Vannier-Santos and Henrique L. This is an open access article distributed under the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract This paper presents many types of interplays between parasites and the host, showing the history of parasites, the effects of parasites on the outcome of wars, invasions, migrations, and on the development of numerous regions of the globe, and the impact of parasitic diseases on the society and on the course of human evolution.
Even the term parasitology should be replaced by cohabitology because there is no parasite alone and host alone: It also suggests switching the old paradigm based on attrition and destruction, to a new one founded on adaptation and living together. The words quoted above suggest that Darwin was rather concerned about parasites.
Many features of the parasitic life style can indubitably surprise most people regardless naturalist or not. Albert Bernhard Frank at Leipzig coined the word Symbiotismus: Thus we attempted to avoid the misleading aspects of strictu sensu definitions such as mutualist, pathogen, or parasite, used to characterize species which flow in a role-exchanging dynamic continuum [ 2 — 5 ], compared to a marriage, where it is difficult to measure the gains of respective partners [ 2 ].
Even we propose that the term parasitology should be replaced by Cohabitology because there is no parasite and host alone: Symbiosis is a cyclical and permanent phenomenon in evolution [ 8 ].
Therefore, symbiosis, which is often under laid by hostility [ 9 ], is a powerful source of biodiversity inside the pangenome [ 10 ]. According to this concept, the Pangenome is the common collective genetic system of all living organisms, the organic molecules, and their complexes DNA-and RNA-containing viruses, plasmids, transposons, insertion sequences involved in the storage and transmission processes of genetic information.
In fact, genes are remarkably outnumbered by retrotransposons and other types of mobile elements [ 10 — 12 ]. The navigation of mobile elements in the pangenome of the living beings is made by infectrons. Tosta coined this term to encompass the broad array of exogenous DNAs that invade a genome and interfere with its structure or organization, and, therefore with its function [ 13 ]. In fact, infectious agents are everywhere and they dwell the uppermost of our individuality: Symbiology plays a central role in ecology and on the overall understanding of Biology.
Nowadays it is widely accepted that most if not all metazoan organisms and many microorganisms harbor different microbes, mainly prokaryotes. These may be harmless commensals, mutually advantageous mutualists, or virulent pathogens, depending on the milieu [ 16 , 17 ].
Microbes may account for up to half the weight of insects such as termites [ 2 ]. Some of these cohabitants present their own endosymbionts which produce enzymes that breakdown lignin and cellulose.
Parasitology Cohabitology plays a central role in biological sciences, not only because parasites constitute the great majority of the living beings [ 21 ], but also because they regulate countless populations in numerous ecosystems.
Nevertheless, this bellicose view which dates from the times of Pasteur may have hindered the understanding of the innovative potential of these creative organisms upon life as we know [ 2 , 3 , 5 , 6 ]. Microbes were and are still largely seen as agents of disease and death rather than dynamic factors in transformation and evolution [ 2 ]. As will be seen below, this belligerent point of view, common in the literature, may be driven by parasites themselves. About parasite species infect the Homo sapiens sapiens being more than agents of zoonosis [ 23 ].
This is not surprising if we keep in mind that among our In the latu sensu, Parasitology would focus viruses, bacteria, fungi, animals, and plants with parasitic way of life. For methodological rather than conceptual reasons, viruses, bacteria, fungi, and sometimes even protozoa are focused by Microbiology and its branches Virology, Bacteriology and Mycology.
Thus these sciences present considerable overlapping. The modern Parasitology Cohabitology constitutes much more than a branch of biological sciences, congregating, in elegant and complex fashion, diverse areas of the knowledge for example, Zoology, Ecology, Pathology, Molecular Biology, Biochemistry, Epidemiology, Immunology, Systems Biology, and others, thus constituting a rich multidisciplinary collection.
The parasitism phenomenon comprises an intricate web of interactions in which the parasite not only is fed, sheltered, and transported through its host, but is also able to significantly modify its physiology, behavior, and even direct the routes of its evolution. Symbiotic consortia involving bacteria and blue-green algae had probably originated, respectively, mitochondria and chloroplasts of the eukaryotic organisms. This perception arose from the similarities between microbes and organelles pointed out by Joshua Lederberg and further examined by Wakeford [ 2 ] and Margulis [ 25 ].
The prokaryote-organelle continuum is the main stream of eukaryotic cell evolution and even the eukaryotic cell nucleus may have had a prokaryotic origin [ 26 , 27 ] or even a viral origin [ 28 , 29 ]. Besides different types of endosymbiont, protozoa may be associated with ectosymbiont spirochaetes that function as undolipodia or locomotion structures, which may have given rise to cilia and flagella of the higher organisms [ 30 ]. It was hypothesized that the infection vestiges of the bacteria of the spotted fever group would play a pivotal role in the origin of sexual reproduction [ 34 ].
