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Parasitism

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A Lithognathus fish with a parasitic isopod, Cymothoa exigua, one of many fish parasites

In biology, parasitism is a relationship between species, where one organism, the parasite, lives on or in another organism, the host, causing it some harm, and is adapted structurally to this way of life.[1] The entomologist E. O. Wilson has characterised parasites as "predators that eat prey in units of less than one".[2] Parasites include protozoa such as the agents of malaria, sleeping sickness, and amoebic dysentery; animals such as hookworms, lice, and mosquitoes; plants such as mistletoe and dodder; and fungi such as honey fungus and ringworm. There are six major evolutionary strategies within parasitism, namely parasitic castrator, directly transmitted parasite, trophically transmitted parasite, vector-transmitted parasite, parasitoid, and micropredator.

Unlike predators, parasites, with the exception of parasitoids, typically do not kill their host, are generally much smaller than their host, and often live in or on their host for an extended period. Parasitism is a type of consumer-resource interaction.[3] Parasites of animals show a high degree of specialization, and reproduce at a faster rate than their hosts. Classic examples include interactions between vertebrate hosts and tapeworms, flukes, the Plasmodium species, and fleas.

Parasites reduce host biological fitness by general or specialized pathology, from parasitic castration and impairment of secondary sex characteristics to modification of host behavior. Parasites increase their own fitness by exploiting hosts for resources necessary for their survival, in particular transmission. Although parasitism is often unambiguous, it is part of a spectrum of interactions between species, grading via parasitoidism into predation, through evolution into mutualism, and in some fungi, shading into being saprophytic.

People have known about parasites such as roundworms and tapeworms since ancient Egypt, Greece, and Rome. In Early Modern times, Antonie van Leeuwenhoek observed Giardia lamblia in his microscope in 1681, while Francesco Redi described endo- and ectoparasites including sheep liver fluke and ticks. Modern parasitology developed in the 19th century. In human culture, parasitism has negative connotations. These were exploited to satirical effect in Jonathan Swift's 1733 poem "On Poetry: A Rhapsody", comparing poets to hyperparasitical "vermin". In fiction, Bram Stoker's 1897 Gothic horror novel Dracula and its many later adaptations featured a blood-drinking parasite. Ridley Scott's 1979 film Alien was one of many works of science fiction to feature a terrifying[4] parasitic alien species.

Etymology[edit]

First used in English in 1539, the word parasite comes from the Medieval French parasite, from the Latin parasitus, the latinisation of the Greek παράσιτος (parasitos), "one who eats at the table of another"[5] and that from παρά (para), "beside, by"[6] + σῖτος (sitos), "wheat", hence "food".[7] The related term parasitism appears in English from 1611.[8]

Evolutionary strategies[edit]

Parasitism is one of several kinds of symbiosis, close and persistent biological interactions. It is distinguished from commensalism and mutualism by the harm done to the host by the parasite.[9] Predation is not generally considered a symbiosis as the interaction is brief, but the entomologist E. O. Wilson has characterised parasites as "predators that eat prey in units of less than one".[2] Within that scope are many possible ways of life. Parasites are classified in a variety of different but overlapping schemes, based on their interactions with their hosts and on their life cycles. An obligate parasite is totally dependent on the host to complete its life cycle, while a facultative parasite is not. A direct parasite has only one host while an indirect parasite has multiple hosts. For indirect parasites, there will always be a definitive host and an intermediate host.[10][11]

Basic strategies[edit]

The parasitic castrator Sacculina carcini (highlighted) attached to a crab

There are six basic evolutionary strategies within parasitism, namely parasitic castrator, directly transmitted parasite, trophically transmitted parasite, vector-transmitted parasite, parasitoid, and micropredator. These apply to parasites whose hosts are plants as well as animals:[12][13] These strategies are adaptive peaks; many intermediate strategies such as mesoparasitism (between endo- and ectoparasitism) are possible,[14] but organisms in many different groups have consistently converged on these six, which are evolutionarily stable.[12]

Parasitic castrators[edit]

Human head lice are obligate directly-transmitted ectoparasites.

Parasitic castrators destroy their hosts' ability to reproduce, diverting the energy that would have gone into reproduction into host growth, with gigantism a common outcome. The hosts' other systems are left intact, allowing it to survive and sustain the parasite.[12] Parasitic crustaceans such as Sacculina specifically cause damage to the gonads of their host crabs. In the case of Sacculina, the testes of over two thirds of their crab hosts degenerate sufficiently for these male crabs to have gained female secondary sex characteristics such as broader abdomens, smaller claws (chelae) and egg-grasping appendages.[15] The trematode Zoogonus lasius causes parasitic castration of the intertidal snail Ilyanassa obsoleta; other trematodes directly or indirectly castrate other species of snail.[15]

Directly transmitted ectoparasites[edit]

Directly transmitted ectoparasites, living on the outside of their hosts, rely on chance encounters with members of their host species to feed and reproduce. They may spread from one host to another through skin-to-skin contact, or lie dormant until a host steps on or brushes against them.[12] Examples include lice, fleas, and ticks.[16]

Schistosoma mansoni is an obligate endoparasite, causing schistosomiasis (bilharzia).

Trophically transmitted endoparasites[edit]

Trophically transmitted endoparasites such as many parasitic worms (helminths) have a life cycle involving two or more hosts. In their juvenile stages, they infect and often encyst in the intermediate host. When this animal is eaten by a predator, the definitive host, the parasite survives the digestion process and matures into an adult; some live as intestinal parasites, others in other intercellular spaces within the body. Some parasites modify the behavior of their intermediate hosts, increasing their chances of being eaten by a predator.[12] Coinfection by multiple parasites is common.[17] With autoinfection, the infection of a primary host with a helminth such as Strongyloides stercoralis, the whole of the parasite's life cycle takes place in a single organism.[18]

Vector-transmitted endoparasites[edit]

The vector-transmitted protozoan parasite Trypanosoma among human red blood cells

Vector-transmitted endoparasites rely on a third party to carry them from one host to another. These are often microscopic non-animal parasites, namely protozoa, bacteria, or viruses, often living inside the cells of their hosts as disease-causing pathogens. Their vectors are mostly parasitic arthropods such as fleas, lice, ticks and mosquitoes.[12][19]

Parasitoids[edit]

Parasitoids are insects which sooner or later kill their hosts, so this form of parasitism is close to predation. The great majority of parasitoids are hymenopterans, parasitoid wasps. They can be divided into two groups, idiobionts and koinobionts, differing in their treatment of their hosts.[20]

Idiobiont parasitoids are usually ectoparasites, stinging their often large prey on capture, either killing them outright or paralyzing them immediately. The immobilised prey is then carried to a nest, sometimes alongside other prey if they are not individually large enough to support a parasitoid throughout its development. An egg is laid on top of the prey, and the nest is then sealed. The parasitoid develops rapidly through its larval and pupal stages, feeding on the provisions left for it.[20]

Koinobiont parasitoids are usually endoparasites, laying their eggs inside young hosts, usually larvae. These are allowed to go on growing, so the host and parasitoid develop together for an extended period. Some koinobionts regulate their host's development with hormones, for example preventing it from pupating or making it moult whenever the parasitoid is ready to moult.[20]

Micropredators[edit]

Mosquitoes are micropredators, and important vectors of disease.

