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Masters of puppets: could the ecdysteroid route be a common pathway for behavioural manipulation in spiders by different parasites?
Abstract
Certain parasites improve their fitness by manipulating their host’s behaviour. Some evidence suggests that parasites exploit innate pathways in the host to manipulate their behaviour. Furthermore, phylogenetically unrelated parasites can generate similar behavioural changes in hosts from the same taxonomic group. Spiders are hosts for several parasites that appear to induce behavioural changes, such as building modified webs that may benefit the parasites. Additionally, some observations on spiders parasitized by Ichneumonidae wasps suggest that the construction of modified webs may merely result from activating the innate ecdysis process. Considering that different parasites may use similar manipulation pathways, we review and examine evidence in the literature that phylogenetically distant parasites (wasps, dipterans, and fungi) may converge on the manipulation mechanism of host spiders through activation of the preexisting mechanism of ecdysis. Also, we suggest that webs built by fungus-infected spiders represent an extended phenotype of these parasites. We conclude that the strategy of behavioural manipulation through activation of innate ecdysis in hosts may have converged in the different spider parasites, which have been favoured over evolutionary time. Therefore, we propose possible pathways for activating this mechanism, and provisions for future investigations to test these hypotheses.
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The parasitoid way of life (parasitizing and finally killing a single arthropod host) is one of the most successful lifeways in the animal kingdom, sparking an explosive diversification and accompanying numerous parasitoid strategies in insects, especially in the order Hymenoptera. Amongst parasitoid wasps, the Polysphincta group of genera has evolved a highly distinctive parasitoid mode of life, as solitary koinobiont ectoparasitoids of spiders (Chelicerata: Araneae). Some species of polysphinctine wasps have a remarkable ability to control spiders’ web-building behaviour (host web manipulation) to protect the vulnerable wasp cocoons. The group currently consists of 25 genera and 294 extant species worldwide, with 14 genera known to manipulate their host spiders. This study reviews the current species composition, distribution, host utilization and biology of all genera belonging to the Polysphincta group and their ancestral genera of spider egg mass pseudo-parasitoids, highlighting specific offensive approaches for subjugating spider hosts for oviposition and web manipulation against specific spider hosts. There must still be many more unique behaviours to be discovered, given that the life histories of several polysphinctine genera are poorly known or unknown. A tidy correspondence between lineages of polysphinctines and host spiders was recognized, implying the evolutionary history of polysphinctines. Based on the integrated information on behavioural data and host utilization, we suggest some hypotheses determining triggers for host shifts and discuss the possibility of adaptive radiation driven by divergent natural selection on host differentiation. One new taxonomic change is proposed: Zaglyptus idukkiensis (Manjusha, Sudheer & Ghosh, 2019), comb. nov. , is transferred from Polysphincta .
Behavioral modifications induced by parasites have been extensively documented across multiple taxa. However, a major challenge is to experimentally determine whether such manipulations confer an adaptive advantage to the parasite. Behavioral alterations in spiders attacked by ichneumonid wasps are characterized by the construction of modified webs. These modified webs can enhance the survival chances of the parasitoid by reducing mortality due to natural enemies and environmental factors during the pupal stage. Additionally, some modified webs offer extra protection by keeping a centrally attached leaf shelter, originally used by the spider as a refuge, where parasitoids can build their cocoon. In these webs, it is possible that web modifications are not critical for the survival of parasitoid pupae. We evaluated the hypothesis that modifications made by parasitized spiders in a web with leaf shelter do not improve the survival of the parasitoid and presented details of behavioral modifications induced by the wasp Zatypota alborhombarta (Ichneumonidae) in its host spider Cryptachaea migrans (Theridiidae). We observed that modified webs built by parasitized spiders had silk thread around the web shelter, reduced vertical lines, and an increase in forked distal ends of lines. However, these changes in the host web did not improve the survival of parasitoid pupae. Our results indicate that the benefits of host behavioral modification for the parasitoids may vary across different host species. In addition, we suggested that the effects of altered web designs may depend on specific host-created web features and environmental factors like predation pressure.
Significance statement
Behavioral manipulations of hosts induced by parasites are often suggested as an adaptive trait, increasing the fitness of the parasitic organism. Still, the influence of host characteristics on the parasite’s fitness is rarely experimentally assessed, raising questions about the extent of the adaptive nature of manipulation. Here, we demonstrate for the first time that behavioral modifications induced by Ichneumonidae wasps in a cobweb spider do not increase the survival of the parasitoids. We argue that the presence of shelters in these webs, used by parasitoids in their pupal stages, provides a safe environment for development, independent of other modifications. Furthermore, we suggest that the behavioral modification reflects the maintenance of a phylogenetically conserved trait.
Camponotus floridanus ants show altered behaviors followed by a fatal summiting phenotype when infected with manipulating Ophiocordyceps camponoti-floridani fungi. Host summiting as a strategy to increase transmission is also observed with parasite taxa beyond fungi, including aquatic and terrestrial helminths and baculoviruses. The drastic phenotypic changes can sometimes reflect significant molecular changes in gene expression and metabolite concentrations measured in manipulated hosts. Nevertheless, the underlying mechanisms still need to be fully characterized. To investigate the small molecules producing summiting behavior, we infected C. floridanus ants with O. camponoti-floridani and sampled their heads for LC–MS/MS when we observed the characteristic summiting phenotype. We link this metabolomic data with our previous genomic and transcriptomic data to propose mechanisms that underlie manipulated summiting behavior in “zombie ants.” This “multiomic” evidence points toward the dysregulation of neurotransmitter levels and neuronal signaling. We propose that these processes are altered during infection and manipulation based on (1) differential expression of neurotransmitter synthesis and receptor genes, (2) altered abundance of metabolites and neurotransmitters (or their precursors) with known behavioral effects in ants and other insects, and (3) possible suppression of a connected immunity pathway. We additionally report signals for metabolic activity during manipulation related to primary metabolism, detoxification, and anti-stress protectants. Taken together, these findings suggest that host manipulation is likely a multi-faceted phenomenon, with key processes changing at multiple levels of molecular organization.
