Int.J.Curr.Microbiol.App.Sci (2020) 9(7): 861-870

International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume 9 Number 7 (2020) Journal homepage: http://www.ijcmas.com

Review Article https://doi.org/10.20546/ijcmas.2020.907.100

Physiology of Neuroparasitism in

N. Vijayaakshayakumar*, P. Yasodha and C. G. L. Justin

Department of Plant Protection, Anbil Dharmalingam Agricultural College & Research Institute, TNAU, Tiruchirappalli, TamilNadu, India

*Corresponding author

ABSTRACT

Parasites have evolved to manipulate the behavior of the host species, in which they dwell for their food and living. Since, most of the invertebrates comes under class Insecta, the chance of parasitization is always higher. In most cases, the manipulation occurs by influencing the nervous system of insects. The upcoming K e yw or ds biological study, dealing with the manipulation of nervous system of insects by

the parasites is neuroparasitology. From microscopic viruses to macroscopic Neuroparasitology , Neuroparasit ism in worms, heterogeneity of parasites have evolved to become parasites (uniquely, Insects parasitic wasps). It is striking that the manipulation spotted doesn‘t require direct entry into the brain and can occur even when the parasite is present external to the

Article Info body or even at a distance from the host. The spatial view of manipulation would provide an integrated approach to investigate such interactions. Incorporation of Accepted: different approaches from basic natural history to improved imaging techniques, 08 June 2020 omics and experiments will come up with new aspects in neuroparasitology. It is Available Online: also recommended that for researchers interested in impending mechanism of 10 July 2020 behaviors, studies of parasites that have evolved to manipulate such behavior is of an important value in future to ascertain the host parasite interaction.

Introduction normal biochemical mechanisms of other organisms, that assists the parasites in its Parasites are living organisms which depends survival and transmission (Godfray and on other organism, the host, for its survival. Godfray, 1994). Due to its high reproductive potential, capacity to flight, and reduced size of insects, Some insects have evolved to gain assist and they are the dominant species in this planet, manipulate the behavior of the other insects of and have the chance to interact with the same class (Askew, 1971). Changes in the parasitic organisms than other species behavior of host organism by the parasites, (Moore, 2002). Due to evolution, some may be due to the direct effects on the central parasite has gained the ability to disrupt the nervous system and associated muscular

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system or indirectly manipulating the immune developmental pathway that underlie the system and host‘s metabolism (Hughes and behavior manipulation. More precisely, such Libersat, 2018). investigations provide new ideas into the mechanism of parasites spread and the Host behavior is an extended phenotype of the mechanism by which the parasitic insects parasite (Dawkins, 1982).Parasite-influenced have evolved into neural manipulators, changes in the host phenotypes were mostly encountering the existing nervous system in adaptable for the parasitic species (Poulin, the host (Hughes and Libersat, 2018). 1998), in case of confirming the suitable location for optimal release of parasites and Different mechanisms of host behavior its progenies (Maitland, 1994), the survival manipulation was increased by providing protection (Brodeur and McNeil, 1989) and also the Regardless of numerous examples of host- behavior was altered, that they were likely parasite interaction, there are only few eaten by other predatory insects, by acting as experimental examples which suggest the an intermediate host (Curtis, 1987). The behavior manipulation of host by the parasite. amount of manipulation diversified from a This alteration in the host‘s behavior, has slight variation in the pre-existing behavior seems to benefit the parasite and not the host (Rogers and Bates, 2007) to an entirely (Hughes and Libersat, 2018). unique behavior that are never seen in unparasitized hosts (Eberhard, 2000). The different mechanism by which the host Edwards and Weaver (2000) noted that behavior is manipulated was grouped as ―parasitoid wasps have evolved a better ‗understanding‘ of the subtleties and Neurological command from an extent regulation of the endocrine systems of their Approaching brain and influencing through insect hosts than is at present understood by ovipositor insect physiologists‖. Commanding brain while binding with the host Neuroparasitology is the budding branch of Influencing the host behavior during biology which deals with the study of departure parasites which are capable of Ruling the brain by residing in body cavity controlling/influencing the nervous system of Relocating to the brain to manipulate the host and its functions (Adamo and behavior Webster, 2013). Many organisms, including viruses, bacteria, fungi, apicomplexans, Neurological command from an extent diverse worms, and even other insects, have evolved to control the insect brain, because it A typical example of mutualism is the is totally free from the host‘s immune systems attraction of ants to honey dew secretions of (Galea et al., 2007) or it provides direct homopteran bugs and in exchange provide access to the insects to induce the protection from the predators. Alike this, ants manipulation (Webster, 2007). protect the Lycaeind caterpillars from predators and they were rewarded with sugar By unveiling the mechanisms, by which the rich secretions from the caterpillar (Pierce et parasites induce behavioral changes, we can al., 2002). Ants have a dorsal nectary organ, obtain new vision in the biology and to on the seventh abdominal segment, which discover new genes, metabolites, proteins and releases a sugar rich substance for the