Micropredators actively hunt for hosts, like traditional predators. However, they choose hosts that are large but unable to resist attack. For example, mosquitoes attack animals too slow to protect themselves from their bite, and serve as vectors of diseases caused by protozoan and other parasites.[12] Similarly, phytophagous scale insects, aphids, and caterpillars attack much larger plants, and serve as vectors of bacteria, fungi and viruses causing plant diseases, and plants defoliated by caterpillars may die, as in parasitoidism. Female scale insects are unable to move, so they are obligate parasites, permanently attached to their hosts.[13]

Variations[edit]

Among the many variations on parasitic strategies are hyperparasitism,[21] social parasitism,[22] brood parasitism,[23] kleptoparasitism,[24] and sexual parasitism.[25]

Hyperparasitism[edit]

Hyperparasites feed on another parasite, as exemplified by protozoa living in helminth parasites,[21] or facultative or obligate parasitoids whose hosts are either parasites or parasitoids.[12][20] Another variant is adelpho-parasitism, where the host species is closely related to the parasite, often in same family or genus, as in the citrus blackfly parasitoid, Encarsia perplexa, unmated females of which may lay haploid eggs in the fully developed larvae of their own species, producing male offspring,[26] while the marine worm Bonellia viridis has a similar reproductive strategy, although the larvae are planktonic.[27]

Parasitism can take the form of isolated cheating or exploitation among more generalized mutualistic interactions. For example, broad classes of plants and fungi exchange carbon and nutrients in common mutualistic mycorrhizal relationships; however, some myco-heterotrophic plants cheat by taking carbon from a fungus rather than donating it.[28]

Social parasitism[edit]

Social parasites take advantage of interactions between members of social organisms such as ants, termites, and bumblebees. Examples include the large blue butterfly, Phengaris arion, its larvae employing ant mimicry (myrmecomorphy) to parasitize certain ants,[22] Bombus bohemicus, a bumblebee which invades the hives of other bees and takes over reproduction while their young are raised by host workers, and Melipona scutellaris, a eusocial bee whose virgin queens escape killer workers and invade another colony without a queen.[29] An extreme example of social parasitism is found in the ant Tetramorium inquilinum, an obligate parasite which lives exclusively on the backs of other Tetramorium ants.[30] Emery's rule notes that social parasites tend to be closely related to their hosts, often being in the same genus.[31][32]

Intraspecific social parasitism occurs in parasitic nursing, where some individual young take milk from unrelated females. In wedge-capped capuchins, higher ranking females sometimes take milk from low ranking females without any reciprocation.[33]

Brood parasitism[edit]

In brood parasitism, the hosts behave as unwitting babysitters as they raise the young as their own. Brood parasites include birds in different families such as cowbirds, whydahs, cuckoos, and black-headed ducks. These do not build nests of their own, but leave their eggs in nests of other species. The eggs of some brood parasites mimic those of their hosts, implying selection by the hosts against parasitic eggs.[23][34] The adult female European cuckoo further mimics a predator, the European sparrowhawk, giving her time to lay her eggs in the host's nest unobserved.[35]

Kleptoparasitism[edit]

In kleptoparasitism (from Greek κλέπτης (kleptēs), "thief"), parasites steal food gathered by the host. The parasitism is often on close relatives, whether within the same species or between species in the same genus or family. For instance, the many lineages of cuckoo bees lay their eggs in the nest cells of other bees in the same family.[24] Kleptoparasitism is uncommon but conspicuous in birds; some such as skuas are specialised in pirating food from other seabirds, relentlessly chasing them down until they disgorge their catch.[36]

Sexual parasitism[edit]

In many animals, males are much smaller than females. In some species of anglerfish, such as Ceratias holboelli, the males are so small they have become sexual parasites, wholly dependent on females of their own species for survival, and unable to fend for themselves. The female nourishes the male and protects him from predators, while the male gives nothing back except the sperm that the female needs to produce the next generation.[25]

Taxonomic range[edit]

Head (scolex) of tapeworm Taenia solium, an intestinal parasite, has hooks and suckers to attach to its host.

Parasitism occurs in a wide range of organisms, including animals,[37] plants,[38] fungi,[39] protozoa,[40] bacteria,[41] and viruses.[42]

Animals[edit]

Parasitism is widespread in the animal kingdom, and has evolved independently from free-living forms hundreds of times.[12] Many species of helminth including trematodes and cestodes have complex life-cycles involving two or more hosts. By far the largest group is the parasitoid wasps in the Hymenoptera.[12] The phyla and classes with the largest numbers of parasitic species are listed in the table. Numbers are conservative minimum estimates. The columns for Endo- and Ecto-parasitism refer to the definitive host, as documented in the Vertebrate and Invertebrate columns.[37]

Cuscuta (a dodder), a stem holoparasite, on an acacia tree

Plants[edit]

A parasitic plant derives some (hemiparasites such as mistletoe) or all of its nutritional requirements (holoparasites such as dodder) from another living plant. They make up about 1% of angiosperms and are in almost every biome in the world.[38] All parasitic plants have modified roots, haustoria, which penetrate the host plants, connecting them to the conductive system – either the xylem, the phloem, or both. This provides them with the ability to extract water and nutrients from the host. Parasitic plants are classified depending on where the parasitic plant latches onto the host – stem or root – and the amount of nutrients it requires. Since holoparasites have no chlorophyll and therefore cannot make food for themselves by photosynthesis, they are always obligate parasites, deriving all their food from their hosts.[38] Some parasitic plants can locate their host plants by detecting chemicals in the air or soil given off by host shoots or roots, respectively. About 4,500 species of parasitic plant in approximately 20 families of flowering plants are known.[44][38]

Species within Orobanchaceae (broomrapes) are some of the most economically destructive species on Earth. Species of Striga (witchweeds) are estimated to cost billions of dollars a year in crop yield loss annually, infesting over 50 million hectares of cultivated land within Sub-Saharan Africa alone. Striga infects both grasses and grains, including corn, rice and sorghum, undoubtedly some of the most important food crops. Orobanche also threatens a wide range of important crops, including peas, chickpeas, tomatoes, carrots, and varieties of the genus Brassica (cabbages). Yield loss from Orobanche can reach 100%; despite extensive research, no method of control has been entirely successful.[45]

The honey fungus, Armillaria mellea, is a parasite of trees, and a saprophyte feeding on the trees it has killed.

Fungi[edit]

Parasitic fungi derive some or all of their nutritional requirements from plants, other fungi, or animals, and unlike mycorrhizal fungi which have a mutualistic relationship with their host plants, they are pathogenic. For example, the honey fungi in the genus Armillaria grow in the roots of a wide variety of trees, and eventually kill them. They then continue to live in the dead wood, feeding saprophytically.[39]

Borrelia burgdorferi, the bacterium that causes Lyme disease, is transmitted by Ixodes ticks.

