Impacts of a newly identified behaviour-altering trematode on its host amphipod: from the level of gene expression to population

Guler, Yasmin; Short, Stephen; Etxabe, Amaia Green; Sherhod, Christopher M.; Kille, Peter; Ford, Alex T.

doi:10.1017/s0031182015000918

Cited by 12 publications

(10 citation statements)

References 72 publications

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“…Several parasites bring about phenotypic alterations in their hosts that appear to increase their own fitness at the expense of that of their hosts (Poulin, ; Moore, ; Thomas, Adamo, & Moore, ; Cézilly & Perrot‐Minnot, ). Such parasite‐induced phenotypic alterations (PIPAs) can take different forms, through affecting, for instance, the physiology (Plaistow, Troussard, & Cézilly, ; Tain, Perrot‐Minnot, & Cezilly, ; Perrot‐Minnot & Cezilly, ; Guler et al ., ; Kopp et al ., ; Perrot‐Minnot, Maddaleno, & Cézilly, ), reproduction (Bollache, Gambade, & Cézilly, ; Bollache, Rigaud, & Cézilly, ; Rauque & Semenas, ; Bollache, ) or appearance (Lewis Jr, ; Camp & Huizinga, ; Oetinger & Nickol, ; Amato et al ., ; Wesołowska & Wesołowski, ) of infected hosts. However, most studies of PIPA concern the altered behaviour of host species.…”

Section: Introductionmentioning

confidence: 99%

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

et al. 2020

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Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta‐analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite‐induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro‐habitat and the anti‐predation behaviour of infected hosts, and by promoting energy‐saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host–parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of par...

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Section: Introductionmentioning

confidence: 99%

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

et al. 2020

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“…These results have implications for the understanding of the ecology of a priority species under the biodiversity action plan, and more widely the ecology of saline lagoon systems. For example, at an estuarine site in close proximity to Gilkicker high levels of infection by trematode metacercariae had a detrimental effect on the overall population size of Echinogammarus marinus (Guler et al ., 2015). While our study did not find major detrimental effects on the population there were effects at the individual level.…”

Section: Discussionmentioning

confidence: 99%

Infection with cerebral metacercariae of microphallid trematode parasites reduces reproductive output in the gammarid amphipodGammarus insensibilis(Stock 1966) in UK saline lagoons

et al. 2017

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Saline lagoons are priority habitats in the United Kingdom supporting several protected specialist species. One specialist, the amphipodGammarus insensibilis, is infected with behaviour-altering microphallid trematodes such asMicrophallus papillorobustus. In saline lagoons around the coast of England (Gilkicker and Lymington–Keyhaven on the Hampshire coast and Moulton Marsh in Lincolnshire) there is variation in the prevalence of this parasite in the gammarid populations (0 at Salterns in the Lymington–Keyhaven lagoon system to 98% at Gilkicker). Infection intensity ranged from 0 to 20 metacercariae in individual amphipods. Higher infection intensity can alter the shape of the amphipod's head. Under experimental conditions respiration rate is significantly reduced in infected animals and reproductive output (expressed as early stage embryos mg g dry weight−1) is significantly lower in infected females. It is important to consider the role of host–parasite interactions in order to understand the ecology of specialist lagoon species such asG. insensibilisand their lagoon habitats.

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“…Females have brood plates (oostigites) whilst males have genital papillae. Any specimens which appeared to be parasitized with behavioral altering trematodes were excluded from the analysis (Guler et al, 2015).…”

Section: Methodology Specimen Collection and Husbandrymentioning

confidence: 99%

Sex Specific Differences Recorded in the Behavior of an Amphipod: Implications for Behavioral Toxicology

2020

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Behavior is a useful endpoint in ecotoxicological research; it links the biochemical effects of contamination with physiology of individuals, which can be applied to higher levels of organization with relevance to ecology. Animals exhibit species-specific and sex specific behaviors. Previous experiments within ecotoxicology using amphipods as models have either not separated by sex or have on the assumption that they may create more variability in the results. Therefore, the objectives of this study were to investigate the effect of time (which controlled light conditions), sex, and the interaction of time and sex on the swimming velocity in males and females of the marine amphipod Echinogammarus marinus. E. marinus exhibited a phototactic response to light, as is consistent with previous findings. It was determined that females swim significantly faster than males and that this response was enhanced during periods when the lights were switched off. This suggests that a greater understanding of the baseline unconditioned behaviors of experimental organisms is needed to avoid impacts of unknown variables on results. The results of this study reveal significant sexual differences in the baseline behavior of E. marinus which has implications for future research in ecotoxicology. It is recommended that in future research specimens be separated by sex prior to experimentation, in order to account for possible behavioral differences such as those observed in the present studies. This study also highlights the need for thorough observation of behavior over shorter time intervals as larger intervals may miss short-term variations.

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Impacts of a newly identified behaviour-altering trematode on its host amphipod: from the level of gene expression to population

Cited by 12 publications

References 72 publications

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Infection with cerebral metacercariae of microphallid trematode parasites reduces reproductive output in the gammarid amphipodGammarus insensibilis(Stock 1966) in UK saline lagoons

Sex Specific Differences Recorded in the Behavior of an Amphipod: Implications for Behavioral Toxicology

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