Transcriptomics of an extended phenotype: parasite manipulation of wasp social behaviour shifts expression of caste-related genes

Geffre, Amy; Liu, Ruolin; Manfredini, Fabio; Beani, L.; Kathirithamby, Jeyaraney; Grozinger, Christina M.; Toth, Amy L.

doi:10.1098/rspb.2017.0029

Cited by 32 publications

(32 citation statements)

References 48 publications

(77 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Indeed, two recent studies suggest that extracellular parasites can have wide reaching impact on their host's genome (Feldmeyer et al, 2016;Geffre et al, 2017), suggesting gene regulation is a key factor in host manipulation. While in both cases compelling evidence is provided for potential gene-induced behavioral manipulation, the researchers could only establish correlation and not causation for the effect of gene regulation on host behavior.…”

Section: Genomic Manipulationmentioning

confidence: 99%

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

Herbison

2017

Front. Ecol. Evol.

View full text Add to dashboard Cite

Scientific and public interest in host manipulation by parasites has surged over the past few decades, resulting in an exponential growth of cases where potential behavioral manipulation has been identified. However, these studies dwarf the number of genuine attempts to elucidate the mechanistic processes behind this behavioral manipulation. Ultimately, this imbalance has slowed progress in the study of the mechanisms underlying host manipulation. As it stands, research suggests that the mechanisms of host manipulation fall into three categories: immunological, genomic/proteomic and neuropharmacological, and forth potential category: symbioant-mediated manipulation. After exploration of the literature pertaining to these four pathways, four major trends become evident. First and foremost, there is a severe disconnect between the observed molecular and behavioral shifts in a parasitized host. Indeed, very rarely a study demonstrates that molecular changes observed in a host are the result of active manipulation by the resident parasite, or that these molecular changes directly result in behavioral manipulation that increases the parasite's fitness. Secondly, parasites may often employ multiple pathways in unison to achieve control over their hosts. Despite this, current scientific approaches usually focus on each manipulation pathway in isolation rather than integrating them. Thirdly, the relative amount of host-parasite systems yet to be investigated in terms of molecular manipulation is staggering. Finally, as a result of the aforementioned trends, guiding mechanisms or principles for the multiple types of behavioral manipulation are yet to be found. Researchers should look to identify the manipulative factors required to generate the molecular changes seen in hosts, while also considering the "multi-pronged" approach parasites are taking to manipulate behavior. Assessing gene expression and its products during transitional periods in parasites may be a key methodological approach for tackling these recent trends in the host manipulation literature.

show abstract

Section: Genomic Manipulationmentioning

confidence: 99%

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

Herbison

2017

Front. Ecol. Evol.

View full text Add to dashboard Cite

show abstract

“…Future research will be required to identify whether these genes were directly impacted by the parasite, or represent biomarkers of nontarget processes affected indirectly by infection. Our findings provide additional support for the use of genomic tools for exploring the molecular mechanisms within host–parasite interactions whereby changes within host transcription may be signatures of ‘extended phenotypes’, the mechanisms underlying which are increasingly being explored within insect systems (eg Biron et al ., ; Geffre et al ., ). Our understanding of the S .…”

Section: Discussionmentioning

confidence: 99%

“…e-mail: mark.brown@rhul.ac.uk with the nematomorph Spinochordodes tellinii (Biron et al, 2005), and induced hydrophilic behaviour to enable completion of the parasite life-cycle, which resulted in host death through drowning (Thomas et al, 2002). High throughput transcriptomics has similarly uncovered genes underlying complex altered host phenotypes in response to parasite infections (de Bekker et al, 2015;Geffre et al, 2017;Guo et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