Protozoa[edit]

Protozoa such as Plasmodium, Trypanosoma, and Giardia[46] are endoparasitic. They cause serious diseases in vertebrates including humans – in these examples, malaria, sleeping sickness, and a form of amoebic dysentery respectively – and have complex life-cycles.[40]

Bacteria[edit]

Many bacteria are parasitic, though they are generally thought of as pathogens (causes of disease) instead.[41] Parasitic bacteria are extremely diverse, and infect their hosts by a variety of routes. To give a few examples, Bacillus anthracis, the cause of anthrax, is spread by contact with infected domestic animals; the bacillus's spores, which can survive for years outside the body, can enter a host through an abrasion or may be inhaled. Borrelia, the cause of Lyme disease and relapsing fever, is transmitted by a vector, ticks of the genus Ixodes, from the diseases' reservoirs in animals such as deer. Campylobacter jejuni, a cause of severe enteritis (gut inflammation), is spread by the fecal-oral route from animals, or by eating insufficiently cooked poultry, or by contaminated water. Haemophilus influenzae, an agent of bacterial meningitis and respiratory tract infections such as influenza and bronchitis, is transmitted by droplet contact. Treponema pallidum, the cause of syphilis, is spread by sexual intercourse.[47]

Enterobacteria phage T4 is a bacteriophage virus. It infects its host, Escherichia coli, by injecting its DNA through its tail, which attaches to the bacterium's surface.

Viruses[edit]

Viruses are obligate intracellular parasites, characterized by extremely limited biological function, to the point where, while they are evidently able to infect all other organisms from bacteria and archaea to animals, plants and fungi, it is unclear whether they can themselves be described as living. Viruses consist of a strip of genetic material (DNA or RNA), covered in a protein coat and sometimes a lipid envelope. They thus lack all the usual machinery of the cell such as enzymes, relying entirely on the host cell's ability to replicate DNA and synthesise proteins. Most viruses are bacteriophages, infecting bacteria, and it is possible that viruses are both extremely ancient, being at least as old as the first cells, and polyphyletic, different groups of viruses having evolved from several entirely unrelated ancestors.[42][48][49][50]

Transmission[edit]

Life cycle of Entamoeba histolytica, an anaerobic parasitic protozoan transmitted by the fecal-oral route

Parasites use a variety of methods to infect their hosts, including physical contact, the fecal-oral route, free-living infectious stages, and insect vectors, suiting their differing hosts.[51] Examples to illustrate some of the possible combinations are given in the table.

Examples of transmission methods in parasite-host relationships[51]
Parasite Host Transmission method Ecological context
Gyrodactylus turnbulli
(a trematode)
Poecilia reticulata
(guppy)
physical contact social behavior
Nematodes
e.g. Strongyloides
Macaca fuscata
(Japanese macaque)
fecal-oral

social behavior (grooming)

Heligomosomoides
(a nematode)
Apodemus flavicollis
(yellow-necked mouse)
fecal-oral sex-biased transmission (mainly to males)
Amblyomma
(a tick)
Sphenodon punctatus
(tuatara)
free-living infectious stages social behavior
Plasmodium
(malaria parasite)
Birds, mammals
(inc. humans)
Anopheles mosquito vector, attracted by odour of infected human host[52]

Among protozoan endoparasites, such as the malarial parasites in the genus Plasmodium and sleeping sickness parasites in the genus Trypanosoma, infective stages in the host's blood are transported to new hosts by biting blood-drinking (hematophagous) insects acting as vectors.[40]

Host defences[edit]

Hosts have evolved a variety of defensive measures against their parasites, including physical barriers like the skin of vertebrates,[53] the immune system of mammals,[54] insects actively removing parasites,[55] and defensive chemicals in plants.[56]

Biologists such as W. D. Hamilton have suggested that genetic recombination through sexual reproduction could have evolved to help to defeat multiple parasites, showing with mathematical modelling that sexual reproduction would be evolutionarily stable even under unpromising conditions, and that the theory's predictions match the actual ecology of sexual reproduction.[57][58] However, there may be a trade-off between immune defence and secondary sex characteristics in breeding male vertebrate hosts, such as the plumage of peacocks and the manes of male lions. This is because the male hormone testosterone encourages the growth of secondary sex characteristics, favouring such males in sexual selection, at the price of reducing their immune defences.[59]

Vertebrates[edit]

The dry skin of vertebrates such as the short-horned lizard prevents entry of many parasites.

The physical barrier of the tough and often dry and waterproof skin of reptiles, birds and mammals keeps invading microorganisms from entering the body. Human skin also secretes sebum, which is toxic to most microorganisms.[53] On the other hand, larger parasites such as trematodes detect chemicals produced by the skin to locate their hosts when they enter the water. Vertebrate saliva and tears contain lysozyme, an enzyme which breaks down cell walls of invading bacteria.[53] Should the organism pass the mouth, the stomach with its hydrochloric acid, toxic to most microorganisms, is the next line of defence.[53] Some intestinal parasites have a thick, tough outer coating which is digested slowly or not at all, allowing the parasite to pass through the stomach alive, at which point they enter the intestine and begin the next stage of their life. Once inside the body, parasites must overcome the immune system's serum proteins and pattern recognition receptors, intracellular and cellular, that trigger the adaptive immune system's lymphocytes such as T cells and antibody-producing B cells. These have receptors that recognize parasites.[54]

Insects[edit]

Leaf spot on oak. The spread of the parasitic fungus is limited by defensive chemicals produced by the tree, resulting in circular patches of damaged tissue.

Insects often adapt their nests to reduce parasitism. For example, one of the key reasons why the wasp Polistes canadensis nests across multiple combs, rather than building a single comb like much of the rest of its genus, is to avoid infestation by tineid moths. The tineid moth lays its eggs within the wasps' nests and then these eggs hatch into larvae that can burrow from cell to cell and prey on wasp pupae. Adult wasps attempt to remove and kill moth eggs and larvae by chewing down the edges of cells, coating the cells with an oral secretion that gives the nest a dark brownish appearance.[55]

Plants[edit]

Plants respond to parasite attack with a series of chemical defences, such as the jasmonic acid-insensitive (JA) and NahG (SA) pathways.[56] Different biochemical pathways are activated by different parasites.[60] In general, plants can either initiate a specific or a non-specific response.[61]

Specific responses involve recognition of a parasite by the plant's cellular receptors, leading to a strong but localized response: defensive chemicals are produced around the area where the parasite was detected, blocking its spread, and avoiding wasting defensive production where it is not needed.[61]

Nonspecific defensive responses are systemic, meaning that the responses are not confined to an area of the plant, but spread throughout the plant, making them costly in energy. These are effective against a wide range of parasites.[61]

Evolutionary ecology[edit]

Restoration of a Tyrannosaurus with holes possibly caused by a Trichomonas-like parasite

Parasitism has arisen independently many times. Depending on the definition used, as many as half of all animals have at least one parasitic phase in their life cycles,[62] and it is frequent in plants and fungi. Almost all free-living animals are host to one or more parasitic taxa.[62] This is harder to demonstrate from the fossil record, but for example holes in the skulls of several specimens of Tyrannosaurus may have been caused by Trichomonas-like parasites.[63]

Coevolution and cospeciation[edit]

Biologists long suspected cospeciation of flamingos and ducks with their parasitic lice, which were similar in the two families. Cospeciation did occur, but it led to flamingos and grebes, with a later host switch of flamingo lice to ducks.

