, Miura T (2012) Hidden aggression in termite workers: plastic defensive behaviour dependent upon social context. Anim Behav 83:737–745
Jarvis JUM (1981) Eusociality in a mammal—cooperative breeding in naked mole-rat colonies. Science 212:571–573
Kamiya T, Poulin R (2013) Caste ratios affect the reproductive output of social trematode colonies. J Evol Biol 26:509–516
Kaspari M (1996) Worker size and seed size selection by harvester ants in a Neotropical forest. Oecologia 105:397–404
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
Koprivnikar J, Poulin R (2009) Effects of temperature, salinity, and water level on the emergence of marine cercariae. Parasitol Res 105:957–965
Kuris AM, Lafferty KD (1994) Community structure—larval trematodes in snail hosts. Annu Rev Ecol Syst 25:189–217
Lecoutey E, Châline N, Jaisson P (2011) Clonal ant societies exhibit fertility-dependent shifts in caste ratios. Behav Ecol 22:108–113
Lei F, Poulin R (2011) Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Mar Biol 158:995–1003
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
Lloyd MM, Poulin R (2011) In vitro culture of marine trematodes from their snail first intermediate host. Exp Parasitol 129:101–106
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
Martorelli SR, Fredensborg BL, Leung TLF, Poulin R (2008) Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). N Z J Zool 35:73–84
Mitchell RE, Frost CL, Hughes WOH (2012) Size and asymmetry: are there costs to winning the royalty race? J Evol Biol 25:522–531
Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton
Paris OH, Petelka FA (1962) Population characteristics of the terrestrial isopod Armadillidium vulgare in California grassland. Ecology 43:222–248
Passera L, Roncin E, Kaufmann B, Keller L (1996) Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379:630–631
Porter SD, Tschinkel WR (1985) Fire ant polymorphism (Hymenoptera, Formicidae)—factors affecting worker size. Ann Entomol Soc Am 78:381–386
Poulin R (2001) Interactions between species and the structure of helminth communities. Parasitology 122:S3–S11
Rinkevich B, Loya Y (1979) Reproduction of the red-sea coral Stylophora pistillata. 1. Gonads and planulae. Mar Ecol Prog Ser 1:133–144
Rissing SW (1987) Annual cycles in worker size of the seed-harvester ant Veromessor pergandei (Hymenoptera, Formicidae). Behav Ecol Sociobiol 20:117–124
Rondelaud D, Vignoles P, Dreyfuss G (2004) Fasciola hepatica: the developmental patterns of redial generations in naturally infected Galba truncatula. Parasitol Res 94:183–187
Schmidt AM, Linksvayer TA, Boomsma JJ, Pedersen JS (2011) Queen-worker caste ratio depends on colony size in the pharaoh ant (Monomorium pharaonis). Insectes Soc 58:139–144
Suchanek TH (1981) The role of disturbance in the evolution of life-history strategies in the inter-tidal mussels Mytilus edulis and Mytilus californianus. Oecologia 50:143–152
R Development Core Team (2011) R: A language and environment for statistical computing. In, 2.14.1 edn. R Foundation for Statistical Computing, Vienna, Austria
Wilson EO (1971) The insect societies. The Belknap Press of Harvard University Press, Cambridge
Yang AS, Martin CH, Nijhout HF (2004) Geographic variation of caste structure among ant populations. Curr Biol 14:514–519
Acknowledgments
We are grateful to Manami Iwakura for field assistance; Melanie Lloyd for lab assistance, and to two anonymous reviewers for useful comments.
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Kamiya, T., O’Dwyer, K., Nuy, J. et al. What determines the growth of individual castes in social trematodes?. Evol Ecol 27, 1235–1247 (2013). https://doi.org/10.1007/s10682-013-9646-y
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DOI: https://doi.org/10.1007/s10682-013-9646-y