Colgan

Carolan

Sumner

et al. 2019

Insect Molecular Biology

View full text Add to dashboard Cite

Parasitism can result in dramatic changes in host phenotype, which are themselves underpinned by genes and their expression. Understanding how hosts respond at the molecular level to parasites can therefore reveal the molecular architecture of an altered host phenotype. The entomoparasitic nematode Sphaerularia bombi is a parasite of bumblebee (Bombus) hosts where it induces complex behavioural changes and host castration. To examine this interaction at the molecular level, we performed genome‐wide transcriptional profiling using RNA‐Sequencing (RNA‐Seq) of S. bombi‐infected Bombus terrestris queens at two critical time‐points: during and just after overwintering diapause. We found that infection by S. bombi affects the transcription of genes underlying host biological processes associated with energy usage, translation, and circadian rhythm. We also found that the parasite affects the expression of immune genes, including members of the Toll signalling pathway providing evidence for a novel interaction between the parasite and the host immune response. Taken together, our results identify host biological processes and genes affected by an entomoparasitic nematode providing the first steps towards a molecular understanding of this ecologically important host–parasite interaction.

show abstract

“…Dramatic alterations are also induced by the parasite on the behaviour of female wasps: if infected, they are turned into gregarious 'zombies' regardless of their putative rank, i.e. workers or gynes (Beani, 2006;Beani et al, 2011;Cappa et al, 2014;Geffre et al, 2017). They leave their colonies few days after emergence without performing any social task, select peculiar sites where they search for shelter and nutrients to survive outside the nest, cluster to favour the parasite mating (Hughes et al, 2004;Beani et al, 2005) and overwinter in aggregations with future queens (Beani et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…Research on Polistes wasps, from the first physio-ethological study by Leo Pardi (1948) to more recent molecular phylogeny and sociogenomics (Schmitz and Moritz, 1998;Carpenter, 2003;Sumner et al, 2006;Toth et al, 2007Toth et al, , 2010Toth et al, , 2014Berens et al, 2015Berens et al, , 2016Geffre et al, 2017), has been mainly focused on the socially competitive and cooperative females, while the male phenotype has not received equal attention Heinze, 2016). The "so transparently Darwinian" scenario (West-Eberhard, 2006) regulating social life among females has centered the interest on the colony.…”

Section: Introductionmentioning

confidence: 99%

Subtle effect of Xenos vesparum (Xenidae, Strepsiptera) on the reproductive apparatus of its male host: Parasite or parasitoid?

Beani

Marchini

Cappa

et al. 2017

Journal of Insect Physiology

View full text Add to dashboard Cite

A B S T R A C TParasitic castration is an adaptive strategy where parasites usurp the hosts' reproductive physiology to complete their life cycle. The alterations in the host traits vary in their magnitude, from subtle changes in the host morphophysiology and behaviour to the production of complex aberrant phenotypes, which often depend on the host gender. The strepsipteran macroparasite Xenos vesparum induces dramatic behavioural and physiological changes in its female host, the paper wasp Polistes dominula, while its effect on the male phenotype is largely unknown.In this study we investigated how a single X. vesparum parasite influences the functional morphology of P. dominula male reproductive apparatus. We performed morphometry and ultrastructure characterization of corpora allata, testes, seminal vesicles and accessory glands in parasitized and unparasitized males, and also in young and old males to control for the effect of age on the natural deterioration of these organs. Our results show that age significantly affects the development of male reproductive apparatus. A low parasite load -one parasite per host is the common prevalence in the field -has only a marginal impact on the reproductive morphology of P. dominula males, affecting quantitatively but not qualitatively the protein content of male accessory glands. Thus, in male P. dominula wasps, X. vesparum appears to behave as a true "parasite", in clear opposition to the role of "parasitoid" that it takes in female hosts where castration causes the reproductive death.

show abstract

Transcriptomics of an extended phenotype: parasite manipulation of wasp social behaviour shifts expression of caste-related genes

Cited by 32 publications

References 48 publications

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation

Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

Subtle effect of Xenos vesparum (Xenidae, Strepsiptera) on the reproductive apparatus of its male host: Parasite or parasitoid?

Contact Info

Product

Resources

About