A parasite sometimes undergoes co-speciation with its host, resulting in the pattern described in Fahrenholz's rule, that the phylogenies of the host and parasite come to mirror each other.[64]

An example is between the simian foamy virus (SFV) and its primate hosts. The phylogenies of SFV polymerase and the mitochondrial cytochrome oxidase subunit II from African and Asian primates were found to be closely congruent in branching order and divergence times, implying that the simian foamy viruses co-speciated with Old World primates for at least 30 million years.[65]

The presumption of a shared evolutionary history between parasites and hosts can help elucidate how host taxa are related. For instance, there has been a dispute about whether flamingos are more closely related to storks or ducks. The fact that flamingos share parasites with ducks and geese was initially taken as evidence that these groups were more closely related to each other than either is to storks. However, evolutionary events such as the duplication or extinction of parasite species (without similar events on the host phylogeny) often erode similarities between host and parasite phylogenies. In the case of flamingos, they have similar lice to those of grebes. Flamingos and grebes do have a common ancestor, implying cospeciation of birds and lice in these groups. Flamingo lice then switched hosts to ducks, creating the situation which had confused biologists.[66]

Parasites infect hosts within their same geographical area (sympatric) more effectively, as has been shown with digenetic trematodes infecting lake snails.[67] This is in line with the Red Queen hypothesis, which states that interactions between species lead to constant natural selection for coadaptation. Parasites track the locally common hosts' phenotypes, so the parasites are less infective to allopatric hosts, those from different geographical regions.[67]

Coevolution favoring mutualism[edit]

The gram-negative bacterium Wolbachia within an insect cell

Long-term coevolution sometimes leads to a relatively stable relationship tending to commensalism or mutualism, as, all else being equal, it is in the evolutionary interest of the parasite that its host thrives. A parasite may evolve to become less harmful for its host or a host may evolve to cope with the unavoidable presence of a parasite—to the point that the parasite's absence causes the host harm. For example, although animals infected with parasitic worms are often clearly harmed, and therefore parasitized, such infections may also reduce the prevalence and effects of autoimmune disorders in animal hosts, including humans.[68] In a more extreme example, some nematode worms cannot reproduce, or even survive, without infection by Wolbachia bacteria.[69]

Lynn Margulis and others have argued, following Peter Kropotkin's 1902 Mutual Aid: A Factor of Evolution, that natural selection drives relationships from parasitism to mutualism when resources are limited. This process may have been involved in the symbiogenesis which formed the eukaryotes from an intracellular relationship between archaea and bacteria, though the sequence of events remains largely undefined.[70][71]

Competition favoring virulence[edit]

Competition between parasites can be expected to favor faster reproducing and therefore more virulent parasites, by natural selection.[72][73] Parasites whose life cycle involves the death of the host, to exit the present host and sometimes to enter the next, evolve to be more virulent, and may alter the behavior or other properties of the host to make it more vulnerable to predators.[74] Conversely, parasites whose reproduction is largely tied to their host's reproductive success tend to become less virulent or mutualist, so that their hosts reproduce more effectively.[74]

The protozoan Toxoplasma gondii facilitates its transmission by inducing behavioral changes in rats through infection of neurons in their central nervous system.

Among competing parasitic insect-killing bacteria of the genera Photorhabdus and Xenorhabdus, virulence depended on the relative potency of the antimicrobial toxins (bacteriocins) produced by the two strains involved. When only one bacterium could kill the other, the other strain was excluded by the competition. But when caterpillars were infected with bacteria both of which had toxins able to kill the other strain, neither strain was excluded, and their virulence was less than when the insect was infected by a single strain.[72]

Modifying host behaviour[edit]

Some parasites modify host behaviour in order to increase the transmission between hosts, often in relation to predator and prey (parasite increased trophic transmission). For example, in California salt marshes, the fluke Euhaplorchis californiensis reduces the ability of its killifish host to avoid predators.[75] This parasite matures in egrets, which are more likely to feed on infected killifish than on uninfected fish. Another example is the protozoan Toxoplasma gondii, a parasite that matures in cats but can be carried by many other mammals. Uninfected rats avoid cat odors, but rats infected with T. gondii are drawn to this scent, which may increase transmission to feline hosts.[76] The malaria parasite modifies the skin odour of its human hosts, increasing their attractiveness to mosquitoes and hence improving the chance that the parasite will be transmitted.[52]

Bed bug, Cimex lectularius, is flightless, like many insect ectoparasites.

Trait loss[edit]

Parasites are able to exploit their hosts for a variety of functions, and so do not need to carry out those activities themselves. Parasites which lose those functions then have a selective advantage, as they can divert resources to reproduction. Many insect ectoparasites including bedbugs, batbugs, lice and fleas have lost their ability to fly, relying instead on their hosts for transport.[77] Trait loss more generally is widespread among parasites.[78]

Biology and conservation[edit]

Ecology and parasitology[edit]

Parasitism and parasite evolution were until the twentyfirst century studied by parasitologists, in a science dominated by medicine, rather than by ecologists or evolutionary biologists. Even though parasite-host interactions were plainly ecological, the history of parasitology caused what the evolutionary ecologist Robert Poulin called a "takeover of parasitism by parasitologists", leading ecologists to ignore the area. This was in his opinion "unfortunate", as parasites are "omnipresent agents of natural selection" and significant forces in evolution and ecology. The long-standing split between the sciences limited the exchange of ideas, with separate conferences and separate journals. The technical languages of ecology and parasitology sometimes involved different meanings for the same words. There were philosophical differences, too: Poulin notes that, influenced by medicine, "many parasitologists accepted that evolution led to a decrease in parasite virulence, whereas modern evolutionary theory would have predicted a greater range of outcomes".[79]

The rescuing from extinction of the California condor was a successful if very expensive project, but its ectoparasite, the louse Colpocephalum californici, became extinct.

Rationale for conservation[edit]

Although parasites are widely considered to be harmful, the eradication of all parasites would not be beneficial. Parasites account for at least half of life's diversity; they perform important ecological roles; and without parasites, organisms might tend to asexual reproduction, diminishing the diversity of traits brought about by sexual reproduction.[80] Parasites provide an opportunity for the transfer of genetic material between species, facilitating evolutionary change.[74] Many parasites require multiple hosts of the different species to complete their life cycles and rely on predator-prey or other stable ecological interactions to get from one host to another. The presence of parasites thus indicates that an ecosystem is healthy.[81]

A well-known case was that of an ectoparasite, the California condor louse, Colpocephalum californici. Any lice found were "deliberately killed" during the major and very costly captive breeding program to rescue its host, the Californian condor. The result was that the condor was saved, and returned to the wild, while the parasite became extinct.[82]

Although parasites are often omitted in depictions of food webs, they usually occupy the top position. Parasites can function like keystone species, reducing the dominance of superior competitors and allowing competing species to co-exist.[83][84][85]

Quantitative ecology[edit]

A single parasite species usually has an aggregated distribution across host individuals, which means that most hosts harbor few parasites, while a few hosts carry the vast majority of parasite individuals. This poses considerable problems for students of parasite ecology, as it renders parametric statistics as commonly used by biologists invalid. Log-transformation of data before the application of parametric test, or the use of non-parametric statistics is recommended by several authors, but this can give rise to further problems, so quantitative parasitology is based on more advanced biostatistical methods.[86]

History[edit]

Cyst and imago of Giardia lamblia, the protozoan parasite that causes giardiasis, first observed by Antonie van Leeuwenhoek in 1681