Gibellula (Cordycipitaceae, Hypocreales) is frequently observed growing on spiders, but little is known about their host range. One of the greatest challenges in describing these interactions is identifying the host, since the fungus often rapidly consumes the parasitised spiders and destroys important diagnostic taxonomic traits. Additionally, the global diversity of Gibellula remains unclear, as does the natural history and phylogenetic relationships of most of the species. Herein, we performed an extensive investigation on the species of Gibellula, reconstructed the most complete molecular phylogeny of the genus in the context of Cordycipitaceae, and performed a systematic review in order to provide the foundations towards a better understanding of the genus. Therefore, we have performed an integrative study to investigate the life history of the genus and to disentangle the questionable number of valid species proposed over time. We provided novel molecular data for published species that had not been sequenced before, such as G. mirabilis and G. mainsii, and evaluated all the original and modern morphological descriptions. In addition, we presented its global known distribution and compiled all available molecular data. We suggested a set of terms and morphological traits that should be considered in future descriptions of the genus and that a total of 31 species should be considered as accepted.
Bodyguard manipulation is a behavioural manipulation in which the host's behaviour is altered to protect the inducer's offspring from imminent biotic threats. The behaviour of a post-parasitoid-egressed host resembles a quiescence state with a characteristic reduction in motor activities like feeding, locomotion, respiration, and metabolic rate. Yet, they respond aggressively through a defensive response when disturbed, which ensures better fitness for the parasitoid's offspring. The behavioural changes in the parasitized host appear after the parasitoid egression. Several hypotheses have been proposed to elucidate how the parasitized host's behaviour is manipulated for the fitness benefits of the inducers, but the exact mechanism is still unknown. We review evidence to explain the behavioural changes and their mechanism in the parasitized hosts. The evidence suggests that parasitoid pre-pupal egression may drive the host to stress-induced sleep. The elevated octopamine concentration also reflects the stress response in the host. Given the theoretical links between the behavioural and the physiological changes in the post-parasitoid-egressed host and stress-induced sleep of other invertebrates, we suggest that behavioural studies combined with functional genomics, proteomics, and histological analyses might give a better understanding of bodyguard manipulation.
Fungal parasites that infect spiders can affect their survival and potentially their behaviour. The genus Gibellula (Ascomycota, Cordycipitaceae) infects arachnids, and due to difficulties in identifying hosts after fungal sporulation, its ecology and spider host diversity are poorly understood. Herein, we propose a new species of Gibellula from the Brazilian Atlantic Forest: Gibellula aurea, which parasitizes two spider families (Anyphaenidae and Corinnidae). Gibellula aurea exhibits characteristic golden-yellow hyphae that completely cover hosts and white conidiophores emerging along synnemata or directly from hosts. Molecular identification was performed by sequencing the small and large nuclear ribosomal subunits, translation elongation factor, and RNA polymerase II second largest subunit regions, and reconstructing multigene phylogenetic trees. Maximum Likelihood and Bayesian Inference phylogenies demonstrate that G. aurea forms a well-supported clade closer to G. flava, G. gamsii, G. leiopus, G. longispora, G. pigmentosinum, and G. pulchra. The phylogenetic reconstruction displayed herein represents the most comprehensive phylogeny for this genus to date. Spider hosts parasitized by G. aurea have been invariably found attached underneath leaves in vegetation, regardless of the identity of the infected hosts. The consistency of the death locations of G. aurea hosts indicates recurrent behaviour given the habitat heterogeneity of these host groups. Nevertheless, it is still unclear to what extent the place where hosts die can favour parasite fitness.
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.
The Tachinidae are natural enemies of many lepidopteran and coleopteran pests of crops, forests, and fruits. However, host-tachinid parasitoid interactions have been largely unexplored. In this study, we investigated the effects of tachinids on host biological traits, using Exorista japonica, a generalist parasitoid, and the silkworm Bombyx mori, its lepidopteran host, as models. We observed that E. japonica parasitoidism did not affect silkworm larval body weight gain and cocooning rate, whereas they caused shortened duration of molting from the final instar to the pupal stage, abnormal molting from larval to pupal stages, and a subsequent decrease in host emergence rate. Moreover, a decrease in juvenile hormone (JH) titer and an increase in 20-hydroxyecdysone (20E) titer in the hemolymph of parasitized silkworms occurred. The transcription of JH and 20E responsive genes was downregulated in mature parasitized hosts, but upregulated in parasitized prepupae while Fushi tarazu factor 1 (Ftz-f1), a nuclear receptor essential in larval ecdysis, showed dramatically reduced expression in parasitized hosts at both the mature and prepupal stages. Moreover, the transcriptional levels of BmFtz-f1 and its downstream target genes encoding cuticle proteins were downregulated in epidermis of parasitized hosts. Meanwhile, the content of trehalose was decreased in the hemolymph, while chitin content in the epidermis was increased in parasitized silkworm prepupae. These data reveal that the host may fine-tune JH and 20E synthesis to shorten developmental duration to combat established E. japonica infestation, while E. japonica silences BmFtz-f1 transcription to inhibit host pupation. This discovery highlights the novel target mechanism of tachinid parasitoids and provides new clues to host/tachinid parasitoid relationships.
Parasites are some of the most abundant, diverse, and ecologically important organisms on the planet. Similarly, spiders are diverse, abundant, and play important roles in many terrestrial ecosystems. It is unfortunate that our understanding of the parasites that affect spiders is so underdeveloped relative to similar fields (e.g., parasites of insects). With this review, we describe characteristics of the major groups known to parasitize spiders and illustrate the ways in which spider biology presents unique challenges and opportunities for their parasites. Particularly promising avenues of future research include testing how parasites alter their spider hosts' behavior and ecology through density-dependent and trait-mediated effects. We close by providing future directions and testable hypotheses at the forefront of spider-parasite research.
An unidentified jumping spider (cf. Anarrhotus) from southwestern India constructs planar orb webs that serve as nocturnal retreats. These webs are not inhabited during the daytime and do not appear to play a role in prey capture by these spiders. Their construction, involving the attachment of silk lines radiating from a hub or platform that is occupied by the spider at night, resembles the early stages of web construction by orb-weaving spiders of the family Araneidae.
Background
For diurnal animals that heavily rely on vision, a nocturnal resting strategy that offers protection when vision is compromised, is crucial. We found a population of a common European jumping spider ( Evarcha arcuata ) that rests at night by suspending themselves from a single silk thread attached overhead to the vegetation, a strategy categorically unlike typical retreat-based resting in this group.
Results
In a comprehensive study, we collected the first quantitative field and qualitative observation data of this surprising behaviour and provide a detailed description. We tested aspects of site fidelity and disturbance response in the field to assess potential functions of suspended resting. Spiders of both sexes and all developmental stages engage in this nocturnal resting strategy. Interestingly, individual spiders are equally able to build typical silk retreats and thus actively choose between different strategies inviting questions about what factors underlie this behavioural choice.
