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A parasitoidal wasp (Trioxys complanatus, Aphidiidae) ovipositing into the body of a spotted alfalfa aphid.[a]

A parasitoid is a parasite, an organism that lives in close association with its host and at the host's expense, but which sooner or later kills it. Parasitoidism is one of six major evolutionary strategies within parasitism, the others being parasitic castrator, directly transmitted parasite, trophically transmitted parasite, vector-transmitted parasite, and micropredator. Parasitoidism is distinguished by the fatal prognosis for the host, which makes the strategy close to predation.

Among parasitoids, strategies range from living inside the host, allowing it to go on growing until the parasitoid emerges as an adult, to paralysing the host and living outside it. Hosts include other parasitoids, resulting in hyperparasitoidism, and in the case of oak galls, up to five levels of parasitism are possible. Some parasitoids influence their host's behaviour in ways that favour the propagation of the parasitoid.

Parasitoids are found in a variety of taxa across the insects including the Diptera, but most are in the Hymenoptera, where the ichneumons and many wasps are highly specialised for a parasitoidal way of life. Some of these parasitoidal wasps are used in biological pest control.

The biology of parasitoidism has inspired science fiction authors and scriptwriters to create numerous parasitoidal aliens that kill their human hosts, such as the alien species in Ridley Scott's 1979 film Alien.

Contents

HistoryEdit

Maria Sibylla Merian (1647–1717) was one of the first naturalists to study and depict parasitoids.[2] The term "parasitoid" was coined in 1913 by the Swedo-Finnish writer Odo Morannal Reuter,[3] and adopted in English by his reviewer, William Morton Wheeler.[4] Reuter used it to describe the strategy where the parasite develops in or on the body of a single host individual, eventually killing that host, while the adult is free-living. Since that time, the concept has been generalised and widely applied.[5]

A spectrum of strategiesEdit

 
Strategy of parasitoidism compared with typical parasite (not killing its host) and predator (killing its prey immediately).[6]

DefinitionEdit

Parasitoidism is one of six main evolutionary strategies within parasitism, the others being parasitic castrator, directly transmitted parasite, trophically transmitted parasite, vector-transmitted parasite, and micropredator. These are adaptive peaks, with many possible intermediate strategies, but organisms in many different groups have consistently converged on these six.[7][8]

Parasitoids feed on a living host which is eventually killed, typically before it can produce offspring. While some conventional parasites kill their hosts under certain conditions, they usually do not. Many species of true parasites can cause the death of their host if they are present in overwhelming numbers, the host is in poor condition, or the host's health is compromised by secondary infections. For example, blood-sucking mites sometimes overwhelm nestlings of birds such as swallows to the point that the young birds cannot fledge.[9]

In their extreme forms, conventional parasitism and parasitoidism are distinct: there is no doubt that the larva of a tarantula hawk wasp behaves more like a parasitoid, or even a predator, than a conventional parasite; and similarly the biting midges that suck blood from large insects are plainly ectoparasites; but many intermediate forms exist. At the opposite extreme, parasitoidism grades into predation. Differences between various hunting wasps provide convenient illustrations. Predatory social wasps hunt flies, caterpillars and the like, kill, cut up, and carry them to a nest to feed to their young. Similarly, some solitary wasps such as beewolves, sting prey, sometimes fatally, before saving it, usually entire, in a nest or burrow for the young to feed on. In contrast, the best-known protelean solitary hunting wasps sting prey to paralyse it before storing it for the young in the nest.[10][11] Other wasps paralyse prey in the plant or other environment in which it feeds, before laying eggs nearby; the emerging young feed on the paralysed prey in its own home.[12]

StrategiesEdit

 
A hyperparasitoid chalcid wasp on the cocoons of its host, a braconid wasp, itself a koinobiont parasitoid of Lepidoptera.

