Stage-dependent behavioural changes but early castration induced by the acanthocephalan parasite Polymorphus minutus in its Gammarus pulex intermediate host

SUMMARYMultidimensionality in parasite-induced phenotypic alterations (PIPA) has been observed in a large number of host–parasite associations, particularly in parasites with complex life cycles. However, it is still unclear whether such a syndrome is due to the successive activation of independent PIPAs, or results from the synchronous disruption of a single mechanism. The aim of the present study was to investigate the onset and progression of two PIPAs (a behavioural alteration: reversion of geotaxis, and castration) occurring in the crustacean amphipod Gammarus pulex infected with the acanthocephalan Polymorphus minutus, at different parasite developmental stages. Modifications of geotaxis in hosts differed according to the parasite developmental stage. Whereas the cystacanth stage induced a negative geotaxis (exposing the gammarid to predation by birds, the definitive hosts), the acanthella stage, not yet infective for the definitive host, induced a stronger positive geotaxis (presumably protecting gammarids from bird predation). In contrast, castration was almost total at the acanthella stage, with no significant variation in the intensity according to parasite maturation. Finally, no significant correlation was found between the intensity of behavioural changes and the intensity of castration. We discuss our results in relation with current views on the evolution of multidimensionality in PIPA.

Download Full-text

Culture of Protozoan Parasites

Clinical Microbiology Reviews ◽

10.1128/cmr.15.3.327-328.2002 ◽

2002 ◽

Vol 15 (3) ◽

pp. 327-328 ◽

Cited By ~ 25

Author(s):

Govinda S. Visvesvara ◽

Lynne S. Garcia

Keyword(s):

Strain Differences ◽

Life Cycle Stage ◽

Life Cycles ◽

In Vitro Cultivation ◽

Protozoan Parasites ◽

Complex Life Cycles ◽

Host Parasite Interactions ◽

Host Parasite

SUMMARY The in vitro culture of protozoan parasites involves highly complex procedures, which are subject to many variables. These parasites have very complex life cycles and, depending on the life cycle stage, may require different culture parameters. However, in vitro cultivation is important for many reasons, some of which include: diagnosis, antigen and antibody production, assessment of parasite immune modulating capabilities, drug screening, improvements in chemotherapy, differentiation of clinical isolates, determination of strain differences, vaccine production, development of attenuated strains, and the continued supply of viable organisms for studying host-parasite interactions.

Download Full-text

Developmental plasticity and the evolution of animal complex life cycles

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0268 ◽

2010 ◽

Vol 365 (1540) ◽

pp. 631-640 ◽

Cited By ~ 33

Author(s):

Alessandro Minelli ◽

Giuseppe Fusco

Keyword(s):

Life Cycle ◽

Developmental Plasticity ◽

Developmental Stages ◽

Ecological Condition ◽

Life Cycles ◽

Complex Life Cycle ◽

Complex Life Cycles ◽

Transcription Profiles ◽

Alternative Phenotypes ◽

Reproductive Events

Metazoan life cycles can be complex in different ways. A number of diverse phenotypes and reproductive events can sequentially occur along the cycle, and at certain stages a variety of developmental and reproductive options can be available to the animal, the choice among which depends on a combination of organismal and environmental conditions. We hypothesize that a diversity of phenotypes arranged in developmental sequence throughout an animal's life cycle may have evolved by genetic assimilation of alternative phenotypes originally triggered by environmental cues. This is supported by similarities between the developmental mechanisms mediating phenotype change and alternative phenotype determination during ontogeny and the common ecological condition that favour both forms of phenotypic variation. The comparison of transcription profiles from different developmental stages throughout a complex life cycle with those from alternative phenotypes in closely related polyphenic animals is expected to offer critical evidence upon which to evaluate our hypothesis.