Ancient[edit]

Human parasites including roundworms, the Guinea worm, threadworms and tapeworms are mentioned in Egyptian papyrus records from 3000 BC onwards; the Ebers papyrus describes hookworm. In ancient Greece, parasites including the bladder worm are described in the Hippocratic Corpus, while the comic playwright Aristophanes called tapeworms "hailstones". The Roman physicians Celsus and Galen documented the roundworms Ascaris lumbricoides and Enterobius vermicularis.[87]

Medieval[edit]

The Persian physician Avicenna recorded human and animal parasites including roundworms, threadworms, the Guinea worm and tapeworms.[87]

Early Modern[edit]

A plate from Francesco Redi's Osservazioni intorno agli animali viventi che si trovano negli animali viventi (Observations on living animals found inside living animals), 1684

Antonie van Leeuwenhoek observed and illustrated Giardia lamblia in 1681, and linked it to "his own loose stools". This was the first protozoan parasite of humans that he recorded, and the first to be seen under a microscope.[87]

Francesco Redi described ecto- and endoparasites in his 1687 book Esperienze Intorno alla Generazione degl'Insetti (Experiences of the Generation of Insects), illustrating ticks, the larvae of nasal flies of deer, and sheep liver fluke. His 1684 book Osservazioni intorno agli animali viventi che si trovano negli animali viventi (Observations on Living Animals found in Living Animals) described and illustrated over 100 parasites including the human roundworm.[88] He noted that parasites develop from eggs, contradicting the theory of spontaneous generation.[89]

Birth of modern parasitology[edit]

Modern parasitology developed in the 19th century with accurate observations by several researchers and clinicians. In 1828, James Annersley described amoebiasis, protozoal infections of the intestines and the liver, though the pathogen, Entamoeba histolytica, was not discovered until 1873 by Friedrich Lösch. James Paget discovered the intestinal nematode Trichinella spiralis in humans in 1835. James McConnell described the human liver fluke in 1875. Patrick Manson discovered the life cycle of elephantiasis, caused by nematode worms transmitted by mosquitoes, in 1877. Manson further predicted that the malaria parasite, Plasmodium, had a mosquito vector, and persuaded Ronald Ross to investigate. Ross confirmed that the prediction was correct in 1897–1898. At the same time, Giovanni Battista Grassi and others described the malaria parasite's life cycle stages in Anopheles mosquitoes. Ross was controversially awarded the 1902 Nobel prize for his work, while Grassi was not.[87]

Vaccine[edit]

Given the importance of malaria, with some 220 million people infected annually, many attempts have been made to interrupt its transmission, such as by killing parasites in the blood with antimalarial drugs, by eradicating its mosquito vectors with organochlorine and other insecticides, or by developing a malaria vaccine. All of these have proven problematic, with drug resistance, insecticide resistance among mosquitoes, and repeated failure of vaccines as the parasite mutates.[90] The first and as of 2015 the only licenced vaccine for any parasitic disease of humans is RTS,S for Plasmodium falciparum malaria.[91]

Cultural significance[edit]

"An Old Parasite in a New Form": an 1881 Punch cartoon by Edward Linley Sambourne compares a crinoletta bustle to a parasitic insect's exoskeleton

Classical times[edit]

In the classical era, the concept of the parasite was not strictly pejorative:[92] the parasitus was an accepted role in Roman society, in which a person could live off the hospitality of others, and in return provide "flattery, simple services, and a willingness to endure humiliation".[93][94]

Society[edit]

Parasitism has a derogatory sense in popular usage. According to the immunologist John Playfair,[95]

In everyday speech, the term 'parasite' is loaded with derogatory meaning. A parasite is a sponger, a lazy profiteer, a drain on society.[95]

The satirical cleric Jonathan Swift refers to hyperparasitism in his 1733 poem "On Poetry: A Rhapsody", comparing poets to "vermin" who "teaze and pinch their foes":[96]

Parasitic "facehugger" alien species in James Cameron's 1986 science fiction film Aliens
The vermin only teaze and pinch
Their foes superior by an inch.
So nat'ralists observe, a flea
Hath smaller fleas that on him prey;
And these have smaller fleas to bite 'em.
And so proceeds ad infinitum.
Thus every poet, in his kind,
Is bit by him that comes behind:

Fiction[edit]

In Bram Stoker's 1897 Gothic horror novel Dracula, and its many film adaptations, the eponymous Count Dracula is a blood-drinking parasite. The critic Laura Otis argues that as a "thief, seducer, creator, and mimic, Dracula is the ultimate parasite. The whole point of vampirism is sucking other people's blood—living at other people's expense."[97]

Disgusting and terrifying parasitic alien species are widespread in science fiction,[98][99] as for instance in Ridley Scott's 1979 film Alien.[100][101] In one scene of that film, an alien bursts out of the chest of a dead man, with blood squirting out under high pressure assisted by explosive squibs. Animal viscera were used to reinforce the shock effect. The scene was filmed in a single take, and the startled reaction of the actors was genuine.[4][102]

References[edit]