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attendant ants. In the eighth segment, they in forelegs for a period of 1-3 minutes. For have tentacle organs, which releases a volatile this transient paralysis, the wasp uses the compound that resembles the alarm approach of venom-induced synaptic block pheromone of the ants, and keep them through chloride channel activation, and the aggressive around the caterpillar. In addition venom contains high level of inhibitory to these, the caterpillar produce surface neurotransmitters GABA, β-alanine and chemicals, which is non-volatile, spread over taurine compounds (Moore et al., 2006). This the cuticle, suppress the ant aggression by facilitates the second sting into the head, mimicking the brood pheromone of ants and through neck membrane, which induces a treat them as their own brood species (Akino long-term complete paralysis of the host. et al., 1999). A long-lasting immobility in cockroach was A research study conducted by Hojo et al., achieved by the wasp, by injecting the venom (2015) focused on ants (Pristomyrmex directly into supra-oesophageal ganglion punctatus) which tend the caterpillar (brain) and the sub-oesophageal ganglion. (Narathura japonica). Ants provide Since the insect brain is protected by the protection to the caterpillar, and in change the perineurium (―blood-brain barrier‖), the brain ants were rewarded with the sugary secretions cells are protected with restriction to entry of from the dorsal nectary organ. The secretions different compounds (Chapman, 2013). It is from the caterpillar made the attendant ants, now visible that, the ovipositor of the wasp more aggressive and less possible to move was developed exclusively to identify and away from the caterpillar, which protects the target the brain cells thereby avoiding all host from other predators. This change in the other cells in the head region. This was behavior was due to the changes in dopamine achieved due to the presence of well- level, as reduced level of dopamine was developed mechanoreceptors (campaniform observed in the ants treated with the sensilla and dome-shaped sensilla) in the secretions of caterpillar. The ants continued to ovipositor (Gal et al., 2014). Following the protect the caterpillar even when the sugary stung of wasp, cockroach performs rewards were stopped. From here, mutualism continuous grooming for about 30 minutes. was changed into . So, the This immoderate grooming has been noted caterpillar manipulated its host ants to move only after the sting on head and cannot be less likely away from them, and gain attributed to stress or to contamination of the protection from the predators and parasitoids. body surface or to systemic or peripheral effects. This indicated that the venom was Approaching brain and influencing influencing the nervous system for grooming, through ovipositor by stimulating dopamine receptors in the cockroach (Weisel-Eichler et al., 1999). Solitary wasps provoke paralysis in their hosts by stinging with their ovipositor. This In addition to this, the stung cockroach immobility in host is due to the entry of showed a reduced responsiveness to venom into the nervous system of the host. mechanical and sensitive stimuli that The parasitoid jewel wasp (Ampulex generally induce an escape response in an compressa) uses cockroaches (Periplaneta alert cockroach. americana) as a host for its progenies (Piek et al., 1989). The wasp generally stings the host After stinging and paralyzing the host, the twice, first in the thorax (prothoracic wasp uses its strong mandibles, to breaks off ganglion) which induces short-term paralysis the cockroach‘s antennae and to drink 863