Conclusions
Our preliminary data hint at a potential sensory switch from visual sensing during the day to silk-borne vibration sensing at night when vision is compromised. The described behaviour potentially is an effective anti-predator strategy either by acting as an early alarm system via vibration sensing or by bringing the animal out of reach for nocturnal predators. We propose tractable hypotheses to test an adaptive function of suspended resting. Further studies will shed light on the sensory challenges that animals face during resting phases and should target the mechanisms and strategies by which such challenges are overcome.
Many organisms are able to elicit behavioral change in other organisms. Examples include different microbes (e.g., viruses and fungi), parasites (e.g., hairworms and trematodes), and parasitoid wasps. In most cases, the mechanisms underlying host behavioral change remain relatively unclear. There is a growing body of literature linking alterations in immune signaling with neuron health, communication, and function; however, there is a paucity of data detailing the effects of altered neuroimmune signaling on insect neuron function and how glial cells may contribute toward neuron dysregulation. It is important to consider the potential impacts of altered neuroimmune communication on host behavior and reflect on its potential role as an important tool in the “neuro-engineer” toolkit. In this review, we examine what is known about the relationships between the insect immune and nervous systems. We highlight organisms that are able to influence insect behavior and discuss possible mechanisms of behavioral manipulation, including potentially dysregulated neuroimmune communication. We close by identifying opportunities for integrating research in insect innate immunity, glial cell physiology, and neurobiology in the investigation of behavioral manipulation.
Host manipulation has already been documented in several distinct host–parasite associations, covering all major phyla of living organisms. While in animals we know that several species have the ability to manipulate their hosts for the benefit of the parasite, in arthropopathogenic fungi there is very little knowledge about possible behavioral manipulation. We report for the first time the interaction between the araneopathogenic fungus genus Gibellula Cavara and the spider Macrophyes pacoti Brescovit, Oliveira, Sobczak and Sobczak, 2019 (Anyphaenidae) in addition to investigating the potential change in behavior of spiders infected by the parasitic fungus. We also investigated whether the rainfall regime influences the abundance of infected spiders and the parasitism rate by the araneopathogenic fungus. Our results corroborated our hypothesis that the fungus induces vertical segregation in the spider population, inducing infected spiders to be at higher heights than uninfected ones. Dead infected spiders were found in a stretched position that probably helps in fixing the carcass on the leaves by increasing the contact surface between the host and the substrate. Our results also confirm the positive relationship between the rainy season and the greater number of parasitized spiders and the parasitism rate.
In the present study, data on the interaction between wasp specimens of the species Epipompilus platensis Roig Alsina, 2017 (Hymenoptera, Pompilidae) and spiders of the species Ariadna mollis (Holmberg 1876) (Araneae, Segestriidae) are presented for the first time. Present in the localities of Punta Lara (Partido de Ensenada) and José Hernández (Partido de La Plata), both belonging to the province of Buenos Aires. Several specimens of A. mollis were collected on april 2015, and those that presented an egg or a small larva attached to the back of the abdomen were selected. They were kept under observation in a bioterium until completing the development of the wasp's adult state. Of the total spiders collected, 9.6% were parasitized by wasps. Of that percentage, four larvae of E. platensis reached the adult stage (three females and one male). The results obtained contribute to the knowledge of a new interaction between wasps and spiders.
Ecdysteroids, as the key growth hormones, regulate moulting, metamorphosis and reproduction in arthropods. Ecdysteroid biosynthesis is catalysed by a series of cytochrome P450 monooxygenases (CYP450s) encoded by Halloween genes, including spook (spo), phantom (phm), disembodied (dib), shadow (sad) and shade (shd). The ecdysteroid biosynthesis in insects is clear with 20‐hydroxyecdysone (20E) as the main ecdysteroid. However, the information on the major ecdysteroids in arachnids is limited. In this study, Halloween genes spo, dib, sad and shd, but not phm, were identified in the pond wolf spider, Pardosa pseudoannulata. Phylogenetic analysis grouped arachnid and insect Halloween gene products into two CYP450 clades, the CYP2 clan (spo and phm) and the mitochondrial clan (dib, sad, and shd). In P. pseudoannulata, the temporal expression profile of the four Halloween genes in concurrence with spiderling moulting with steady increase in the course of the 2nd instar followed by a rapid dropdown once moulting was completed. Spatially, the four Halloween genes were highly expressed in spiderling abdomen and in the ovaries of female adults. In parallel, ponasterone A (PA), but not 20E, was detected by LC–MS/MS analysis in P. pseudoannulata, and it was demonstrated as a functional ecdysteroid in the spider by accelerating of moulting with PA addition. The present study revealed the different ecdysteroid biosynthesis pathways in spiders and insects.
Thailand is known to be a part of what is called the Indo-Burma biodiversity hotspot, hosting a vast array of organisms across its diverse ecosystems. This is reflected by the increasing number of new species described over time, especially fungi. However, a very few fungal species from the specialized spider-parasitic genus Gibellula have ever been reported from this region. A survey of invertebrate-pathogenic fungi in Thailand over several decades has led to the discovery of a number of fungal specimens with affinities to this genus. Integration of morphological traits into multi-locus phylogenetic analysis uncovered four new species: G. cebrennini, G. fusiformispora, G. pigmentosinum, and G. scorpioides. All these appear to be exclusively linked with torrubiella-like sexual morphs with the presence of granulomanus-like asexual morph in G. pigmentosinum and G. cebrennini. A remarkably high host specificity of these new species towards their spider hosts was revealed, and for the first time, evidence is presented for manipulation of host behavior in G. scorpioides.
Ant-infecting Ophiocordyceps fungi are globally distributed, host manipulating, specialist parasites that drive aberrant behaviors in infected ants, at a lethal cost to the host. An apparent increase in activity and wandering behaviors precedes a final summiting and biting behavior onto vegetation, which positions the manipulated ant in a site beneficial for fungal growth and transmission. We investigated the genetic underpinnings of host manipulation by: ( i) producing a high-quality hybrid assembly and annotation of the Ophiocordyceps camponoti-floridani genome, ( ii ) conducting laboratory infections coupled with RNAseq of O. camponoti-floridani and its host, Camponotus floridanus , and ( iii ) comparing these data to RNAseq data of Ophiocordyceps kimflemingiae and Camponotus castaneus as a powerful method to identify gene expression patterns that suggest shared behavioral manipulation mechanisms across Ophiocordyceps -ant species interactions. We propose differentially expressed genes tied to ant neurobiology, odor response, circadian rhythms, and foraging behavior may result by activity of putative fungal effectors such as enterotoxins, aflatrem, and mechanisms disrupting feeding behaviors in the ant.