  1. ^ Poulin, Robert (2007). Evolutionary ecology of parasites. Princeton University Press. pp. 4–5. ISBN 978-0-691-12085-0. 
  2. ^ a b Wilson, Edward O. (2014). The Meaning of Human Existence. W. W. Norton & Company. p. 112. ISBN 978-0-87140-480-0. Parasites, in a phrase, are predators that eat prey in units of less than one. Tolerable parasites are those that have evolved to ensure their own survival and reproduction but at the same time with minimum pain and cost to the host. 
  3. ^ Getz, W.M. (2011). "Biomass transformation webs provide a unified approach to consumer-resource modelling". Ecol. Lett. 14 (2): 113–24. doi:10.1111/j.1461-0248.2010.01566.x. PMC 3032891Freely accessible. PMID 21199247. 
  4. ^ a b "The Making of Alien's Chestburster Scene". The Guardian. 13 October 2009. Archived from the original on 30 April 2010. Retrieved 29 May 2010. 
  5. ^ παράσιτος, Liddell, Henry George; Scott, Robert, A Greek-English Lexicon, on Perseus Digital Library
  6. ^ παρά, Henry George Liddell, Robert Scott, A Greek-English Lexicon, on Perseus Digital Library
  7. ^ σῖτος, Liddell, Henry George; Scott, Robert, A Greek-English Lexicon, on Perseus Digital Library
  8. ^ σιτισμός, Liddell, Henry George; Scott, Robert, A Greek-English Lexicon, on Perseus Digital Library
  9. ^ Martin, Bradford D.; Schwab, Ernest (2013). "Current usage of symbiosis and associated terminology". International Journal of Biology. 5 (1): 32–45. doi:10.5539/ijb.v5n1p32. 
  10. ^ "A Classification of Animal-Parasitic Nematodes". plpnemweb.ucdavis.edu. 
  11. ^ Garcia, L. S. (1999). "Classification of Human Parasites, Vectors, and Similar Organisms" (PDF). Clin Infect Dis. 29 (4): 734–746. doi:10.1086/520425. PMID 10589879. 
  12. ^ a b c d e f g h i j k Poulin, Robert; Randhawa, Haseeb S. (February 2015). "Evolution of parasitism along convergent lines: from ecology to genomics". Parasitology. 142 (Suppl 1): S6–S15. doi:10.1017/S0031182013001674. PMC 4413784Freely accessible. PMID 24229807. 
  13. ^ a b Poulin, Robert (2011). Rollinson, D.; Hay, S. I., eds. The Many Roads to Parasitism: A Tale of Convergence. Advances in Parasitology. Academic Press. pp. 27–28. ISBN 978-0-12-385897-9. 
  14. ^ Van Damme, P. A.; et al. (1997). "The suprapopulation dynamics of Lernaeocera branchialis and L. lusci in the Oosterschelde: seasonal abundance on three definitive host species". ICES Journal of Marine Science. 54: 4–31. doi:10.1006/jmsc.1996.0187. 
  15. ^ a b Cheng, Thomas C. (2012). General Parasitology. Elsevier Science. pp. 13–15. ISBN 978-0-323-14010-2. 
  16. ^ Hopla, C. E.; Durden, L. A.; Keirans, J. E. "Ectoparasites and classification" (PDF). Rev. sci. tech. Off. int. Epiz. 13 (4): 985–1017. doi:10.20506/rst.13.4.815. 
  17. ^ Cox, FE (2001). "Concomitant infections, parasites and immune responses". Parasitology. 122. Suppl: S23–38. doi:10.1017/s003118200001698x. PMID 11442193. 
  18. ^ "Helminth Parasites". Australian Society of Parasitology. Retrieved 9 October 2017. 
  19. ^ "Pathogenic Parasitic Infections". PEOI. Retrieved 2013-07-18. 
  20. ^ a b c d Gullan, P. J.; Cranston, P. S. (2010). The Insects: An Outline of Entomology (4th ed.). Wiley. pp. 308, 365–367, 375, 440–441. ISBN 978-1-118-84615-5. 
  21. ^ a b Dissanaike, A. S. (1957). "On Protozoa hyperparasitic in Helminth, with some observations on Nosema helminthorum Moniez, 1887". J. Helminthology. 31 (1-2): 47–64. doi:10.1017/s0022149x00033290. PMID 13429025. 
  22. ^ a b Thomas, J. A.; Schönrogge, K; Bonelli, S.; Barbero, F.; Balletto, E. (2010). "Corruption of ant acoustical signals by mimetic social parasites: Maculinea butterflies achieve elevated status in host societies by mimicking the acoustics of queen ants". Commun Integr Biol. 3 (2): 169–171. doi:10.4161/cib.3.2.10603. PMC 2889977Freely accessible. PMID 20585513. 
  23. ^ a b Payne, R. B. (1997). D. H. Clayton and J. Moore, ed. Avian brood parasitism. Host-parasite evolution: General principles and avian models. Oxford University Press. pp. 338–369. ISBN 978-0198548928. 
  24. ^ a b Peter J.B. Slater; Jay S. Rosenblatt; Charles T. Snowdon; Timothy J. Roper; H. Jane Brockmann; Marc Naguib (30 January 2005). Advances in the Study of Behavior. Academic Press. p. 365. ISBN 978-0-08-049015-1. 
  25. ^ a b Pietsch, Theodore W. (25 August 2005). "Dimorphism, parasitism, and sex revisited: modes of reproduction among deep-sea ceratioid anglerfishes (Teleostei: Lophiiformes)". Ichthyological Research. 52 (3): 207–236. doi:10.1007/s10228-005-0286-2. 
  26. ^ "Featured Creatures. Encarsia perplexa". University of Florida. Retrieved 6 January 2018. 
  27. ^ Berec, Ludek; Schembri, Patrick J.; Boukal, David S. (2005). "Sex determination inBonellia viridis(Echiura: Bonelliidae): population dynamics and evolution". Oikos. 108 (3): 473–484. doi:10.1111/j.0030-1299.2005.13350.x. 
  28. ^ Leake, J. R. (1994). "The biology of myco-heterotrophic ('saprophytic') plants". New Phytologist. 127: 171–216. doi:10.1111/j.1469-8137.1994.tb04272.x. 
  29. ^ Van Oystaeyen, Annette; Araujo Alves, Denise; Caliari Oliveira, Ricardo; Lima do Nascimento, Daniela; Santos do Nascimento, Fábio; Billen, Johan; Wenseleers, Tom (September 2013). "Sneaky queens in Melipona bees selectively detect and infiltrate queenless colonies". Animal Behaviour. 86 (3): 603–609. doi:10.1016/j.anbehav.2013.07.001. 
  30. ^ "Social Parasites in the Ant Colony". Antkeepers. Retrieved 4 April 2016. 
  31. ^ Richard Deslippe (2010). "Social Parasitism in Ants". Nature Education Knowledge. Retrieved 2010-10-29. In 1909, the taxonomist Carlo Emery made an important generalization, now known as Emery’s rule, which states that social parasites and their hosts share common ancestry and hence are closely related to each other (Emery 1909). 
  32. ^ Emery, C. "Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen". Biologisches Centralblatt 29, 352–362 (1909)
  33. ^ O'Brien, Timothy G. (1988). "Parasitic nursing behavior in the wedge-capped capuchin monkey (Cebus olivaceus)". American Journal of Primatology. 16 (4): 341–344. doi:10.1002/ajp.1350160406. 
  34. ^ Rothstein, S.I (1990). "A model system for coevolution: avian brood parasitism". Annual Review of Ecology and Systematics. 21: 481–508. doi:10.1146/annurev.ecolsys.21.1.481. 
  35. ^ Welbergen, J.; Davies, N. B. (2011). "A parasite in wolf's clothing: hawk mimicry reduces mobbing of cuckoos by hosts". Behavioral Ecology. 22 (3): 574–579. doi:10.1093/beheco/arr008. 