Parasitoids can be classified as either endo- or ectoparasitoids with idiobiont or koinobiont developmental strategies. Endoparasitoids live within their host's body. Ectoparasitoids feed on the host from outside. Idiobiont parasitoids prevent further development of the host after initially immobilizing it. Koinobiont parasitoids allow the host to continue its development while feeding upon it. Most ectoparasitoids are idiobiont, as the host could damage or dislodge the external parasitoid if allowed to move and or molt. Most endoparasitoids are koinobionts, giving them the advantage of a host that continue to grow larger and avoid predators.[13]

Primary parasitoids have the simplest parasitic relationship with two organisms involved: the host and the parasitoid. Hyperparasitoids are parasitoids of parasitoids. Secondary parasitoids are hyperparasitoids which use a primary parasitoid as their host. In this case there are three organisms involved. Hyperparasitoids are either facultative (can be a primary parasitoid or hyperparasitoid depending on the situation) or obligate (always develop as a hyperparasitoid). Levels of parasitoids beyond secondary also occur, especially among facultative parasitoids. In oak gall systems, there can be up to five levels of parasitism.[14] Cases in which two or more species of parasitoids simultaneously attack the same host without parasitizing each other are called multi- or multiple parasitism. In many cases, multiple parasitism still leads to the death of one or more of the parasitoids involved. If multiple parasitoids of the same species coexist in a single host, it is called superparasitism. Gregarious species purposefully lay multiple eggs or polyembryonic eggs which lead to multiple larvae in a single host. The end result of gregarious superparasitism can be a single surviving parasitoid individual or multiple surviving individuals, depending on the species. If superparasitism occurs accidentally in normally solitary species the larvae often fight among themselves until only one is left.[15]

Influence on host behaviourEdit

In another strategy, some parasitoids influence the host's behaviour in ways that favour the propagation of the parasitoid, often at the cost of the host's life. A spectacular example is the lancet liver fluke that causes host ants to die clinging to grass stalks, where grazers or birds may be expected to eat them and complete the parasitoidal fluke's life cycle in its definitive host. Similarly, as strepsipteran parasitoids of ants mature, they cause the hosts to climb high on grass stalks, positions that are risky, but favour the emergence of the strepsipterans.[16] Among pathogens of mammals, the rabies virus affects the host's central nervous system, eventually killing it, but perhaps helping to disseminate the virus by modifying the host's behaviour.[17] Among the parasitic wasps, Glyptapanteles modifies the behaviour of its host caterpillar to defend the pupae of the wasps after they emerge from the caterpillar's body.[18] The phorid fly Apocephalus borealis oviposits into the abdomen of its hosts, including honey bees, causing them to abandon their nest, flying from it at night and soon dying, allowing the next generation of flies to emerge outside the hive.[19]

Taxonomic rangeEdit

About 10% of described insects are parasitoids, in six orders: Hymenoptera, Diptera, Coleoptera, Neuroptera, Lepidoptera, and Trichoptera. The majority are wasps within the Hymenoptera; most of the others are Dipteran flies.[5][20][21]

Parasitoid waspsEdit

The many species of parasitoid wasps[22] often have remarkable life cycles.[23][24] They can be classified as either endoparasitic or ectoparasitic according to where they lay their eggs.[25] Endoparasitic wasps insert their eggs inside their host, while ectoparasitic wasps deposit theirs outside the host's body.[5] Most species of wasps attack the eggs or larvae of their host, but some attack adults. Oviposition depends on finding the host and on evading host defenses; the ovipositor is a tube-like organ used to inject eggs into hosts, sometimes as long as the wasp's body.[26][27] Hosts such as ants are often aware of the wasps' presence, making violent movements to prevent oviposition. Wasps may wait for the host to stop moving, and then attack suddenly.[28]

Parasitoid wasps face a range of obstacles to oviposition,[5] including behavioural, morphological, physiological and immunological defenses of their hosts.[29][30] To thwart this, some wasps inundate their host with their eggs so as to overload the encapsulation response;[31] others introduce a virus which interferes with the host's immune system.[32] Some parasitoid wasps locate hosts by detecting the chemicals that plants release to defend against insect herbivores.[33]

Other insectsEdit

The true flies (Diptera) include several families of parasitoids, the largest of which is the Tachinidae, along with the Pipunculidae and Conopidae. Other families of flies include some protelean species.[34] For example, some Phoridae are parasitoidal on ants.[35] Aome flesh flies are parasitoids: for instance Emblemasoma auditrix is parasitoidal on cicadas, locating its host by sound.[36]