Records of interactions between acrocerid parasitoids (Diptera: Acroceridae) and their hosts are very scarce. Here we report a case of acrocerid fly (most likely Ogcodes sp.) parasitising zodariid spiders of the genus Pax from Israel. We describe the parasitoid development and possible host manipulation.
Surgical removal and larval transplantation experiments were carried out to evaluate behavioral manipulativeeffects caused by larvae of the polysphinctine ichneumonid,Reclinervellus nielseni(Roman, 1923), on its orb-weavingspider host,Cyclosa argenteoalbaB ̈osenberg & Strand, 1906 (Araneidae). Residual behavioral effects on spiders fromwhich parasitoid larvae had been removed were recognized and are described. Some transplanted parasitoid larvae alsosuccessfully consumed alternative spider hosts provided to them, and completed metamorphosis. The removal experimentsupports previous hypotheses proposed by Eberhard, that larval effects involve chemicals, which are still unidentified andare dosage-dependent, because (1) spiders with parasitoid larvae removed continued to show manipulated behavior, and(2) the later in their development that the parasitoid larvae were removed, the more acute remaining effects were (e.g.,production of V radii, new hub loops and silk decorations on webs). Further, the results support the idea that the spider’sweb-building behavior is composed of independent units (modules), because whether or not specific web features wereproduced depended on when the larva was removed. Transplantation experiments provide a new technique for rearingparasitoid larvae whose host spider dies: penultimate instar parasitoid larvae were successfully reared following theirremoval from their original host by providing them with another host spider held by a mesh. Transplantation of a smallyoung larva by gluing it onto another host that was released after successful transplantation, caused the new host toproduce a modified web identical to the ‘‘cocoon’’ webs typically produced by parasitized spiders. This shows that venominjected by the adult parasitoid prior to oviposition is not necessary to induce behavioral changes in the host, which can becaused entirely by wasp larval secretions.
(PDF) Evaluation of manipulative effects by an ichneumonid spider-ectoparasitoid larva upon an orb-weaving spider host (Araneidae: Cyclosa argenteoalba) by means of surgical removal and transplantation. Available from: https://www.researchgate.net/publication/335852624_Evaluation_of_manipulative_effects_by_an_ichneumonid_spider-ectoparasitoid_larva_upon_an_orb-weaving_spider_host_Araneidae_Cyclosa_argenteoalba_by_means_of_surgical_removal_and_transplantation [accessed Sep 21 2019].
Parasitoids may change host behavior in order to improve their
survival during the pupal stage. This has been observed in some
ichneumonid wasps (Polysphincta genus group), which are able to induce
modifications in the movements of host spiders during web construction.
These changes usually result in web patterns distinct from those of
normal webs of spiders. In this study, we describe the behavioral change
in the orb-weaver spider Metazygia laticeps (Araneidae), parasitized by a
new species of parasitoid wasp, Polysphincta sinearanea sp. n.
(Ichneumonidae), which has a high prevalence in M. laticeps populations.
This parasitoid induces behavioral changes in M. laticeps that result in
the complete suppression of the normal orb-web structure. The absence of
the orb probably reduces accumulation of debris and interception of
insects by the webs (factors that could result in the rupture of threads
that hold the shelter of the web) during the period from cocoon
construction to the emergence of the adult wasp. Also, the suppression of
the normal orb-web structure implies that resources that would have been
invested in the web will be available to the larva wasp.
Neuro-parasitology is an emerging branch of science that deals with parasites that can control the nervous system of the host. It offers the possibility of discovering how one species (the parasite) modifies a particular neural network, and thus particular behaviors, of another species (the host). Such parasite–host interactions, developed over millions of years of evolution, provide unique tools by which one can determine how neuromodulation up-or-down regulates specific behaviors. In some of the most fascinating manipulations, the parasite taps into the host brain neuronal circuities to manipulate hosts cognitive functions. To name just a few examples, some worms induce crickets and other terrestrial insects to commit suicide in water, enabling the exit of the parasite into an aquatic environment favorable to its reproduction. In another example of behavioral manipulation, ants that consumed the secretions of a caterpillar containing dopamine are less likely to move away from the caterpillar and more likely to be aggressive. This benefits the caterpillar for without its ant bodyguards, it is more likely to be predated upon or attacked by parasitic insects that would lay eggs inside its body. Another example is the parasitic wasp, which induces a guarding behavior in its ladybug host in collaboration with a viral mutualist. To exert long-term behavioral manipulation of the host, parasite must secrete compounds that act through secondary messengers and/or directly on genes often modifying gene expression to produce long-lasting effects.
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.
The neuroendocrine system of insects, including the presence of the main neuroactive compounds, and their role in ontogenesis are probably best understood of all the arthropods. Development, metamorphosis, the maturation of the gonads, vitellogenesis and egg production are regulated by hormones (juvenile hormones, ecdysteroids) and neuropeptides. However, knowledge about their presence and functions in spiders is fragmentary. In this paper, we present a summary of the current data about the juvenile hormones, ecdysteroids and neuropeptides in selected groups of arthropods, with particular emphasis on spiders. This is the first article that takes into account the occurrence, action and role of hormones and neuropeptides in spiders. In addition, the suggestions for possible ways to study these compounds in Araneomorphae spiders are unique and cannot be found in the arachnological literature.
While molting occurs in the development of many animals especially in arthropods, post-maturity molting (PMM, organisms continue to molt after sexual maturity) has received little attention. Mechanism of molting has been studied intensively, however, the mechanism of PMM remains unknown although it is suggested to be crucial for the development of body size. In this study, we investigated factors that potentially induce PMM in the golden orb-web spider Nephila pilipes, which has the greatest degree of sexual dimorphism among terrestrial animals. We manipulated the mating history and the nutrient consumption of the females to examine whether they can affect PMM. The results showed that female spiders under low nutrition were more likely to molt as adults, and mating had no significant influence to the occurrence rate of PMM. Moreover, spiders that experienced PMM lived longer than those without and their body sizes were significantly increased. Therefore, we concluded that it is the nutritional condition rather than the mating history that has affected PMM.
