Proximate mechanism of behavioral manipulation of an orb-weaver spider host by a parasitoid wasp

Kloss, Thiago Gechel; Gonzaga, Marcelo O.; Oliveira, Leandro Licursi de; Sperber, Carlos Frankl

doi:10.1371/journal.pone.0171336

Cited by 30 publications

(16 citation statements)

References 32 publications

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“…However, most studies of PIPA concern the altered behaviour of host species. For instance, several species of ectoparasitoid wasps are known to modify the web‐building behaviour of their spider hosts (Eberhard, ; Matsumoto, ; Korenko et al ., ; Takasuka et al ., ; Kloss et al ., ). Just before the wasp enters its final stage of development, the spider host builds a modified web in the form of a ‘cocoon’ (Eberhard, ) that appears to enhance the survival of the parasitoid pupae.…”

Section: Introductionmentioning

confidence: 97%

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: 97%

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

et al. 2020

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“…Urban males show increased aggression towards prey when compared to males at lower non-urban desert temperatures while juvenile urban females have reduced web building behavior and produce smaller webs [ 7 ]. A link has been shown between ecydsteroid concentrations and web-building behavior in the orb-weaver spiders, Cyclosa morretes and Cyclosa fililineata [ 111 ]. These spiders serve as hosts for parasitoid wasps, which manipulate web-building behavior of their spider hosts by injecting ecdysteroids [ 111 ].…”

Section: Discussionmentioning

confidence: 99%

Ecdysteroid responses to urban heat island conditions during development of the western black widow spider (Latrodectus hesperus)

2022

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The steroid hormone 20-hydroxyecdysone (20E) controls molting in arthropods. The timing of 20E production, and subsequent developmental transitions, is influenced by a variety of environmental factors including nutrition, photoperiod, and temperature, which is particularly relevant in the face of climate change. Environmental changes, combined with rapid urbanization, and the increasing prevalence of urban heat islands (UHI) have contributed to an overall decrease in biodiversity making it critical to understand how organisms respond to elevating global temperatures. Some arthropods, such as the Western black widow spider, Latrodectus hesperus, appear to thrive under UHI conditions, but the physiological mechanism underlying their success has not been explored. Here we examine the relationship between hemolymph 20E titers and spiderling development under non-urban desert (27°C), intermediate (30°C), and urban (33°C) temperatures. We found that a presumptive molt-inducing 20E peak observed in spiders at non-urban desert temperatures was reduced and delayed at higher temperatures. Intermolt 20E titers were also significantly altered in spiders reared under UHI temperatures. Despite the apparent success of black widows in urban environments, we noted that, coincident with the effects on 20E, there were numerous negative effects of elevated temperatures on spiderling development. The differential effects of temperature on pre-molt and intermolt 20E titers suggest distinct hormonal mechanisms underlying the physiological, developmental, and behavioral response to heat, allowing spiders to better cope with urban environments.

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“…Spider wasps have been reported to inoculate spiders with its venom, and these injected ingredients control the spider’s net-weaving behavior. This has been suggested as a potential model for mind control psychotropics (Takasuka et al, 2015; Kloss et al, 2017).…”

Section: Methodsmentioning

confidence: 99%

Opportunities in Novel Psychotropic Drug Design from Natural Compounds

Tang

2019

International Journal of Neuropsychopharmacology

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Multiple initiatives at the national and international level support natural drug discovery. Psychiatrists and patients are not well informed about natural psychotropics in general. Existing antidepressant and antipsychotic drugs were developed from atropine, a natural product. Subsequent drug developments were largely based on extension and modification of earlier molecular scaffolds. This limits their mechanisms of action to similar neuropathways. Natural psychotropic substances, particularly those with hallucinogenic and psychedelic properties and different chemical structures, may serve as new paths to novel psychotropic drug development.

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Proximate mechanism of behavioral manipulation of an orb-weaver spider host by a parasitoid wasp

Cited by 30 publications

References 32 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

Ecdysteroid responses to urban heat island conditions during development of the western black widow spider (Latrodectus hesperus)

Opportunities in Novel Psychotropic Drug Design from Natural Compounds

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