Download Full-text

Proteomic Analysis of the Parasitic Cnidarian Ceratonova shasta (Cnidaria: Myxozoa) Reveals Diverse Roles of Actin in Motility and Spore Formation

Frontiers in Marine Science ◽

10.3389/fmars.2021.632700 ◽

2021 ◽

Vol 8 ◽

Author(s):

Vera Brekhman ◽

Maya Ofek-Lalzar ◽

Stephen D. Atkinson ◽

Gema Alama-Bermejo ◽

Keren Maor-Landaw ◽

...

Keyword(s):

Developmental Stages ◽

Mature Spore ◽

Life Cycles ◽

Fish Host ◽

Spore Formation ◽

Highly Pathogenic ◽

Complex Life Cycles ◽

Life Cycle Stages ◽

Waterborne Transmission ◽

Transmission Stage

Myxozoans are widely distributed aquatic obligate endoparasites that were recently recognized as belonging within the phylum Cnidaria. They have complex life cycles with waterborne transmission stages: resistant, infectious spores that are unique to myxozoans. However, little is known about the processes that give rise to these transmission stages. To understand the molecular underpinnings of spore formation, we conducted proteomics on Ceratonova shasta, a highly pathogenic myxozoan that causes severe mortalities in wild and hatchery-reared salmonid fishes. We compared proteomic profiles between developmental stages from inside the fish host, and the mature myxospore, which is released into the water where it drifts passively, ready to infect the next host. We found that C. shasta contains 2,123 proteins; representing the first proteomic catalog of a myxozoan myxospore. Analysis of proteins differentially expressed between developing and mature spore stages uncovered processes that are active during spore formation. Our data highlight dynamic changes in the actin cytoskeleton, which provides myxozoan developmental stages with mobility through lamellipodia and filopodia, whereas in the mature myxospore the actin network supports F-actin stabilization that reinforces the transmission stage. These findings provide molecular insight into the myxozoan life cycle stages and, particularly, into the process of sporogenesis.

Download Full-text

Parasite-modified behaviour in non-trophic transmission: trematode parasitism increases the attraction between snail intermediate hosts

Canadian Journal of Zoology ◽

10.1139/cjz-2019-0251 ◽

2020 ◽

Vol 98 (7) ◽

pp. 417-424

Author(s):

L.K. Eliuk ◽

S. Brown ◽

R.C. Wyeth ◽

J.T. Detwiler

Keyword(s):

Life Cycles ◽

Intermediate Hosts ◽

Free Swimming ◽

Complex Life Cycles ◽

Trophic Transmission ◽

Y Maze ◽

Second Intermediate Host ◽

Behavioural Experiments ◽

Lymnaea Elodes ◽

Host Parasite

Many parasites with complex life cycles cause host behavioural changes that increase the likelihood of transmission to the next host. Parasite modification is often found in trophic transmission, but its influence on non-trophic transmission is unclear. In trematodes, transmission from the first to second intermediate host is non-trophic, suggesting that free-swimming larvae (cercariae) emerging in closer proximity to the next host would have higher transmission success. We performed a series of behavioural experiments with echinostome trematodes and their snail hosts to determine if potential second hosts (ramshorn snail, genus Planorbella Haldeman, 1842) were more attracted to parasitized first hosts (marsh pondsnail, Lymnaea elodes Say, 1821). In a Y maze, a responding snail (Planorbella sp.) was placed in the base and its response to five treatments was assessed: no stimulus, turion duckweed (Lemna turionifera Landolt; a food item), non-parasitized L. elodes, parasitized L. elodes, and finally parasitized versus non-parasitized L. elodes. Snails showed some attraction to uninfected snails, but had a stronger response to infected first host snails. These results indicate that potential second host snails were more attracted to parasitized, heterospecific first host snails over non-parasitized heterospecific snails. This study demonstrates that echinostome trematodes alter snail behaviour by changing navigational choices in uninfected potential hosts through a chemical communication mechanism.