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hemolymph from the cut end. Notably, the Eventually, the spider returns to its usual cockroach doesn‘t show any defensive doing. Till the next fortnight, it builds normal behavior in response to this stimulus. Such orb webs to capture prey, the wasp‘s egg defensive behaviors to pain were termed as hatches and the grub feeds by sucking the nocifensive. The unresponsiveness of the spider‘s haemolymph. A day before pupation, cockroach to stimuli allows the wasp to the grub releases an unidentified substance, handle the cockroach further, lead it to which influence the spider to produce a burrow, and lay an egg on the cockroach‘s distinctive ―cocoon web‖, different from the cuticle (Hughes and Libersat, 2018). normal orb web. This cocoon web provides durable support to the wasp to hang This prolonged behavioral change may be due down and thus to prevent the hyperparasitism to the results of venom-mediated changes in (Eberhard, 2000). the neurochemistry of the brain. The venom compounds bind with the cerebral ganglia Larva of ichneumonid wasp Zatypotaper proteins of synapsis and presumably inhibit contatoria, performed species-specific the pre- and post-synaptic conduction in the manipulation of theridiid spiders, Neottiurabi brain (Kaiser et al., 2019). This precise maculata and Theridion varians. Shortly positioning of the venom and eggs in the before the pupation, the larva induces the brain of the host by parasite, has increased the host‘s normal foraging and web spinning fitness of the parasite, by preventing the activity, to produce a special web structure, encounter with specialized cells, called which are either dense in nature (N. macrophages (Askew, 1971). bimaculata), or a cupola-like structure (T. varians). These induced that the webbing Commanding brain while binding with the behaviors were naturally present in the spider host itself, but occurred only at the time of specific life history periods, like, before Some parasitic wasps which are ectoparasites, overwintering. Due to the effect of parasite, lays its eggs on the host body surface. The these modified webbing patterns are obtained emerging grubs, bore the cuticle and obtain in the summer time itself, to protect the wasp the haemolymph. At the completion of their (Korenko and Pekár, 2011). parasitic stage, they manipulate the behavior of the host by remaining on the body. These Influencing the host behavior during wasps are koinobiont ectoparasitoids which departure influence the web spinning pattern of the host spiders (Kloss et al., 2016). Since spiders are So far, we have seen examples on behavior the natural predators, these wasps have manipulation ofhost by parasites being evolved to attack and kill the predatory external to the host. Now, the parasites are spiders, hence can be termed as predatory internal to the host, entering into the body parasitoids. cavity, feeding on the internal content of the host, and emerging from the body before the The female ichneumonid wasp, changes occur. Cotesia glomerate, a braconid Hymenoepimecis sp. attacks the spider wasp is an endoparasite on different Plesiometa argyra at the center of its orb web. Lepidoperan larvae. The wasp stings the spider‘s mouth leading to temporary paralysis which helps the wasp to The behavior manipulation was observed lay an egg on the spider‘s abdomen. when encountered with the wasp. The wasp

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lays eggs inside the body cavity of the host, told before, there is no residing sibling to and the emerging progenies feed on the induce this host, how this manipulation can be internal content. At the time of pupation, they occurred? The resulting manipulation was due exit the host to pupate. At this step, the to the injection of virus Dinocampus behavior of the parasitized larva was changed. coccinellae paralysis virus (DcPV) by the At the time of parasitoid emergence, the wasp into the host, during oviposition along parasitized larva has reduced feeding and the with the eggs. The presence of virus particles metamorphosis is stopped to make the host in host, induces an antiviral immune response. remain in the pre-pupal stage (Beckage, Due to the down regulation of multiple genes 1985). Transient paralysis of the host, makes involved in immune response, the host‘s the pupating wasp to emerge and spin cocoon nervous tissues allow DcPV neurotropism without interrupting host body movements. (ability to invade and live in neural tissue). Host bleeding was prevented by plugging the Later, the accumulation of phagosomes and emergence hole with their 2nd or 3rd lysosomes, re-establish the immune system sibling (Smith and Smilowitz, 1976). The and eliminate the virus from the body, before parasitoid cocoons are now vulnerable to which the virus gets replicated in host. Then, hyperparasitism. So, the host was induced to elimination of high load of virus will lead to make vigorous head swings to snap front and neuropathy which triggers the paralysis in the back, biting and to secrete fluid droplets, host. which makes the hyperparasites difficult to attack the wasp cocoon. Besides, the host DcPV belongs to Iflavirus group, which was produces a dense webbing and make a silk first documented in beneficial insects like mat, that attaches the cocoon strongly with silkworm and honeybees. This was highly the substrate, and makes the host selection pathogenic and believed to be the cause for process tedious for the hyperparasites colony collapse disorder in honeybees (van (Brodeur and Vet, 1994). A similar change Oers, 2010). This virus is unique, that it was observed in Glyptapanteles sp. and its mainly replicates in the oviduct of female caterpillar host Thyrinteina leucocerae. In the wasp and produced in abundance to be field condition, the parasitized host have injected along with the eggs during shown two fold reduction in the mortality of oviposition into the host (Beckage and the wasp cocoons (Maure et al., 2013). Drezen, 2011). Due to these factors, the pathogenic effects are low in wasps. Another example is the manipulation of the Similarly, the manipulation of lepidopteran ladybird beetle host (Coccinella larvae by the bauculoviruses causes the septumpuncta) by the braconid wasp affected larva to remain in the exposed foliage (Dinocampus coccinellae) while leaving the of plants when they die (―Wipfelkrankheit‖), host, and without the help of sibling wasps, as which enhances the spread of the virions from above (Dheilly et al., 2015). The the dead cadavers (Mehlhorn, 2015). A study entomoparsitism of C. septumpunctata by the has proved that this may be due to the wasp leads to induce protection for the expression of baculovirus gene, ecdysteroid pupating wasp (Triltsch, 1996). The single uridine 5´-diphosphate (UDP)– wasp grub develops inside the host and after glucosyltransferase (egt) encodes the enzyme 20 days emerge out to pupate. (EGT), that inactivates the host‘s moulting hormone 20-hydroxyecdysone (20E), and After the emergence, the host remains alive induced death at the elevated positions but paralyzed, twitching its body to protect (Hoover et al., 2011, Hughes, 2013). the pupating wasp from predatory insects. As 865