Though the best known natural enemies of arachnids are Hymenoptera, Diptera also form an important group of arachnid enemies, attacking 31 spider families in all three suborders of Araneae, as well as members of the Acari, Amblypygi and Scorpiones. Some species of Bombyliidae, Chloropidae, Drosophilidae, Ephydridae, Phoridae and Sarcophagidae are known to attack eggs of several families of arachnids, acting as predators, parasitoids and/or parasites of egg sacs. Alternatively, members of Acroceridae and Tachinidae are internal parasitoids, attacking juvenile and/or adult spiders. One species of Sarcophagidae is reported as a predator of individual Liphistiidae (Mesothelae) spiders. We summarize the available information on all lineages of Diptera known to attack arachnids, including predators, parasites, kleptoparasites and parasitoids. A table including host records pertaining to the aforementioned dipteran families is presented. Particular emphasis is given to Acroceridae, the only lineage of Diptera known to develop exclusively on arachnids, and one of the most significant groups of natural enemies of spiders.
Some ichneumonid wasps induce modifications in the web building behavior of their spider hosts to produce resistant “cocoon” webs. These structures hold and protect the wasp’s cocoon during pupa development. The mechanism responsible for host manipulation probably involves the inoculation of psychotropic chemicals by the parasitoid larva during a specific developmental period. Recent studies indicate that some spiders build cocoon webs similar to those normally built immediately before ecdysis, suggesting that this substance might be a molting hormone or a precursor chemical of this hormone. Here, we report that Cyclosa spider species exhibiting modified behavior presented higher 20-OH-ecdysone levels than parasitized spiders acting normally or unparasitized individuals. We suggest that the lack of control that spiders have when constructing modified webs can be triggered by anachronic activation of ecdysis.
Background
Synthesis of multiple randomized controlled trials (RCTs) in a systematic review can summarize the effects of individual outcomes and provide numerical answers about the effectiveness of interventions. Filtering of searches is time consuming, and no single method fulfills the principal requirements of speed with accuracy. Automation of systematic reviews is driven by a necessity to expedite the availability of current best evidence for policy and clinical decision-making.
We developed Rayyan (http://rayyan.qcri.org), a free web and mobile app, that helps expedite the initial screening of abstracts and titles using a process of semi-automation while incorporating a high level of usability. For the beta testing phase, we used two published Cochrane reviews in which included studies had been selected manually. Their searches, with 1030 records and 273 records, were uploaded to Rayyan. Different features of Rayyan were tested using these two reviews. We also conducted a survey of Rayyan’s users and collected feedback through a built-in feature.
Results
Pilot testing of Rayyan focused on usability, accuracy against manual methods, and the added value of the prediction feature. The “taster” review (273 records) allowed a quick overview of Rayyan for early comments on usability. The second review (1030 records) required several iterations to identify the previously identified 11 trials. The “suggestions” and “hints,” based on the “prediction model,” appeared as testing progressed beyond five included studies. Post rollout user experiences and a reflexive response by the developers enabled real-time modifications and improvements. The survey respondents reported 40% average time savings when using Rayyan compared to others tools, with 34% of the respondents reporting more than 50% time savings. In addition, around 75% of the respondents mentioned that screening and labeling studies as well as collaborating on reviews to be the two most important features of Rayyan.
As of November 2016, Rayyan users exceed 2000 from over 60 countries conducting hundreds of reviews totaling more than 1.6M citations. Feedback from users, obtained mostly through the app web site and a recent survey, has highlighted the ease in exploration of searches, the time saved, and simplicity in sharing and comparing include-exclude decisions. The strongest features of the app, identified and reported in user feedback, were its ability to help in screening and collaboration as well as the time savings it affords to users.
Conclusions
Rayyan is responsive and intuitive in use with significant potential to lighten the load of reviewers.
The genus Paracyphononyx Gribodo, 1884 (Pompilidae) contains species that act as koinobiont parasitoids of cursorial spiders. Here, we record a new parasitism interaction involving the pompilid wasp Paracyphononyx scapulatus (Brethes) and the hunter spider Trochosa sp. (Lycosidae), and we describe how the wasp develops on the spider. This study contributes new information about the interaction between koinobiont ectoparasitoid wasps and spiders, which probably arose independently in different groups of wasps.
Host manipulation by parasites and parasitoids is a fascinating phenomenon within evolutionary ecology, representing an example of extended phenotypes. To elucidate the mechanism of host manipulation, revealing the origin and function of the invoked actions is essential. Our study focused on the ichneumonid spider ectoparasitoid Reclinervellus nielseni, which turns its host spider (Cyclosa argenteoalba) into a drugged navvy, to modify the web structure into a more persistent cocoon web so that the wasp can pupate safely on this web after the spider's death. We focused on whether the cocoon web originated from the resting web that an unparasitized spider builds before moulting, by comparing web structures, building behaviour and silk spectral/tensile properties. We found that both resting and cocoon webs have reduced numbers of radii decorated by numerous fibrous threads and specific decorating behaviour was identical, suggesting that the cocoon web in this system has roots in the innate resting web and ecdysteroid-related components may be responsible for the manipulation. We also show that these decorations reflect UV light, possibly to prevent damage by flying web-destroyers such as birds or large insects. Furthermore, the tensile test revealed that the spider is induced to repeat certain behavioural steps in addition to resting web construction so that many more threads are laid down for web reinforcement.
© 2015. Published by The Company of Biologists Ltd.
During the transition from feeding to molting, larval insects undergo profound changes in behavior and patterns of gene expression regulated by the neuroendocrine system. For some species, a distinctive characteristic of molting larvae is presence of a quiescent state sometimes referred to as "molt-sleep". Here, observations of 4(th) instar Manduca sexta larvae indicate the molting period involves a predominantly quiescent state that shares behavioral properties of adult insect sleep in that it is rapidly reversible and accompanied by a reduced responsiveness to both mildly arousing and noxious stimuli. When subjected to noxious stimuli, molting larvae exhibit locomotory and avoidance behaviors similar to those of inter-molt larvae. Although less consolidated, inter-molt quiescence shares many of the same behavioral traits with molting quiescence. However, when subjected to deprivation of quiescence, inter-molt larvae display a compensatory rebound behavior that is not detected in molting larvae. This suggests that molting quiescence is a specialized form of inactivity that affords survival advantages to molting larvae. RNA-seq analysis of molting larvae shows general reduction in expression of genes encoding GPCRs and down regulation of genes connected with cyclic nucleotide signaling. On the other hand, certain ion channel genes are up-regulated, including transient receptor potential (TRP) channels, chloride channels and a voltage-dependent calcium channel. These findings suggest patterns of gene expression consistent with elevation of quiescent state characteristic of the molt in a model holometabolous insect.