Download Full-text

The secretome of a parasite alters its host’s behaviour but does not recapitulate the behavioural response to infection

10.1101/799551 ◽

2019 ◽

Cited By ~ 1

Author(s):

Chloé Suzanne Berger ◽

Nadia Aubin-Horth

Keyword(s):

Gasterosteus Aculeatus ◽

Final Host ◽

Life Cycles ◽

Avian Host ◽

Allopatric Population ◽

Late Infection ◽

Intermediate Hosts ◽

Behavioural Changes ◽

Schistocephalus Solidus ◽

Host Parasite

ABSTRACTParasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its environment (the secretome), but this has rarely been assessed. We studied a non-cerebral parasite, the cestode Schistocephalus solidus, and its intermediate host, the threespine stickleback (Gasterosteus aculeatus), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only during late infection, when the worm is ready to reproduce in its final avian host. Sympatric host-parasite pairs show higher infection success for parasites, suggesting that the secretome effects could differ for allopatric host-parasite pairs with independent evolutionary histories. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting them in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours, but secretome from early infection resulted in more cautious hosts, only in fish from the allopatric population. Our results suggest that the secretome of Schistocephalus solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial, and that local adaptation between host-parasite pairs may extend to the response to the parasite’s secretome content.

Download Full-text

The secretome of a parasite alters its host's behaviour but does not recapitulate the behavioural response to infection

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.0412 ◽

2020 ◽

Vol 287 (1925) ◽

pp. 20200412 ◽

Cited By ~ 1

Author(s):

Chloé Suzanne Berger ◽

Nadia Aubin-Horth

Keyword(s):

Gasterosteus Aculeatus ◽

Final Host ◽

Life Cycles ◽

Avian Host ◽

Allopatric Population ◽

Late Infection ◽

Intermediate Hosts ◽

Behavioural Changes ◽

Host Parasite ◽

Host Behaviour

Parasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its environment (the secretome), but this has rarely been assessed. We studied a non-cerebral parasite, the cestode Schistocephalus solidus , and its intermediate host, the threespine stickleback ( Gasterosteus aculeatus ), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only during late infection, when the worm is ready to reproduce in its final avian host. Sympatric host–parasite pairs show higher infection success for parasites, suggesting that the secretome effects could differ for allopatric host–parasite pairs with independent evolutionary histories. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting them in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours, but secretome from early infection resulted in more cautious hosts, only in fish from the allopatric population. Our results suggest that the secretome of S. solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial and that local adaptation between host–parasite pairs may extend to the response to the parasite's secretome content.

Download Full-text

Behavioural and physiological effects of the trophically transmitted cestode parasite, Cyathocephalus truncatus, on its intermediate host, Gammarus pulex

Parasitology ◽

10.1017/s0031182007003228 ◽

2007 ◽

Vol 134 (12) ◽

pp. 1839-1847 ◽

Cited By ~ 16

Author(s):

N. FRANCESCHI ◽

T. RIGAUD ◽

Y. MORET ◽

F. HERVANT ◽

L. BOLLACHE

Keyword(s):

Behavioural Change ◽

Predation Rate ◽

Life Cycles ◽

Gammarus Pulex ◽

Intermediate Hosts ◽

Host Reaction ◽

Complex Life Cycles ◽

Cestode Parasite ◽

Behavioural Manipulation ◽

Pathogenic Effects

SUMMARYSome parasites with complex life-cycles are able to manipulate the behaviour of their intermediate hosts in a way that increases their transmission to the next host. Gammarids infected by the tapeworm Cyathocephalus truncatus (Cestoda: Spathebothriidea) are known to be more predated by fish than uninfected ones, but potential behavioural manipulation by the parasite has never been investigated. In this study, we tested the hypothesis that C. truncatus is able to manipulate the behaviour of one of its intermediate hosts, Gammarus pulex (Crustacea: Amphipoda). To assess if any behavioural change was linked to other phenotypic alterations, we also measured the immunity of infected and uninfected individuals and investigated the pathogenic effects of the parasite. Infected gammarids were significantly less photophobic than uninfected ones, but no effect of infection on the level of immune defence was found. The results on survival, swimming activity and oxygen consumption suggest that the parasite also has various pathogenic effects. However, the alteration in host phototaxis was not correlated to some of these pathogenic effects. Therefore, we propose that the modification in host reaction to light is a behavioural manipulation, explaining the previously observed increase of gammarid predation rate.