  36. ^ Furness, R.W. (1978). "Kleptoparasitism by great skuas (Catharacta skua Brünn.) and Arctic skuas (Stercorarius parasiticus L.) at a Shetland seabird colony". Animal Behaviour. Elsevier BV. 26: 1167–1177. doi:10.1016/0003-3472(78)90107-0. 
  37. ^ a b c Poulin, Robert (2007). Evolutionary ecology of parasites. Princeton University Press. p. 6. ISBN 978-0-691-12085-0. 
  38. ^ a b c d Heide-Jørgensen, H.; Heide-Jørgensen, Henning S. (2008). Parasitic flowering plants. Brill. 
  39. ^ a b "What is honey fungus?". Royal Horticultural Society. Retrieved 12 October 2017. 
  40. ^ a b c Pollitt, Laura C.; MacGregor, Paula; Matthews, Keith; Reece, Sarah E. (2011). "Malaria and trypanosome transmission: different parasites, same rules?". Trends in Parasitology. 27 (5): 197–203. doi:10.1016/j.pt.2011.01.004. ISSN 1471-4922. 
  41. ^ a b McFall-Ngai, Margaret (January 2007). "Adaptive Immunity: Care for the community". Nature. 445 (7124): 153–153. doi:10.1038/445153a. ISSN 0028-0836. 
  42. ^ a b Koonin, E. V.; Senkevich, T. G.; Dolja, V. V. (2006). "The ancient Virus World and evolution of cells". Biology Direct. 1: 29. doi:10.1186/1745-6150-1-29. PMC 1594570Freely accessible. PMID 16984643. 
  43. ^ Sekar, Sandhya (22 May 2015). "Parasitoid wasps may be the most diverse animal group". BBC. Retrieved 14 February 2018. 
  44. ^ Nickrent, D. L.; Musselman, L. J. (2004). "Introduction to Parasitic Flowering Plants". The Plant Health Instructor. doi:10.1094/PHI-I-2004-0330-01. 
  45. ^ Westwood, James H.; Yoder, John I.; Timko, Michael P.; dePamphilis, Claude W. (2010). "The evolution of parasitism in plants". Trends in Plant Science. 15 (4): 227–235. doi:10.1016/j.tplants.2010.01.004. 
  46. ^ Esch KJ, Petersen CA (January 2013). "Transmission and epidemiology of zoonotic protozoal diseases of companion animals". Clin Microbiol Rev. 26 (1): 58–85. doi:10.1128/CMR.00067-12. PMC 3553666Freely accessible. PMID 23297259. 
  47. ^ Fisher, Bruce; Harvey, Richard P.; Champe, Pamela C. (2007). Lippincott's Illustrated Reviews: Microbiology (Lippincott's Illustrated Reviews Series). Hagerstown, MD: Lippincott Williams & Wilkins. pp. 332–353. ISBN 0-7817-8215-5. 
  48. ^ Breitbart, M.; Rohwer, F.. Here a virus, there a virus, everywhere the same virus?. Trends in Microbiology. 2005;13(6):278–284. doi:10.1016/j.tim.2005.04.003. PMID 15936660.
  49. ^ Lawrence, C. M.; Menon, S.; Eilers, B. J.; et al. (2009). "Structural and functional studies of archaeal viruses". The Journal of Biological Chemistry. 284 (19): 12599–603. doi:10.1074/jbc.R800078200. PMC 2675988Freely accessible. PMID 19158076. 
  50. ^ Edwards, R. A.; Rohwer, F. (2005). "Viral metagenomics". Nature Reviews Microbiology. 3 (6): 504–10. doi:10.1038/nrmicro1163. PMID 15886693. 
  51. ^ a b Godfrey, Stephanie S. (December 2013). "Networks and the ecology of parasite transmission: A framework for wildlife parasitology". Wildlife. 2: 235–245. doi:10.1016/j.ijppaw.2013.09.001. 
  52. ^ a b de Boer, Jetske G.; Robinson, Ailie; Powers, Stephen J.; Burgers, Saskia L. G. E.; Caulfield, John C.; Birkett, Michael A.; Smallegange, Renate C.; van Genderen, Perry J. J.; Bousema, Teun; Sauerwein, Robert W.; Pickett, John A.; Takken, Willem; Logan, James G. (August 2017). "Odours of Plasmodium falciparum-infected participants influence mosquito-host interactions". Scientific Reports. 7 (1). doi:10.1038/s41598-017-08978-9. 
  53. ^ a b c d "Host-Parasite Interactions Innate Defenses of the Host" (PDF). University of Colorado. 
  54. ^ a b Maizels, R. M. (2009). "Parasite immunomodulation and polymorphisms of the immune system". J. Biol. 8 (7): 62. doi:10.1186/jbiol166. PMC 2736671Freely accessible. PMID 19664200. 
  55. ^ a b Jeanne, Robert L. (1979). "Construction and Utilization of Multiple Combs in Polistes canadensis in Relation to the Biology of a Predaceous Moth". Behavioral Ecology and Sociobiology. 4 (3): 293–310. doi:10.1007/bf00297649. 
  56. ^ a b Runyon, J. B.; Mescher, M. C.; De Moraes, C. M. (2010). "Plant defenses against parasitic plants show similarities to those induced by herbivores and pathogens". Plant Signal Behav. 5 (8): 929–31. doi:10.4161/psb.5.8.11772. PMC 3115164Freely accessible. PMID 20495380. 
  57. ^ Hamilton, W. D.; Axelrod, R.; Tanese, R. (May 1990). "Sexual reproduction as an adaptation to resist parasites (a review)". Proceedings of the National Academy of Sciences. Proceedings of the National Academy of Sciences. 87 (9): 3566–3573. doi:10.1073/pnas.87.9.3566. 
  58. ^ Ebert, Dieter; Hamilton, William D. (1996). "Sex against virulence: the coevolution of parasitic diseases". Trends in Ecology & Evolution. Elsevier BV. 11 (2): 79–82. doi:10.1016/0169-5347(96)81047-0. 
  59. ^ Folstad, Ivar; Karter, Andrew John (1992). "Parasites, Bright Males, and the Immunocompetence Handicap". The American Naturalist. 139 (3): 603–622. doi:10.1086/285346. 
  60. ^ Hatcher, J. M.; Dunn, M. A. (2011). Parasites in Ecological Communities. Cambridge University Press. 
  61. ^ a b c Frank, S. A. (2000). "Specific and non-specific defense against parasitic attack". J. Theor. Biol. 202 (4): 283–304. doi:10.1006/jtbi.1999.1054. PMID 10666361. 
  62. ^ a b Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press. 
  63. ^ Wolff, Ewan D. S.; Salisbury, Steven W.; Horner, John R.; Varrichio, David J. (2009). "Common Avian Infection Plagued the Tyrant Dinosaurs". PLoS ONE. 4 (9): e7288. doi:10.1371/journal.pone.0007288. PMC 2748709Freely accessible. PMID 19789646. 
  64. ^ Page, Roderic D. M. (2006-01-27), Cospeciation, John Wiley, doi:10.1038/npg.els.0004124, ISBN 0-470-01617-5 
  65. ^ Switzer, William M.; Salemi, Marco; Shanmugam, Vedapuri; Gao, Feng; Cong, Mian-er; Kuiken, Carla; Bhullar, Vinod; Beer, Brigitte E.; Vallet, Dominique; Gautier-Hion, Annie; Tooze, Zena; Villinger, Francois; Holmes, Edward C.; Heneine, Walid (2005). "Ancient co-speciation of simian foamy viruses and primates". Nature. 434 (7031): 376–380. doi:10.1038/nature03341. 
  66. ^ Johnson, K. P.; Kennedy, M.; McCracken, K. G (2006). "Reinterpreting the origins of flamingo lice: cospeciation or host-switching?". Biology Letters. 2 (2): 275–278. doi:10.1098/rsbl.2005.0427. PMC 1618896Freely accessible. 
  67. ^ a b Lively, C. M.; Dybdahl, M. F. (2000). "Parasite adaptation to locally common host genotypes". Nature. 405 (6787): 679–81. doi:10.1038/35015069. PMID 10864323. 
  68. ^ Rook, G. A. (2007). "The hygiene hypothesis and the increasing prevalence of chronic inflammatory disorders". Transactions of the Royal Society of Tropical Medicine and Hygiene. 101 (11): 1072–4. doi:10.1016/j.trstmh.2007.05.014. PMID 17619029. 