Copyright © 2015 Elsevier Ltd. All rights reserved.
Some new cases of ectoparasitoid wasps from the Polysphincta genus-group manipulating the behaviour of host spiders have been described in recent years, indicating that the modification of normal web structure is the rule rather than an exception as the outcome of these interactions. In most cases, orb web diameter and the number of adhesive spirals are reduced, which decreases the probability of web damage from the interception of insects on the viscid threads during the development of the parasitoid within the cocoon. In this study, we describe a new interaction between the host spider Leucauge volupis and the recently described parasitoid Hymenoepimecis jordanensis. Web modifications induced by larvae in their last instar, in this case, are different to those described for two other Leucauge species attacked by Hymenoepimecis spp., L. argyra and L. roseosignatha. The cocoon webs constructed by the parasitized L. volupis are similar to those webs constructed by immature individuals, presenting a lower tangle, which may increase the stability of the web or offer additional physical protection for the cocoon. As in other previously described cases, sticky spirals are absent from cocoon webs. However, the photographs of webs constructed by spiders carrying second instar larvae indicated that the reduction in spirals begins before the construction of the cocoon web. These webs remain functional, being substantially modified only when the larvae reach the third instar. Variation among cocoon web designs of congeneric hosts attacked by distinct Hymenoepimecis species indicate that the substance used for host manipulation 182 Parasitic induced changes in the web architecture may vary in concentration and/or composition. Alternatively, distinct host responses may occur to the same substances.
Exetasis jujuyensis Gillung sp. nov. (Acroceridae) is described from Argentina and a dichotomous key to species of Exetasis Walker is provided. Detailed observations are presented on the effect of fly larval development on the behavior of the host spider (Acanthoscurria sternalis Pocock (Theraphosidae)).
Parasite manipulation of host behavior, as an effective strategy to establish transmission, has evolved multiple times across taxa, including fungi. Major strides have been made to propose molecular mechanisms that underlie manipulative parasite-host interactions including the manipulation of carpenter ant behavior by Ophiocordyceps. This research suggests that the secretion of parasite proteins and light-driven biological rhythms are likely involved in the infection and manipulation biology of Ophiocordyceps and other manipulating parasites. Here, we discuss research on Ophiocordyceps considering findings from other (fungal) parasites that either are relatively closely related (e.g., other insect- and plant-infecting Hypocreales) or also manipulate insect behavior (e.g., Entomophthorales). As such, this review aims to put forward this question: Are the mechanisms behind Ophiocordyceps manipulation and infection unique, or did they convergently evolve? From this discussion, we pose functional hypotheses about the infection biology of Ophiocordyceps that will need to be addressed in future studies.
This volume presents ecological consequences and evolutionary mechanisms that may be associated with behavioral alterations in parasitized hosts. Alterations may result from natural selection favoring the host or parasite, or there may be side effects of physiological changes associated with symbiosis. This book summarizes the literature in this area, showing that reports of alteration may frequently be consistent with more than one evolutionary explanation and that rigorous tests are needed before the phenomenon can be understood and placed in a predictive framework. Such understanding is important, because these behavioral alterations have been shown to have the potential to affect the distribution of animals in nature and their interactions with predators and competitors, and the alterations may have implications for vector biology.
Parasitoids are significant ecological elements of terrestrial food webs and have evolved within seven insect orders. Interestingly, however, associations with spiders as hosts have evolved only in two insect orders, Diptera and Hymenoptera. Here, we summarize various aspects of host utilization by dipteran flies with an emphasis on associations with spiders. Our synthesis reveals that spider flies (family Acroceridae) have evolved a unique life strategy among all the parasitoid taxa associated with spiders, in which koinobiont small-headed flies utilize an indirect oviposition strategy. This indirect oviposition in spider flies is inherited from Nemestrinimorpha ancestors which appeared in the Late Triassic and is characterized by the evolution of planidial larvae. Further, we discuss the advantages and disadvantages of indirect oviposition in spider flies. On the one hand, indirect oviposition allows the fly to avoid contact/wrestling with spider hosts. On the other hand, larval survival is low because the planidium must actively seek out and infect a suitable host individually. The risk of failure to find a suitable spider host is offset by the fly’s extremely high fecundity.
Strategies to invade and exploit hosts for survival are an essential part of the parasitic lifestyle. Species of the Polysphincta genus group (Hymenoptera: Ichneumonidae), which utilize spiders as hosts, are examples of parasitoids that present several behavioral strategies in host immobilization and egg laying. In this study, we characterized the oviposition behavior of the Darwin wasp Hymenoepimecis cameroni Townes, 1966 (Hymenoptera: Ichneumonidae) on their host spider, performed the taxonomic description of the female, and redescribed the male parasitoid. We observed eight H. cameroni females endeavoring to parasitize young Leucauge volupis (Keyserling, 1893) spiders. Each female made up to 12 successive attempts at oviposition, totaling 36 observed attacks, with only two successful attacks. The main oviposition behavior of H. cameroni individuals consists of flying close to the web and performing a direct attack on the spider, which often results in the spider escaping into the vegetation. We observed that in seven events where the spiders fled into the vegetation, the individuals of H. cameroni adopted a second strategy, which consisted of hanging from the hind legs in the web hub. This observation showed that the females of H. cameroni have the ability to modulate the oviposition strategy after a failure in the initial attack. The pattern observed for the attack of H. cameroni indicates that the ability to adjust the approach could be specific to the behavioral habits of L. volupis.
The ichneumonid parasitoid Sinarachna nigricornis (Holmgren, 1860) was associated only with Araneus sturmi (Hahn, 1831) in the studied locality. The normal capturing orb web of A. sturmi was always vertical and had a median of 18 radii and 9 spirals in laboratory conditions. When spiders did not build capture webs, they built resting and molting webs which consisted of a few threads between the ends of the provided tree twigs. There were no significant differences in the number of radials and spirals between unparasitized spiders and spiders parasitized by early instar parasitoid larvae. Araneus sturmi under manipulation by S. nigricornis built a modified cocoon web, serving parasitoid larva pupation. S. nigricornis exhibited high plasticity in the architecture of the cocoon web induced by its penultimate instar larva. The most common cocoon web was of 3D architecture with a small central silk platform, from which the wasp cocoon was suspended by its apical end (72% of webs). In 22% of cases, the cocoon web consisted only of a few threads, presumably resembling a molting web. In one case, the manipulated spider built a 3D tangle, though radials and the central hub (typical for the normal capturing web) were also present. The genus specificity of the cocoon web architecture described here, in which the typical cocoon web exhibits a sparse but strong 3D architecture and in which the wasp cocoon is suspended by its apical end at the center, is expected for the genus Sinarachna.