Download Full-text

Variation and covariation in infectivity, virulence and immunodepression in the host–parasite association Gammarus pulex – Pomphorhynchus laevis

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2009.1299 ◽

2009 ◽

Vol 276 (1676) ◽

pp. 4229-4236 ◽

Cited By ~ 12

Author(s):

Stéphane Cornet ◽

Nathalie Franceschi ◽

Loïc Bollache ◽

Thierry Rigaud ◽

Gabriele Sorci

Keyword(s):

Immune Response ◽

Genetic Variation ◽

Host Immunity ◽

Gammarus Pulex ◽

Pomphorhynchus Laevis ◽

Host Mortality ◽

Host Parasite ◽

Acanthocephalan Parasite ◽

The Relationship ◽

Immune Depression

Parasites often manipulate host immunity for their own benefit, either by exacerbating or suppressing the immune response and this may directly affect the expression of parasite virulence. However, genetic variation in immunodepression, which is a prerequisite to its evolution, and the relationship between immunodepression and virulence, have rarely been studied. Here, we investigated the variation among sibships of the acanthocephalan parasite, Pomphorhynchus laevis , in infecting and in immunodepressing its amphipod host, Gammarus pulex . We also assessed the covariation between infectivity, parasite-induced immune depression and host mortality (parasite virulence). We found that infectivity, the intensity of immunodepression and virulence were variable among parasite sibships. Infectivity and the level of immunodepression were not correlated across parasite sibships. Whereas infectivity was unrelated to host mortality, we found that gammarids that were exposed to the parasite sibships that immunodepressed their hosts the most survived better. This positive covariation between host survival and immunodepression suggests that gammarids exposed to the less immunodepressive parasites could suffer from damage imposed by a higher activity of the phenoloxidase.

Download Full-text

Pairing success and sperm reserve of male Gammarus pulex infected by Cyathocephalus truncatus (Cestoda: Spathebothriidea)

Parasitology ◽

10.1017/s0031182011001247 ◽

2011 ◽

Vol 138 (11) ◽

pp. 1429-1435 ◽

Cited By ~ 6

Author(s):

MATTHIAS GALIPAUD ◽

ZOÉ GAUTHEY ◽

LOÏC BOLLACHE

Keyword(s):

Mate Guarding ◽

Potential Effect ◽

Life Cycles ◽

Mating Strategies ◽

Gammarus Pulex ◽

Physiological Changes ◽

Sperm Number ◽

Intermediate Hosts ◽

Complex Life Cycles ◽

Rival Male

SUMMARYManipulative parasites with complex life cycles are known to induce behavioural and physiological changes in their intermediate hosts. Cyathocephalus truncatus is a manipulative parasite which infects Gammarus pulex as intermediate host. G. pulex males display pre-copulatory mate guarding as a response to male-male competition for access to receptive females. In this paper, we tested the influence that C. truncatus-infection might have on male G. pulex sperm number and pairing success. We considered 3 classes of G. pulex males in our experiments: (i) uninfected males found paired in the field, (ii) uninfected males found unpaired in the field, or (iii) infected males found unpaired in the field. Both infected males and uninfected unpaired males paired less with a new female than uninfected paired males did. Furthermore, infected males appear to be at a strong disadvantage when directly competing for females with a healthy rival male, and had fewer sperm in their testes. We discuss the potential effect of male and female mating strategies on such male host mating alteration.

Download Full-text