The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host

Beros, Sara; Jongepier, Evelien; Hagemeier, Felizitas; Foitzik, Susanne

doi:10.1098/rspb.2015.1473

Cited by 26 publications

(48 citation statements)

References 42 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Indeed, they are even more often fed and survive longer than unparasitized workers (Beros et al . ). Behavioural changes extend to all workers from parasitized colonies.…”

Section: Introductionmentioning

confidence: 97%

See 1 more Smart Citation

Gene expression patterns underlying parasite‐induced alterations in host behaviour and life history

et al. 2016

Self Cite

View full text Add to dashboard Cite

Many parasites manipulate their hosts' phenotype. In particular, parasites with complex life cycles take control of their intermediate hosts' behaviour and life history to increase transmission to their definitive host. The proximate mechanisms underlying these parasite-induced alterations are poorly understood. The cestode Anomotaenia brevis affects the behaviour, life history and morphology of parasitized Temnothorax nylanderi ants and indirectly of their unparasitized nestmates. To gain insights on how parasites alter host phenotypes, we contrast brain gene expression patterns of T. nylanderi workers parasitized with the cestode, their unparasitized nestmates and unparasitized workers from unparasitized colonies. Over 400 differentially expressed genes between the three groups were identified, with most uniquely expressed genes detected in parasitized workers. Among these are genes that can be linked to the increased lifespan of parasitized workers. Furthermore, many muscle (functionality) genes are downregulated in these workers, potentially causing the observed muscular deformations and their inactive behaviour. Alterations in lifespan and activity could be adaptive for the parasite by increasing the likelihood that infected workers residing in acorns are eaten by their definitive host, a woodpecker. Our transcriptome analysis reveals numerous gene expression changes in parasitized workers and their uninfected nestmates and indicates possible routes of parasite manipulation. Although causality still needs to be established, parasite-induced alterations in lifespan and host behaviour appear to be partly explained by morphological muscle atrophy instead of central nervous system interference, which is often the core of behavioural regulation. Results of this study will shed light upon the molecular basis of antagonistic species interactions.

show abstract

“…Indeed, they are even more often fed and survive longer than unparasitized workers (Beros et al . ). Behavioural changes extend to all workers from parasitized colonies.…”

Section: Introductionmentioning

confidence: 97%

“…Moreover, these workers are mainly inactive and remain in the nest, even when disturbed (Beros et al . )—a behaviour that could increase parasite transmission to the definitive woodpecker host, which is known to feed on wood‐boring insects and acorns. Despite their deviant chemical profile (Trabalon et al .…”

Section: Introductionmentioning

confidence: 99%

Gene expression patterns underlying parasite‐induced alterations in host behaviour and life history

et al. 2016

Self Cite

View full text Add to dashboard Cite

show abstract

“…For a parasite that manipulates the host to bite leaves before using the host cadaver as a platform for transmission, the permanence of a leaf as a platform may impact its fitness. Although there are other parasites that manipulate ant behavior, including other fungi (Boer 2008), cestodes (Beros et al 2015), nematodes (Poinar and Yanoviak 2008), trematodes (Krull and Mapes 1952;Carney 1969), and flies (Henne and Johnson 2007), none of them have been as extensively studied as the zombie ants. This deeper understanding of the biology implies the zombie ant system may be a more suitable model for studying how environmental variation affects the behavioral manipulation of hosts by parasites.…”

mentioning

confidence: 99%

Evidence for convergent evolution of host parasitic manipulation in response to environmental conditions

et al. 2018

View full text Add to dashboard Cite

Environmental conditions exert strong selection on animal behavior. We tested the hypothesis that the altered behavior of hosts due to parasitic manipulation is also subject to selection imposed by changes in environmental conditions over time. Our model system is ants manipulated by parasitic fungi to bite onto vegetation. We analyzed the correlation between forest type (tropical vs. temperate) and the substrate where the host bites (biting substrate: leaf vs. twigs), the time required for the fungi to reach reproductive maturity, and the phylogenetic relationship among specimens from tropical and temperate forests from different parts of the globe. We show that fungal development in temperate forests is longer than the period of time leaves are present and the ants are manipulated to bite twigs. When biting twigs, 90% of the dead ants we examined had their legs wrapped around twigs, which appears to provide better attachment to the plant. Ancestral state character reconstruction suggests that leaf biting is the ancestral trait and that twig biting is a convergent trait in temperate regions of the globe. These three lines of evidence suggest that changes in environmental conditions have shaped the manipulative behavior of the host by its parasite.

show abstract

“…Insecta; Formicidae (Temnothorax nylanderi) Behavior (Beros et al, 2015) Aves; Picidae (Dendrocopos major, Dendrocopos minor) No reports…”

Section: Anomotaenia Brevismentioning

confidence: 99%

Kindness to the Final Host and Vice Versa: A Trend for Parasites Providing Easy Prey?

Øverli

Johansen

2019

Front. Ecol. Evol.

View full text Add to dashboard Cite

Traditionally the "extended phenotype" concept refers to parasites that manipulate host phenotype to increase parasite fitness. This includes parasites that render intermediate hosts more susceptible to predation by final hosts. We explore here the proposition that an evolutionary driver in such cases is the energetic benefit to the final host, in addition to increased parasite fitness. We will review some well-established host-manipulation models, where such a scenario seems likely. One example is provided by the protozoan Toxoplasma gondii, which conspicuously impairs predator avoidance in rodents. Pathologies in humans that acquire T. gondii are known, but infection in adult feline definitive hosts are most commonly asymptomatic and apparently innocuous. In another well-documented case of parasite-mediated trophic transmission, trematode (Euhaplorchis californiensis) infected killifish (Fundulus parvipinnis) abandon normal caution and exhibit a range of behaviors which makes them more conspicuous to predatory birds. The birds get a free meal, but the presence of adult trematodes in the gut would seem to incur few if any negative consequences for the birds. There are exceptions to this pattern also among cases of parasite mediated trophic transmission, but major pathology in definitive hosts seems for the most part restricted to cases where manipulated intermediate hosts are of minor energetic importance. Current theories for the evolution of reduced pathogenicity in predatory final hosts primarily focus on parasites minimizing pathogenicity to increase their own reproductive output and/or avoid selection on host preference for non-infected prey types. Here we advocate another alternative: If or when the benefit of increased prey acquisition outweighs pathogenicity or resource drain, there should be little or no selection on final hosts to minimize parasite infections. This means that not only will host avoidance of infection not develop, but the molecular arms race for increased immunological defense will also likely be halted in such cases.

show abstract

The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host

Cited by 26 publications

References 42 publications

Gene expression patterns underlying parasite‐induced alterations in host behaviour and life history

Gene expression patterns underlying parasite‐induced alterations in host behaviour and life history

Evidence for convergent evolution of host parasitic manipulation in response to environmental conditions

Kindness to the Final Host and Vice Versa: A Trend for Parasites Providing Easy Prey?

Contact Info

Product

Resources

About