Ecdysteroids are a group of steroid hormones originally identified as moulting hormones in insects. Ever since the isolation of the first ecdysteroid, studies in multiple model insect species have revealed their modes of action and pleiotropic functions. It is now established that they control a multitude of physiological processes, including moulting, metamorphosis, reproduction, and stress responses. Here I summarize our current understanding of the diverse functions of ecdysteroids throughout the insect life cycle. I then highlight six steps of ecdysteroid signalling as a framework to comprehend this complex hormone signalling pathway: biosynthesis, secretion, circulation, transport, modification, and gene expression regulation.
Wasps in the Polysphincta group of Ichneumonidae induce their web-spinning spider hosts to construct modified ‘cocoon’ webs that support and protect the wasps’ cocoons, but the mechanisms used by wasps to manipulate their host spiders have been unclear. We evaluate the hypothesis that wasps manipulate spider ecdysteroid moulting hormones, using the taxonomic distribution of the hosts and cocoon web types of different wasp lineages in the Polysphincta group, with new data comparing cocoon webs with the moulting webs of non-parasitized host spiders. Several predictions were confirmed: wasp and spider species have not co-evolved in a strict sense, with wasp lineages jumping between host lineages; cocoon web designs induced by closely related wasps varied widely in spiders with differing natural histories; cocoon web designs were consistently adjusted to the natural history of the spider in ways promoting wasp survival; and cocoon web designs often resembled those of moulting webs of non-parasitized spiders. Several other types of data did not fit the predictions of simple versions of the ecdysteroid hypothesis, however. We conclude that the use of ecdysteroids by the wasps to manipulate host spider behaviour is probably widespread, but that some wasps might also use other mechanisms.
A diverse set of pathogens have evolved extended phenotypes that manipulate the moribund behavior of their various insect hosts. By elevating host positioning at death, a phenomenon called “summit disease”, these pathogens have been shown to have higher fitness. Though a few summit disease systems have been intensively characterized, in particular the Ophiocordyceps-ant system, summit diseases lack an overarching theory for the underlying mechanisms of this complex behavioral manipulation. In this article, we combine the gamut of summiting systems into a cohesive framework: we propose two types of summit disease (juvenile and adult), which both exploit natural insect behaviors during periods of quiescence. We place this framework in the context of available literature and propose investigations that follow from this comprehensive understanding of summit disease in insects.
Spider wasps of the genus Minagenia have evolved koinobiontism as a relatively rare life strategy within the widely diversified hymenopteran family Pompilidae. In this study, we evaluated several aspects of the parasitic strategy of the wasp Minagenia sp. – namely host specificity, ontogeny, and sex determination as a function of host size. We found that Minagenia sp. is highly host specific, being associated only with the genus Lycosa from the family Lycosidae, namely Lycosa u-album (Mello-Leitão, 1938), Lycosa erythrognatha (Lucas, 1836) and Lycosa poliostoma (Koch, 1847) with a parasitism incidence of 18.9%, 15.8% and 12.5%, respectively. Both ecological and taxonomical host traits determine the host selection and sex allocation of Minagenia female wasps. Charnov's host-size model explains Minagenia’s host-size-dependent sex ratio in combination with the effect of host development stage, host species, and host foraging strategy. We also found that the final instar larva of Minagenia induces behavioural changes in spider hosts. The manipulated spider builds a protective silk chamber as a shelter for parasitoid pupation. Our results suggest that host manipulation seems to be narrowly connected with koinobiont life style throughout Hymenoptera. This study provides new information about the host-parasitoid koinobiont life strategy among spider wasps, which probably arose convergently in distant taxonomical groups within Pompilidae.
Spider-pathogenic fungi are widely distributed in the world. Our review shows at least eighty six spider- and harvestman-pathogenic fungi that are currently accommodated in genera Akanthomyces Lebert, Beauveria Vuill., Clonostachys Corda, Cordyceps Fr., Engyodontium de Hoog, Gibellula Cavara, Hevansia Luangsa-ard et al., Hirsutella Pat., Hymenostilbe Petch, Lecanicillium W. Gams & Zare, Ophiocordyceps Petch, Purpureocillium Luangsa-ard et al., and Torrubiella Boud. within Hypocreales. Akanthomyces neoaraneogenum (W.H. Chen, Y.F. Han, J.D. Liang, Z.Q. Liang & D.C. Jin) W.H. Chen, Y.F. Han & Z.Q. Liang, comb. nov. is also proposed here. Among the genera, Gibellula, Hevansia, Torrubiella, and Akanthomyces are exclusively or dominantly spider pathogens. Gibellula pulchra, G. leiopus, P. atypicola, A. aranearum, and T. aranicida are some of the cosmopolitan spider-pathogenic fungi. A total of twenty spider families and two harvestman families are known to be parasitized by hypocrealean fungi. Spider-pathogenic fungi are known from diverse areas of Europe, and Central and South America, but are only known from limited parts in Asia and Africa. However, east and southeast Asia shows the highest richness of spider-pathogenic fungi. Among three entomogenous families within Hypocreales, we show that the majority of the spider pathogens are distributed in Cordycipitaceae while a few in Ophiocordycipitaceae, but none in the family Clavicipitaceae. Through this review, we show that spiders constitute one of the major host groups of arthropod-associated fungi and hope a continuous interest will be generated to utilize such fungal resources through in vitro growth and extraction of useful bio-active secondary metabolites (extrolites).
Some parasitoids modify the behavior of their hosts, benefiting themselves at the host's expense. This phenomenon is called ‘manipulation’, and current research on parasitoid manipulation of host behavior tends to fall into one of three categories. First, the frequency of manipulation and the magnitude of its benefits to the parasitoid remains unclear. Basic documentation of manipulations is thus a major research focus, with especially valuable recent data coming from spiders manipulated by Polysphincta wasps. Second, for a handful of systems, we now have sufficient phylogenetic and behavioral data to begin asking questions about how manipulation evolved. Finally, the field continues to probe the mechanisms through which parasitoids manipulate host behavior, and now examines the role of parasitoid symbionts in this interaction.
