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Progenesis and Reduced Virulence As an Alternative Transmission Strategy in a Parasitic Trematode

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Progenesis and Reduced Virulence As an Alternative Transmission Strategy in a Parasitic Trematode 623 Progenesis and reduced virulence as an alternative transmission strategy in a parasitic trematode R.POULIN* Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand (Received 5 June 2001; revised 6 July 2001; accepted 7 July 2001) The complexity of the life-cycle of many parasitic helminths has driven the evolution of several well-documented adaptations serving to facilitate the completion of each difficult step in the cycle. In some trematode taxa, selection has even favoured the truncation of the life-cycle: progenetic larval stages (metacercariae) are capable of producing eggs inside their usual intermediate hosts, eliminating the need to be transmitted by predation to a definitive host. In some species, progenesis is shown by all individuals, whereas in other species both the normal and truncated life-cycles coexist in the same populations. Here, the strategies chosen by normal and progenetic metacercariae of the trematode Coitocaecum parvum are investigated and compared. Normal metacercariae, i.e. metacercariae that only develop into adults following ingestion by a suitable fish definitive host, were not capable of manipulating the behaviour of their amphipod intermediate host in ways that could facilitate their capture by fish. These metacercariae were associated with increased mortality in amphipods. Progenetic metacercariae, on the other hand, showed lower virulence levels than normal metacercariae. At the time of their death, amphipods harbouring progenetic metacercariae contained close to the maximum number of eggs that can be produced by progenetic metacercariae, suggesting that the parasite lowers its virulence to keep its host alive long enough to maximize egg output. The maintenance of the 2 strategies in the C. parvum population suggests that they may have equal fitness payoffs: progenesis and low virulence guarantee the production of at least some eggs, whereas the normal life-cycle and its associated higher virulence in the intermediate host provides a low probability of much higher fecundity. Key words: amphipod, Coitocaecum parvum, host manipulation, Paracalliope fluviatilis, truncated life-cycle. phenotype of their intermediate hosts such that their conspicuousness or vulnerability to predatory The life-cycle of many parasitic helminths consists definitive hosts is increased (Moore & Gotelli, 1990; of a series of unlikely events for which parasites have Combes, 1991; Poulin, 1995, 1998). Second, some evolved a range of adaptations (Poulin, 1998). For parasites adopt patience as their transmission strat- example, the complex life-cycle of a typical digenean egy, producing long-lived larval stages in their trematode involves 3 different host species and 3 intermediate hosts that can wait for rare acts of improbable transmission events (Kearn, 1998). First, predation, i.e. rare transmission opportunities microscopic miracidia hatched from eggs must locate (Poulin, 1998). and penetrate a suitable molluscan first intermediate In some systems, however, neither of the above host. Then, the cercariae that develop within the two strategies provides an advantage to the parasite. mollusc must leave this host to seek and infect the If the second intermediate host of a trematode is second intermediate host in the life-cycle. Finally, short-lived and if its risk of predation by a definitive encysted metacercariae within the second inter- host cannot be enhanced, then producing long-lived mediate host must be ingested by a suitable ver- metacercariae and the manipulation of the inter- tebrate definitive host for the parasite to become an mediate host’s phenotype are not features that will egg-producing adult. High adult fecundity and be favoured by selection. In these cases, deleting this asexual multiplication within the molluscan first transmission step from the life-cycle is one possible intermediate host are seen as adaptations serving to solution. Progenesis, or the precocious development counter the odds faced by the parasite during the of the reproductive system in juvenile stages, is first 2 transmission events (Poulin, 1998). The third observed in some taxa of parasitic helminths step in the cycle i.e., the ingestion of metacercariae (Combes, 1995; Kearn, 1998). Progenetic trema- by the definitive host, can be facilitated in at least 2 todes display a truncated life-cycle, in which the ways (Poulin, 1998). First, many parasitic helminths, second intermediate host also serves as definitive including trematodes, are capable of altering the host: cercariae infect this host and develop straight into adults. Usually, all members of a species are * Tel: j64 3 479 7983. Fax: j64 3 479 