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Ruling the brain by residing in body cavity manipulation, the fungus certainly kills the ant and it is done outside the colony, because The parasites are capable of controlling the ants can eliminate the dead mates out and for host brain, without direct contact with the the development of perithecia and spore brain. Classic examples of this mechanism are dispersal. The infected ants behaved as the parasitic nematodes and fungus, that have zombies, showing random walking patterns evolved to produce suicidal behavior in the and they bite the leaf veins hard by piercing hosts. Adult male and female nematodes are through mandibles. Because of unknown free living in aquatic ecosystem whereas the metabolite production or due to the high juvenile forms are parasitic in terrestrial density of the spores inside the head, the insects which becomes infected through the muscles in the mandibles were atrophied and ingestion of parasitic larva (Schmidt-Rhaesa leads to death grips after the death of host and Ehrmann, 2001, Hanelt and Janovy Jr, (Andersen et al., 2009). Future clarification in 1999). During the development, the parasitic this study is awaited. nematode grows throughout the body cavity and occupies all the body parts except head Relocating to the brain to manipulate and legs. Mature nematodes manipulate the behavior behavior of their host by making them search for water and jump into it (Dawkins, 1990, In the above discussed examples, the jewel Thomas and Poulin, 1998). The cricket, wasp envenomated the brain of cockroach by Nemobius sylvestris was infected by the directly injecting ovipositor into the brain or nematode Paragordius tricuspidatus (Thomas in the case of D. coccinellae, the virus et al., 2002). By distinguishing the host and (DcPV) was replicated in the brain cells. But parasite proteomes during the intimation of in some cases, the parasite present in the water-seeking behavior, it was found that the haemolymph was carried to the brain through parasite produces molecules from Wnt family circulatory system (heart), which helps in the that may act directly on the development of migration of the parasite by pumping the central nervous system (CNS), which causes insect blood. An example for this type was the differential expression of proteins specifically behavior manipulation elicited by the liver linked to neurogenesis, circadian rhythm and fluke (trematode) in ants, the second neurotransmitter activities (Biron et al., intermediate host, for the completion of its 2006). lifecycle. The adult stage of liver fluke (Dicrocoelium dendriticum) occupies the liver Additional reference was the interaction of the mammalian host (cattles, humans). between the fungus Ophiocordyceps After fertilization, the eggs are produced and unilateralis and its host worker ant excreted with the host feces. The eggs were Camponotus leonardi which expressed the inserted into snails (preceding host), in which death grip behavior soon before death to assist the eggs developed into cercariae (free- parasite reproduction and spread (Hughes et swimming larval stage). The cercariae were al., 2011). During foraging, the worker ants excreted via snail slime, which was fed by were infected by the spores, attach and ants (intermediate host). Most of the liver penetrate the cuticle and progress inside the fluke cercariae, encysts in the ant body (Hughes et al., 2009). The fruiting body, haemolymph, while one or two move to ants perithecium, was formed as a large stalk from nervous system, persuading the ants to climb back of the head, from which the spores were and bite the grass or simply remain spread (Evans and Samson, 1984). For this motionless (Romig et al., 1980). The former

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How to cite this article:

Vijayaakshayakumar. N., P. Yasodha and Justin. C. G. L. 2020. Physiology of Neuroparasitism in Insects. Int.J.Curr.Microbiol.App.Sci. 9(07): 861-870. doi: https://doi.org/10.20546/ijcmas.2020.907.100

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