Some parasites manipulate host behavior by exploiting the host's behavioral control networks. This review explores two examples of this approach using parasites from opposite ends of the size spectrum, that is, viruses and parasitic insects. The first example explores the use of the gene (egt) by some baculoviruses to deactivate the hormone 20-hydroxyecdysone. Suppressing this chemical signal prevents the expression of behaviors that could reduce viral transmission. The second example explores how a parasitic wasp uses the host's immune/neural communication system to control host behavior. When a host's manipulated behavior requires complex neural coordination, exploitation of host behavioral control systems is likely to be involved. Simpler host behaviors can be induced by damage to host tissues.
A new genus and eight new species, all with isaria-like phialides, are described in Cordycipitaceae from Thailand. The new genus, Samsoniella, is segregated from Akanthomyces based on morphological and molecular evidence. Samsoniella differs from Akanthomyces in producing orange cylindrical to clavate stromata with superficial perithecia and orange conidiophores with isaria-like phialides and white to cream conidia. A new combination for CBS 240.32, originally identified as Paecilomyces farinosus (Isaria farinosa), and CBS 262.58, originally identified as Penicillium alboaurantium, respectively, is made in Samsoniella. Two new species, Samsoniella aurantia and S. inthanonensis, are described from lepidopteran larvae. Two new species of Cordyceps, C. blackwelliae and C. lepidopterorum, were also found on coleopteran and lepidopteran larvae. Both produce isaria-like morphs with globose phialides and attenuated long necks and white mycelium in culture. The authors established a sexual-asexual link for Cordyceps javanica (= Isaria javanica) on lepidopteran larvae. Four new species, Akanthomyces kanyawimiae, A. sulphureus, A. thailandicus, and A. waltergamsii, were pathogenic on spiders, with some strains of A. kanyawimiae also found on unidentified insect larvae. These four species of Akanthomyces occur on the underside of leaves and produce white to cream white powdery conidia, whereas S. aurantia and S. inthanonensis were found in leaf litter and produce bright orange stromata and synnemata with white conidia. Another new combination, Akanthomyces ryukyuensis, is proposed. Phylogenetic analyses based on a combined data set comprising the nuc rDNA region encompassing the internal transcribed spacers 1 and 2 along with the 5.8S rDNA (ITS), nuc 28S rDNA (28S), partial sequences of translation elongation factor 1-α gene (TEF1), and the genes for RNA polymerase II largest (RPB1) and second-largest (RPB2) subunits strongly support the delimitation of these new species of Cordyceps, Akanthomyces, and in a new genus Samsoniella in Cordycipitaceae.
Some parasites alter the behaviour of their hosts. The larvae of the parasitic wasp Cotesia congregata develop within the body of the caterpillar Manduca sexta During the initial phase of wasp development, the host's behaviour remains unchanged. However, once the wasps begin to scrape their way out of the caterpillar, the caterpillar host stops feeding and moving spontaneously. We found that the caterpillar also temporarily lost sensation around the exit hole created by each emerging wasp. However, the caterpillars regained responsiveness to nociception in those areas within 1 day. The temporary reduction in skin sensitivity is probably important for wasp survival because it prevents the caterpillar from attacking the emerging wasp larvae with a defensive strike. We also found that expression of plasmatocyte spreading peptide (PSP) and spätzle genes increased in the fat body of the host during wasp emergence. This result supports the hypothesis that the exiting wasps induce a cytokine storm in their host. Injections of PSP suppressed feeding, suggesting that an augmented immune response may play a role in the suppression of host feeding. Injection of wasp larvae culture media into non-parasitized caterpillars reduced feeding, suggesting that substances secreted by the wasp larvae may help alter host behaviour.
Parasitic infection or tissue consumption by parasitoids typically leads to several phenotypic alterations in hosts, including distinct changes in behavioural, morphological, or life history traits. Some of these changes may not result solely from host responses, but actively induced changes by parasites/parasitoids to manipulate the host to acquire some benefit (e.g. parasite/parasitoid survivorship or dispersal ability). Field experiments investigating the effects of host behavioural alterations on parasite or parasitoid survivorship and the mechanisms involved in these changes are important for confirmation of behavioural manipulation. In the present study, we examined web design modification in the host spider species Cyclosa fililineata and Cyclosa morretes, which are attacked by the polysphinctine ectoparasitoid wasps Polysphincta sp. nr. purcelli and Polysphincta janzeni, respectively. We tested whether changes in orb spider web design (1) result from nutritional restrictions imposed by parasitoids and (2) increase the chances of adult wasp emergence from the cocoon. Furthermore, we describe changes in web design consistent with parasitoid larval development. Results, for both spider species, showed that web design modifications occurred only during the night preceding host spider death, and that modifications involved a reduction in the number of spirals and radii of orb webs. Food restriction did not generate web design modification, suggesting that observed changes in host behaviour resulted from direct actions of parasitoid larvae rather than as a by-product of nutritional deficiencies. Rain events were the major factor causing web rupture and subsequent parasitoid mortality. Modifications in web design reduced the frequency of web ruptures, increasing parasitoid adult emergence, and thus survivorship probability, during the pupal stage. These results confirm that web modifications by spiders are adaptive to parasitoid wasps.
The family Acroceridae (Insecta: Diptera; "Small Headed Flies") are a seldom seen yet cosmopolitan group of endoparasitoids of spiders. Recent host and distribution records are presented here for six species of acrocerids: Ogcodes borealis Cole, 1919; Ogcodes pallidipennis (Loew, 1866); Opcodes sp.; Acrocera bimaculata Loew, 1866; Turbopsebius sulphuripes (Loew, 1869); and Exetasis eickstedtae Schlinger, 1972. New hosts for each fly species are; O. borealis—Schizocosa rovneri Uetz and Dondale, 1979, Pardosa spp.; O. pallidipennis—Schizocosa rovneri, Schizocosa spp.; Ogcodes
Sp.—Anyphaena californica (Banks, 1904); Acrocera bimaculata—Coras montanus (Emerton, 1890b); T. sulphuripes—C. montanus.Detailed field measurements and behavioral observations of host spiders and fly development are described and compared with known data. Examination of these comparisons suggests that host–parasitoid relationships follow spider guild associations (i.e. ground/surface dwelling hosts or those building webs in close contact with surfaces), especially with the spider family Agelenidae. These affiliations probably result from a combination of the spider’s web building, web maintenance, hunting behaviors, and fly oviposition activities, which dispose spiders exhibiting these behaviors to greater chances for parasitoidism. These factors act in concert to increase probabilities for host–parasitoid interactions. Compiled data indicate duration of pupation may be related to ambient temperature. Evidence is presented that acrocerid larvae may alter their hosts’ behavior to increase the parasitoids’ probability of survival.