The "twisted-wing parasites" (Strepsiptera) consists entirely of parasitoids; they usually sterilise their hosts.[37]

Two beetle families, Ripiphoridae[38][39] and Rhipiceridae, are largely parasitoids, as are Aleochara rove beetles.[34][40]

In biological pest controlEdit

 
Encarsia formosa, an endoparasitic chalcid wasp, bred commercially to control whitefly in greenhouses

Parasitoids are among the most widely used biological control agents. Classic biological pest control using natural enemies of pests (parasitoids or predators) is extremely cost-effective, the cost/benefit ratio for classic control being 1:250, but more variable in its effects than pesticides; it reduces rather than eliminates pests. The cost/benefit ratio for screening natural enemies is similarly far higher than for screening chemicals: 1:30 against 1:5 respectively, since search for suitable natural enemies can be guided accurately with ecological knowledge. Natural enemies are more difficult to produce and to distribute than chemicals, as they have a shelf life of weeks at most; and they face a commercial obstacle, namely that they cannot be patented.[41][42]

From the point of view of the farmer or horticulturalist, the most important groups are the ichneumonid wasps, which prey mainly on caterpillars of butterflies and moths; braconid wasps, which attack caterpillars and a wide range of other insects including greenfly; chalcid wasps, which parasitise eggs and larvae of greenfly, whitefly, cabbage caterpillars, and scale insects; and tachinid flies, which parasitize a wide range of insects including caterpillars, adult and larval beetles, and true bugs.[43] Commercially, there are two types of rearing systems: short-term seasonal daily output with high production of parasitoids per day, and long-term year-round low daily output with a range in production of 4–1000 million female parasitoids per week, to meet demand for suitable parasitoids for different crops.[44][45]

In cultureEdit

Charles DarwinEdit

Parasitoids influenced the thinking of Charles Darwin,[b] who wrote in an 1860 letter to the American naturalist Asa Gray: "I cannot persuade myself that a beneficent and omnipotent God would have designedly created parasitic wasps with the express intention of their feeding within the living bodies of Caterpillars."[47] The palaeontologist Donald Prothero notes that religiously-minded people of the Victorian era, including Darwin, were horrified by this instance of evident cruelty in nature, particularly noticeable in the Ichneumonidae wasps.[48]

In science fictionEdit

Parasitoids have inspired science fiction authors and screenwriters to create disgusting and terrifying parasitic alien species that kill their human hosts.[49] One of the best-known is the alien species in Ridley Scott's 1979 film Alien.[50][51] In one scene of that film, an alien bursts out of a man's chest, killing him. The scene was filmed in a single take, and the startled reaction of the actors was genuine.[52] The molecular biologist Alex Sercel, writing in Signal to Noise Magazine, compares "the biology of the [Alien] Xenomorphs to parasitoid wasps and nematomorph worms from Earth to illustrate how close to reality the biology of these aliens is and to discuss this exceptional instance of science inspiring artists".[53] Sercel notes that the way the Xenomorph grasps a human's face to implant its embryo is comparable to the way a parasitoid wasp lays its eggs in a living host. He further compares the Xenomorph life-cycle to that of the nematomorph Paragordius tricuspidatus which grows to fill its host's body cavity before bursting out and killing it.[53] Alistair Dove, on the science website Deep Sea News, writes that there are multiple parallels with parasitoids, though there are in his view more disturbing life cycles in real biology. In his view, the parallels include the placing of an embryo in the host; its growth in the host; the resulting death of the host; and alternating generations, as in the Digenea (parasitoidal trematodes).[54] The social anthropologist Marika Moisseeff argues that "The parasitical and swarming aspects of insect reproduction make these animals favored bad-guy characters in Hollywood science fiction. The battle of culture against nature is depicted as an unending combat between humanity and insect-like extraterrestrial species that tend to parasitize human beings in order to reproduce."[49] The Encyclopedia of Science Fiction lists many instances of "parasitism", often causing the host's death, in science fiction.[55]

NotesEdit

  1. ^ The species has been introduced to Australia to control the spotted alfalfa aphid.[1]
  2. ^ Darwin mentions "parasitic" wasps in On the Origin of Species, Chapter 7, page 218.[46]

ReferencesEdit

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