7584. E-mail: progenetic, and even all species within a mono- robert.poulin!stonebow.otago.ac.nz phyletic clade. The trematode family Schisto- Parasitology (2001), 123, 623–630. " 2001 Cambridge University Press DOI: 10.1017\S0031182001008794 Printed in the United Kingdom R. Poulin 624 somatidae is a good example of a taxon in which all life-cycle. In other trematode species using species display a derived 2-host life-cycle (Combes, amphipods as intermediate hosts, this is sometimes 1995). Progenesis occurs in other trematode taxa as solved by manipulation of amphipod behaviour to well. For instance, the trematode Aphalloides increase their susceptibility to predation by the coelomicola (Cryptogonimidae) also has an abbrevi- definitive host (e.g. Helluy, 1984; McCurdy, Forbes ated life-cycle: cercariae penetrate the skin of gobiid & Boates, 2000). Various factors may limit the fish, go through a metacercarial stage before potential effectiveness of host manipulation in the maturing into adults within the body cavity of the case of C. parvum. Its amphipod host, P. fluviatilis, fish (Maillard, 1973). As in other taxa, the progenetic is a small crustacean common in coastal lakes of New adult trematode is not located in the host’s gut, and Zealand. It feeds by grazing on epiphytic diatoms has no easy way of releasing its eggs in the external and fine detritus attached to macrophytic plants such environment. In the case of A. coelomicola, eggs can as Nitella spp. or the introduced Elodea canadensis. only reach the external aquatic habitat following the Two obvious features of its behaviour are its mild death and disintegration of the fish host. Recent photophobia, which keeps it in poorly-lit waters, and evidence suggests that A. coelomicola has evolved a its positive thigmotactism, i.e. its tendency to cling to level of virulence higher than that of related macrophytes or other substrates with only infrequent trematodes, and that it causes its host to die as a swimming bouts (Macfarlane, 1939). These means of achieving egg dispersal (Pampoulie et al. behavioural responses can serve to reduce the risk of 1999, 2000). Thus the adoption of progenesis and a predation on amphipods by small fish, and would be truncated life-cycle allows trematodes to skip an good targets for manipulation by parasites. However, improbable transmission event (the predation of an the densities of P. fluviatilis in coastal lakes are intermediate host by a definitive host), but it may extremely high (more than 15 individuals per litre; necessitate changes in how the parasite exploits its F. Wilhelm, personal communication), and fish host. predators ingest only a tiny fraction of the popu- An ideal system to address these issues would be lation. In addition, P. fluviatilis is short-lived one in which progenesis is facultative, i.e. only (! 1 year), and thus is only available to predators adopted by certain individuals in a trematode species for a short period of time, whether manipulated or while others go through the ‘normal’ 3-host 1ife- not. In such circumstances, host manipulation cycle. Coitocaecum parvum (Opecoelidae) is such a should be advantageous, but other strategies, such species (Macfarlane, 1939; Holton, 1984a). This as progenesis, may be even more advantageous. trematode uses the common freshwater snail Here, I investigate several questions relating to the Potamopyrgus antipodarum as its first intermediate use of progenesis as a transmission strategy of the host; cercariae produced asexually in snails then trematode C. parvum in the amphipod P. fluviatilis, encyst in the next intermediate host, the amphipod its second intermediate host. First, are either or both Paracalliope fluviatilis (Amphipoda: Eusiridae). normal and progenetic metacercariae capable of Normally, the life-cycle is completed when infected manipulating amphipod behaviour? Second, is the amphipods are eaten by suitable definitive hosts, occurrence of progenesis related to the size (or age) which include several fish species: bullies Gobio- of the amphipod host? Third, do normal and morphus spp. (Eleotridae), Galaxias spp. progenetic metacercariae show different levels of (Galaxiidae), and eels Anguilla spp. (Anguillidae). virulence (defined here as parasite-induced host However, progenetic metacercariae are commonly mortality) in amphipods? Fourth, since egg pro- found in amphipod intermediate hosts (Macfarlane, duction by progenetic metacercariae stops when 1939; Holton, 1984a). Progenetic metacercariae their amphipod host dies, is there evidence that these reproduce by self-fertilization within their cyst metacercariae accumulate eggs before causing any (trematodes are hermaphroditic); following the harm to the host? Taken together, answers to those death of their host, they excyst and the eggs (up to questions will allow the first test of progenesis as an 200 per worm; Macfarlane, 1939) they
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