Lack of seasonal variation in the life-history strategies of the trematode Coitocaecum parvum: No apparent environmental effect

Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand.
Parasitology (Impact Factor: 2.56). 10/2008; 135(10):1243-51. DOI: 10.1017/S0031182008004782
Source: PubMed


Parasites with complex life cycles have developed numerous and very diverse adaptations to increase the likelihood of completing this cycle. For example, some parasites can abbreviate their life cycles by skipping the definitive host and reproducing inside their intermediate host. The resulting shorter life cycle is clearly advantageous when definitive hosts are absent or rare. In species where life-cycle abbreviation is facultative, this strategy should be adopted in response to seasonally variable environmental conditions. The hermaphroditic trematode Coitocaecum parvum is able to mature precociously (progenesis), and produce eggs by selfing while still inside its amphipod second intermediate host. Several environmental factors such as fish definitive host density and water temperature are known to influence the life-history strategy adopted by laboratory raised C. parvum. Here we document the seasonal variation of environmental parameters and its association with the proportion of progenetic individuals in a parasite population in its natural environment. We found obvious seasonal patterns in both water temperature and C. parvum host densities. However, despite being temporally variable, the proportion of progenetic C. parvum individuals was not correlated with any single parameter. The results show that C. parvum life-history strategy is not as flexible as previously thought. It is possible that the parasite's natural environment contains so many layers of heterogeneity that C. parvum does not possess the ability to adjust its life-history strategy to accurately match the current conditions.

    • "It is thought that populations of Corophium amphipods infected with trematodes are prone to local collapse due to the capacity of its parasites to induce behavioural change (Damsgaard et al. 2005), and our findings are certainly consistent with the hypothesis that trematodes can have a major impact on amphipod populations. In addition, we found no significant relationship between trematode abundance and any recorded environmental parameter, a finding also consistent with other trematode and host population studies (Lagrue and Poulin, 2008). The large fluctuations in the prevalence of trematode infection possibly reflect a build-up of individuals infected with trematode cysts undergoing a period of development prior to reaching the infective stage, after which the parasite manipulates its host in an attempt to complete its life cycle. "
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    ABSTRACT: Changes to host behaviour induced by some trematode species, as a means of increased trophic transmission, represents one of the seminal examples of host manipulation by a parasite. The amphipod Echinogammarus marinu s (Leach, 1815) is infected with a previously undescribed parasite, with infected individuals displaying positive phototaxic and negative geotaxic behaviour. This study reveals that the unknown parasite encysts in the brain, nerve cord and the body cavity of E. marinus , and belongs to the Microphallidae family. An 18 month population study revealed that host abundance significantly and negatively correlated with parasite prevalence. Investigation of the trematode's influence at the transcriptomic level revealed genes with putative neurological functions, such as serotonin receptor 1A, an inebriated-like neurotransmitter, tryptophan hydroxylase and amino acid decarboxylase, present consistent altered expression in infected animals. Therefore, this study provides one of the first transcriptomic insights into the neuronal gene pathways altered in amphipods infected with a trematode parasite associated with changes to its host's behaviour and population structure.
    No preview · Article · Aug 2015 · Parasitology
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    • "This facultative strategy allows an individual to bypass the definitive host by producing viable eggs at the metacercarial stage, while still inside the intermediate host, thereby truncating the life cycle to just two hosts. Although anywhere between 10 and 50% of individuals of these species can be progenetic in samples from the field (Lagrue and Poulin, 2008a; Herrmann and Poulin, 2011), they can nonetheless continue their life and possibly achieve greater egg production if ingested by their definitive host. Thus their inclusion in estimates of potential trophic transmission bottlenecks is justified. "
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    ABSTRACT: The fundamental assumption underpinning the evolution of numerous adaptations shown by parasites with complex life cycles is that huge losses are incurred by infective stages during certain transmission steps. However, the magnitude of transmission losses or changes in the standing crop of parasites passing from upstream (source) to downstream (target) hosts have never been quantified in nature. Here, using data from 100 pairs of successive upstream–downstream life stages, from distinct populations representing 10 parasite species, we calculated the total density per m 2 of successive life stages. We show that clonal amplification of trematodes in their first intermediate host leads to an average 4-fold expansion of numbers of individuals at the next life stage, when differences in the longevity of successive life stages are taken into account. In contrast, trophic transmission to the definitive host results in almost no numerical change for trematodes, but possibly in large decreases for acanthocephalans and nematodes, though a correction for longevity was not possible for the latter groups. Also, we only found a positive association between upstream and downstream stage densities for transmission involving free-swimming cercariae in trematodes, suggesting a simple output-recruitment process. For trophic transmission, there was no coupling between downstream and upstream parasite densities. These first quantitative estimates of ontogenetic rises and falls in numbers under natural conditions provide new insights into the selective pressures acting on parasites with complex cycles.
    Full-text · Article · Jan 2015 · Parasitology
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    • "Adoption of progenesis by metacercariae is influenced by numerous external factors in addition to definitive host presence in the environment. For example, because progenetic metacercariae grow much larger than nonprogenetic ones and thus require more resources, intrahost competition with other parasite species and amphipod host size also influence whether or not progenesis is adopted (Lagrue & Poulin, 2008a; Ruiz Daniels et al., 2012). The developmental plasticity offered by progenesis could also allow parasites to adjust life strategies according to specific contexts, including genetic relatedness between individual parasites sharing the same host. "
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    ABSTRACT: For conspecific parasites sharing the same host, kin recognition can be advantageous when the fitness of one individual depends on what another does; yet, evidence of kin recognition among parasites remains limited. Some trematodes, like Coitocaecum parvum, have plastic life cycles including two alternative life-history strategies. The parasite can wait for its intermediate host to be eaten by a fish definitive host, thus completing the classical three-host life cycle, or mature precociously and produce eggs while still inside its intermediate host as a facultative shortcut. Two different amphipod species are used as intermediate hosts by C. parvum, one small and highly mobile and the other larger, sedentary, and burrow dwelling. Amphipods often harbour two or more C. parvum individuals, all capable of using one or the other developmental strategy, thus creating potential conflicts or cooperation opportunities over transmission routes. This model was used to test the kin recognition hypothesis according to which cooperation between two conspecific individuals relies on the individuals' ability to evaluate their degree of genetic similarity. First, data showed that levels of intrahost genetic similarity between co-infecting C. parvum individuals differed between host species. Second, genetic similarity between parasites sharing the same host was strongly linked to their likelihood of adopting identical developmental strategies. Two nonexclusive hypotheses that could explain this pattern are discussed: kin recognition and cooperation between genetically similar parasites and/or matching genotypes involving parasite genotype-host compatibility filters.
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