  69. ^ Werren, John H. (February 2003). "Invasion of the Gender Benders: by manipulating sex and reproduction in their hosts, many parasites improve their own odds of survival and may shape the evolution of sex itself". Natural History. 112 (1): 58. OCLC 1759475. Archived from the original (Reprint) on 8 July 2012. Retrieved 15 November 2008. 
  70. ^ Margulis, Lynn; Sagan, Dorion; Niles Eldredge (1995). What Is Life?. Simon and Schuster. ISBN 978-0684810874. 
  71. ^ Sarkar, Sahotra; Plutynski, Anya (2008). A Companion to the Philosophy of Biology. John Wiley & Sons. p. 358. ISBN 978-0-470-69584-5. 
  72. ^ a b Massey, R. C.; Buckling, A.; ffrench-Constant, R. (2004). "Interference competition and parasite virulence". Proceedings of the Royal Society B: Biological Sciences. 271 (1541): 785–788. doi:10.1098/rspb.2004.2676. PMC 1691666Freely accessible. 
  73. ^ Rigaud, T.; Perrot-Minnot, M.-J.; Brown, M. J. F. (2010). "Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence". Proceedings of the Royal Society B: Biological Sciences. 277 (1701): 3693–3702. doi:10.1098/rspb.2010.1163. 
  74. ^ a b c Claude Combes, The Art of being a Parasite, University of Chicago Press, 2005
  75. ^ Lafferty, K. D.; Morris, A. K. (1996). "Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts". Ecology. 77: 1390. doi:10.2307/2265536. 
  76. ^ Berdoy, M.; Webster, J.P.; Macdonald, D. W. (2000). "Fatal attraction in rats infected with Toxoplasma gondii". Proc. Biol. Sci. 267 (1452): 1591–4. doi:10.1098/rspb.2000.1182. PMC 1690701Freely accessible. PMID 11007336. 
  77. ^ Alexander, David E. (2015). On the Wing: Insects, Pterosaurs, Birds, Bats and the Evolution of Animal Flight. Oxford University Press. p. 119. ISBN 978-0-19-999679-7. 
  78. ^ Poulin, R. (September 1995). "Evolution of parasite life history traits: myths and reality". Parasitology Today. 11 (9): 342–345. doi:10.1016/0169-4758(95)80187-1. PMID 15275316. 
  79. ^ Poulin, Robert (2007). Evolutionary ecology of parasites. Princeton University Press. pp. x, 1–2. ISBN 978-0-691-12085-0. 
  80. ^ Holt, R. D. (2010). "IJEE Soapbox". Israel Journal of Ecology and Evolution. 56 (3): 239–250. doi:10.1560/IJEE.56.3-4.239. 
  81. ^ Hudson, Peter J.; Dobson, Andrew P.; Lafferty, Kevin D. (2006). "Is a healthy ecosystem one that is rich in parasites?". Trends in Ecology & Evolution. 21 (7): 381–385. doi:10.1016/j.tree.2006.04.007. 
  82. ^ Stringer, Andrew Paul; Linklater, Wayne (2014). "Everything in Moderation: Principles of Parasite Control for Wildlife Conservation". BioScience. 64 (10): 932. doi:10.1093/biosci/biu135Freely accessible. 
  83. ^ Sukhdeo, Michael V. K. (2012). "Where are the parasites in food webs?". Parasites & Vectors. 5 (1): 239. doi:10.1186/1756-3305-5-239. 
  84. ^ Lafferty, Kevin D.; Allesina, Stefano; Arim, Matias; Briggs, Cherie J.; et al. (2008). "Parasites in food webs: the ultimate missing links". Ecology Letters. 11 (6): 533–546. doi:10.1111/j.1461-0248.2008.01174.x. ISSN 1461-023X. 
  85. ^ Chase, Jonathan (2013). "Parasites in Food Webs: Untangling the Entangled Bank". PLoS Biology. 11 (6): e1001580. doi:10.1371/journal.pbio.1001580. 
  86. ^ Rózsa, L.; Reiczigel, J.; Majoros, G. (2000). "Quantifying parasites in samples of hosts". J. Parasitol. 86 (2): 228–32. doi:10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2. PMID 10780537. 
  87. ^ a b c d Cox, Francis E. G. (June 2004). "History of human parasitic diseases". Infectious Disease Clinics of North America. 18 (2): 173–174. doi:10.1016/j.idc.2004.01.001. PMID 15145374. 
  88. ^ Ioli, A; Petithory, J.C.; Theodorides, J. (1997). "Francesco Redi and the birth of experimental parasitology". Hist Sci Med. 31 (1): 61–66. PMID 11625103. 
  89. ^ Bush, A. O.; Fernández, J. C.; Esch, G. W.; Seed, J. R. (2001). Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge University Press. p. 4. ISBN 0521664470. 
  90. ^ "Malaria and Malaria Vaccine Candidates". The College of Physicians of Philadelphia. 19 April 2017. Retrieved 11 February 2018. 
  91. ^ Walsh, Fergus (24 July 2015). "Malaria vaccine gets 'green light'". BBC. Retrieved 25 July 2015. 
  92. ^ Toussaint-Samat, M. (2009). A History of Food. Wiley-Blackwell. ISBN 978-1405181198. 
  93. ^ Donahue, J. F. (2014). Food and Drink in Antiquity: A Sourcebook: Readings from the Graeco-Roman World. Bloomsbury. ISBN 978-1441133458. 
  94. ^ Damon, Cynthia (1997). "5". The Mask of the Parasite: A Pathology of Roman Patronage. University of Michigan Press. p. 148. ISBN 978-0472107605. A satirist seeking to portray client misery naturally focuses on the relationship with the greatest dependency, that in which a client gets his food from his patron, and for this the prefabricated persona of the parasite proved itself extremely useful. 
  95. ^ a b Playfair, John (2007). Living with Germs: In health and disease. Oxford University Press. p. 19. ISBN 978-0-19-157934-9.  Playfair is comparing the popular usage to a biologist's view of parasitism, which he calls (heading the same page) "an ancient and respectable view of life".
  96. ^ Swift, Jonathan (1733). On Poetry: A Rapsody. And sold by J. Huggonson, next to Kent's Coffee-house, near Serjeant's-inn, in Chancery-lane; [and] at the bookseller's and pamphletshops. 
  97. ^ Otis, Laura (2001). Networking: Communicating with Bodies and Machines in the Nineteenth Century. University of Michigan Press. p. 216. ISBN 0-472-11213-9. 
  98. ^ "Parasitism and Symbiosis". The Encyclopedia of Science Fiction. 10 January 2016. 
  99. ^ Dove, Alistair (9 May 2011). "This is clearly an important species we're dealing with". Deep Sea News. 
  100. ^ Pappas, Stephanie (29 May 2012). "5 Alien Parasites and Their Real-World Counterparts". Live Science. 
  101. ^ Sercel, Alex (19 May 2017). "Parasitism in the Alien Movies". Signal to Noise Magazine. 
  102. ^ Nordine, Michael (25 April 2017). "'Alien' Evolution: Explore Every Stage in the Xenomorph's Gruesome Life Cycle. Celebrate Alien Day with a look at the past, present and future of cinema's most terrifying extraterrestrial". IndieWire. Nothing speaks to the xenomorph's visceral terror quite like the fact that this stage of its life cycle — which, true to its name, finds the creature literally bursting through its host's ribcage — isn't even its final form. For every alien that is born, another being (usually a human) is violently killed. And there's a reason the other actors look utterly terrified by what's happening in that infamous scene: Scott intentionally withheld key details from them in order to elicit genuine reactions. 

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