Life cycle abbreviation in trematode parasites and the developmental time hypothesis: is the clock ticking?

Abstract

The typical multi‐host life cycle of many parasites, although conferring several advantages, presents the parasites with a highly hazardous transmission route. As a consequence, parasites have evolved various adaptations increasing their chances of transmission between the different hosts of the life cycle. Some trematode species like the opecoelid Coitocaecum parvum have adopted a more drastic alternative strategy whereby the definitive host is facultatively dropped from the cycle, resulting in a shorter, hence easier to complete, life cycle. Like other species capable of abbreviating their life cycle, C. parvum does so through progenetic development within its intermediate host. Laboratory‐reared C. parvum can modulate their developmental strategy inside the second intermediate host according to current transmission opportunities, though this ability is not apparent in natural C. parvum populations. Here we show that this difference is likely due to the time C. parvum individuals spend in their intermediate hosts in the natural environment. Although transmission opportunities, i.e. chemical cues of the presence of definitive hosts, promoted the adoption of a truncated life cycle in the early stages of infection, individuals that remained in their amphipod host for a relatively long time had a similar probability of adopting progenesis and the abbreviated cycle, regardless of the presence or absence of chemical cues from the predator definitive host. These results support the developmental time hypothesis which states that parasites capable of facultative life cycle abbreviation should eventually adopt progenesis regardless of transmission opportunities, and provide further evidence of the adaptive plasticity of parasite transmission strategies.

Genetic structure and host-parasite co-divergence: evidence for trait-specific local adaptation

“…Coitocaecum parvum cercariae were obtained from naturally infected snails under controlled conditions to standardize time between the release of cercariae from the snail and exposure to the amphipod host (Lagrue, Poulin & Keeney, ). That delay was also kept to a minimum (< 20 min) as C. parvum cercariae have a limited life span (~ 5 h; Lagrue & Poulin, , ). Infected snails were transferred from the stock tank to Petri dishes (around 50 haphazardly‐chosen snails per dish) filled with water and then incubated at 25 °C for 20 min under constant light, conditions that induce cercarial release (Lagrue & Poulin, , ).…”

“…amphipod hosts (Bryan‐Walker, Leung & Poulin, ). Surviving metacercariae also attain widely different sizes in amphipod hosts (Lagrue & Poulin, ). Since C. parvum size influences fecundity, larger metacercariae should achieve higher fitness (Lagrue & Poulin, , ).…”

A case of a facultative life-cycle diversification in the fluke Pleurogenoides sp. (Lecithodendriidae, Plagiorchiida)

“…A subsequent transmission of the precocious larva put the life-cycle simply back on track -as observed in our Bush Viper case. Th is hypothesis explains the cases of facultative progenesis in a fl uke species infecting an intermediate host that outlive the parasite [15], which seems to be an appropriate fi ction in case of perennial water frogs.…”

“…Th is also accounts for predation rates so low that the predator might as well be almost completely absent to a parasite larva waiting inside a prey [14]. Waiting stages, especially the metacercarial stage, are generally seen as a sophisticated addition in the evolution of a fl uke life-cycle, enhancing the chances of transmission to a consecutive, but rare host [15].…”

Alternative parasite development in transmission strategies: how time flies!

“…Developmental plasticity, which is the ability of individual genotypes to produce alternative phenotypes depending on environmental conditions (see West‐Eberhard, 1989; Piersma & Drent, 2003), has been well documented within parasitic plathyhelminths with complex life cycles. Some digenean species can trigger precocious maturation through progenesis within the intermediate host in order to cope with the lack of transmission opportunities towards their definitive host in variable ecosystems (Lefebvre & Poulin, 2005b; Lagrue & Poulin, 2009). However, all modifications in the completion of life cycles may have drawbacks which can perturb the dynamic equilibrium of the resulting host–parasite systems (Lefebvre & Poulin, 2005b).…”