Social organization in a flatworm: trematode parasites form soldier and reproductive castes

In some of the most complex animal societies, individuals exhibit a cooperative division of labour to form castes. The most pronounced types of caste formation involve reproductive and non-reproductive forms that are morphologically distinct. In colonies comprising separate or mobile individuals, this type of caste formation has been recognized only among the arthropods, sea anemones and mole-rats. Here, we document physical and behavioural caste formation in a flatworm. Trematode flatworm parasites undergo repeated clonal reproduction of ‘parthenitae’ within their molluscan hosts forming colonies. We present experimental and observational data demonstrating specialization among trematode parthenitae to form distinct soldier and reproductive castes. Soldiers do not reproduce, have relatively large mouthparts, and are much smaller and thinner than reproductives. Soldiers are also more active, and are disproportionally common in areas of the host where invasions occur. Further, only soldiers readily and consistently attack heterospecifics and conspecifics from other colonies. The division of labour described here for trematodes is strongly analogous to that characterizing other social systems with a soldier caste. The parallel caste formation in these systems, despite varying reproductive mode and taxonomic affiliation, indicates the general importance of ecological factors in influencing the evolution of social behaviour. Further, the ‘recognition of self’ and the defence of the infected host body from invading parasites are comparable to aspects of immune defence. A division of labour is probably widespread among trematodes and trematode species encompass considerable taxonomic, life history and environmental diversity. Trematodes should therefore provide new, fruitful systems to investigate the ecology and evolution of sociality.     

Ultimate parasites

Evolutionary Ecology of Parasites. From Individuals to Communities by Robert Poulin, Chapman & Hall, 1998. £55.00 hbk (x+212 pages) ISBN 0 412 80560 X     

Flypaper for parasites

In this issue, Kamhawi et al. (2004) describe the identification of an insect galectin as the receptor for the stage-specific Leishmania adhesin lipophosphoglycan (LPG). This interaction is critical for parasite survival in the midgut of its sand fly vector. The results open new avenues for studies of insect immunity, transmission binding vaccines, and host-parasite coevolution.     

Antlers and parasites

Development of ornamental characters exposed to directional selection may be particularly sensitive to the effect of parasitic infections. Antlers are ornamental characters of importance in intraspecific interactions, and are in reindeer (Rangifer) developed by both males and females. By antihelmintic treatment of naturally infected female reindeer we show that parasite intensities affect development of antler asymmetry, but not antler length. These results suggest that asymmetry in antlers may reflect parasite intensities and thus be of importance in intraspecific assessment of genetic resistance towards infectious organisms.     

Ecology of marine parasites

Important ecological aspects of marine parasites are discussed. Whereas effects of parasites on host individuals sometimes leading to death are known from many groups of parasites, effects on host populations have been studied much less. Mass mortalities have been observed mainly among hosts occurring in abnormally dense populations or after introduction of parasites by man. As a result of large-scale human activities, it becomes more and more difficult to observe effects of parasites on host populations under natural conditions. Particular emphasis is laid on ecological characteristics of parasites, such as host range and specificity, microhabitats, macrohabitats, food, life span, aggregated distribution, numbers and kinds of parasites, pathogenicity and mechanisms of reproduction and infection and on how such characteristics are affected by environment and hosts. It is stressed that host specificity indices which take frequency and/or intensity of infection into account, are a better measure of restriction of parasites to certain hosts than host range which simply is the number of host species found to be infected.     

Signaling health versus parasites

The Hamilton-Zuk hypothesis, that parasite-host coevolution can maintain heritable variation in fitness, has inspired a very successful research program on sexual selection on signals of health. The immunocompetence handicap hypothesis was developed to provide a handicapping mechanism to stabilize the correlation between signals and health. In earlier articles, I showed that handicap signaling is a special case, not a general law that we can rely on to deduce relative costs across signalers of different quality at equilibrium. The essential requirement for reliable signaling is that higher-quality signalers are more efficient; they get greater marginal fitness returns from an incremental increase in the signal. This does not undermine the Hamilton-Zuk hypothesis or the immunocompetence mechanism, but it does raise doubts about a widespread assumption that is commonly used to test these hypotheses: that sexual selection on signals of health implies the choice of mates with the fewest parasites. Immunity and parasites might play a fundamental role in many biological signaling systems, but viability-indicating traits are not necessarily parasite-load-indicating traits. Theory allows for the possibility that high-quality big signalers have greater health and more parasites than low-quality small signalers (and the data suggest that in many systems they do). This means that we cannot test the Hamilton-Zuk hypothesis or the immunocompetence handicap hypothesis by counting parasites. More generally, we cannot understand sexual selection on signals of health by focusing on the viability costs of signals.     

Encystation of entamoeba parasites

Entamoeba histolytica is a protozoan parasite of humans, and the causitive agent of intestinal amebiasis. The disease-causing stage of the parasite is an osmotically sensitive ameboid form, which differentiates into a thick-walled cyst for transmission from person to person. The conditions within the human intestine that induce encystment of the amoeba are unknown, but studies using an amoebic parasite of reptiles are now yielding information about the molecules and host:parasite interactions involved in the process. An understanding of the amoeba's obligatory encystment pathway should provide an approach for interrupting the transmission of this parasite, for which there is currently no vaccine.     

Acidocalcisomes in Apicomplexan parasites

Acidocalcisomes are acidic calcium stores found in diverse organisms, being conserved from bacteria to man. They posses an acidic matrix that contains several cations bound to phosphates, mainly present in the form of short and long polyphosphate chains. Their matrix is acidified through the action of proton pumps such as a vacuolar proton ATPase and a vacuolar proton pyrophosphatase. The calcium uptake occurs through a Ca2+/H+ counter transporting ATPase located in the membrane of the organelle. Acidocalcisomes have been identified in a variety of microorganisms, including Apicomplexan parasites such as Plasmodium and Eimeria species, and in Toxoplasma gondii. In this paper, we review the structural, biochemical and physiological aspects of acidocalcisomes in Apicomplexan parasites and discuss their functional roles in the maintenance of intracellular ion homeostasis.