Larval size in acanthocephalan parasites: Influence of intraspecific competition and effects on intermediate host behavioural changes

Abstract

BackgroundParasites often face a trade-off between exploitation of host resources and transmission probabilities to the next host. In helminths, larval growth, a major component of adult parasite fitness, is linked to exploitation of intermediate host resources and is influenced by the presence of co-infecting conspecifics. In manipulative parasites, larval growth strategy could also interact with their ability to alter intermediate host phenotype and influence parasite transmission.MethodsWe used experimental infections of Gammarus pulex by Pomphorhynchus laevis (Acanthocephala), to investigate larval size effects on host behavioural manipulation among different parasite sibships and various degrees of intra-host competition.ResultsIntra-host competition reduced mean P. laevis cystacanth size, but the largest cystacanth within a host always reached the same size. Therefore, all co-infecting parasites did not equally suffer from intraspecific competition. Under no intra-host competition (1 parasite per host), larval size was positively correlated with host phototaxis. At higher infection intensities, this relationship disappeared, possibly because of strong competition for host resources, and thus larval growth, and limited manipulative abilities of co-infecting larval acanthocephalans.ConclusionsOur study indicates that behavioural manipulation is a condition-dependant phenomenon that needs the integration of parasite-related variables to be fully understood.

Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition?

“…For example, parasite size, gender, age, and genotype, as well as host genotype, can influence host modification. Recently, Dianne et al (2012) proposed that competition among parasites that share a host could potentially influence host modification if it constrains the amount of resources that are available to allocate to manipulation. This type of mechanism could explain the intensity-related effect on behavior modification identified in the current study if both host sharing and host manipulation are costly to the A. dirus parasites.…”

Multidimensionality of Modification in an Isopod-Acanthocephalan System

“…A change in the strategy of manipulation may be expected if host manipulation is energetically costly and if the competitive interactions influence the amount of resources each parasite has available to allocate to manipulation (Dianne et al, 2012;Caddigan et al, 2014Caddigan et al, , 2017. Previous research on the population studied here has shown that mating behavior is suppressed in infected male C. intermedius relative to uninfected males and that this suppression is less likely to occur at higher parasite intensities, i.e., when intraspecific competition is more intense (Caddigan et al, 2014).…”

“…Numerous studies have shown that host sharing can impact parasite development, growth, body size, and energy content, and that each of these factors has the potential to influence trait modification (Read and Phifer, 1959;Roberts, 2000;Dezfuli et al, 2001;Sparkes et al, 2004Sparkes et al, , 2006Benesh and Valtonen, 2007a;Franceschi et al, 2008Franceschi et al, , 2010Benesh et al, 2009a;Dianne et al, 2010Dianne et al, , 2012Caddigan et al, 2014Caddigan et al, , 2017. If competitive interactions among parasites influence the patterns of development, growth, and energy allocation, and if manipulation is costly, then parasites may benefit by adopting strategies that balance the conflicting demands associated with their own growth, and development with those that are associated with host manipulation (e.g., Poulin, 1994a;Parker et al, 2003;Thomas et al, 2005Thomas et al, , 2011Michaud et al, 2006;Ball et al, 2008;Franceschi et al, 2010;Maure et al, 2013).…”

The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms

“…They then tested their model experimentally by altering the duration of infection in the copepod, and found immature S. solidus actively suppressed copepod activity, reducing the likelihood of premature fish predation (and death of the immature parasites); however, when S. solidus reached the next developmental stage and required transmission to the second intermediate (fish) host, they increased copepod activity and the likelihood of predation (Hammerschmidt et al, 2009). Similarly, Dianne et al (2012) demonstrated that the Amphipod, Gammarus pulex, exhibited stronger anti-predator behaviour (that is, was more likely to hide in predator refuges) when infected with immature stages of the acanthocephalan Pomphorhynchus laevis, than when uninfected. Once P. laevis had reached maturity within its G. pulex host, this anti-predator behaviour decreased and infected G. pulex were significantly more likely to experience predation by the definitive host, the brown trout, Salmo trutta.…”

“…Parasite growth (or asexual replication) is often lower when within-host competition is high (for both SLPs and CLPs). CLP coinfections (multi-genotype infections) in intermediate hosts occur in many but not all helminth taxa, and when they do occur (either naturally or experimentally), competition leads to clear parasite fitness reductions (De Roode et al, 2005;Bell et al, 2006;Jäger and Schjørring, 2006;Michaud et al, 2006;Lagrue and Poulin, 2008;Balmer et al, 2009;Cornet, 2011;Dianne et al, 2012). However, sexually reproducing parasites often benefit from being in genotypically diverse infections, because they can acquire genetically dissimilar mates (Brown et al, 2001) and thus reduce the incidence of inbreeding and the associated fitness costs.…”