Sterrer [ 35 ] also proposed that infection may have originated sex. It should be kept in mind that sexual reproduction is involved in parasite resistance vide infra , and the parasite-host interface is frequently depicted as a red queen race [ 36 , 37 ] but we would rather use the Sisyphus punishment metaphor.
Sisyphus, founder and king of Corinth or Ephyra as it was called in those days , was condemned in Tartarus to an eternity of rolling a boulder uphill then watching it roll back down again the Sisyphus metaphor was previously used to depict the parasite-host interplay [ 38 ].
In these consortia both species strive to overcome the opponent strategies, keeping a dynamic adaptive balance. In this kind of dance, the cohabitants beings suffer adaptive epigenetic changes, that is, they never retain the same initial state as is expressed by the red queen metaphor. Symbionts can cross continuum between commensals, mutualists, and pathogens in both directions. Also, parasitic and predatory life styles may be exchangeable and sometimes overlapping.
Therefore, it is necessary to analyze the ecology of these symbiotic associations in a broader and dynamic form [ 2 , 3 ]. Protozoa of the Phylum Apicomplexa such as Toxoplasma gondii and Plasmodium sp.
Today these compartments constitute a chemotherapy target [ 39 ]. Similarly many invertebrate species including filarid nematode parasites such as Wuchereria bancrofti were infected by the bacterium Wolbachia pipientis and depend on the prokaryote for optimal reproduction [ 40 ], and this bacterium enhances the Tribolium confusum male beetle fertility [ 41 ]. Actually the algal cells react to refrain the hyphal invasion, but are eventually killed during the fungi saprobic feeding.
The axenic cultivation of each partner is not always simple, but the algae are more easily isolated and maintained less dependent. These facts point to the parasitic nature of fungi. Phylogenetic studies using small subunit ribosomal DNA SSU rDNA indicate that lichen symbionts arose from parasitic fungi, and that there is no general evolutionary progression from parasitism to mutualism [ 42 ].
These authors propose that neither mutualism nor parasitism should be seen as endpoints in the evolution, and symbiosis and mutualism may give rise to parasitism, causing human diseases [ 5 , 43 ].
Interestingly lichens are classified taxonomically, although made-up of two distinct species belonging to different kingdoms. Therefore, two species form a third one. That may be considered symbiogenesis. Similarly, the parasite-host biocartel is suggested to be the target of natural selection [ 20 ]. Animals that feed on algae, such as Elysia viridis, may preserve functioning chloroplasts and perform photosynthesis, and these organelles can even multiply in the marine ciliate Mesodinium.
This kind of consortium is so common among marine zooplankton that it was asked why the cows are not green? Presumably because they are not translucent, but this problem was solved, at least in part, by the giant clam, the bivalve Tridacna maxima, by the development of hyaline organs, which scatter sunlight to the neighboring aggregated photosynthetic dinoflagellates or zooxantellae [ 45 ].
Most corals present zooxantellae, and these microorganisms play a pivotal role in the energy flow in the reefs, ecosystems of rich biodiversity. Photosynthetic symbionts also nourish animal species such as Hydra viridis and Convoluta roscoffensis. Although the latter can be 15 mm-long, this turbellarian flatworm is devoid of functional pharynx and mouth, so, unable to perform heterotrophic nutrition, relies solely on their endosymbionts for survival [ 45 ].
In addition symbiotic microbes take part in blood meal digestion in the lice Pediculus sp. Parasitism Ecology Since parasitology approaches the interactions among species and their environment which may be our very bodies , it is considered an area of ecology [ 46 ].
In fact parasitism, as well as other types of ecological relations, is considered symbiotic consortia. Currently, the evolutionary biologists are beginning to recognize parasitism as an important creative force of biodiversity [ 47 , 48 ]. When our societies moved from the hunter-gatherer way of life to farming, our populations reached much higher numbers, supporting many epidemics and keeping the sedentary humans in close contact with flock animals as well as with its feces, urine, tissues, and so forth [ 49 ].
Infections from wild animals such as AIDS, schistosomiasis, leishmaniasis, tularemia, and many hemorrhagic fevers comprise important sources of emergent and reemergent diseases. Parasites are continually exploring new available ecological niches in our organism and therefore originating emergent diseases. Protozoa such as Giardia are increasing its prevalence due to the vacant niches left by helminthes, as a result of the more efficient antihelminthic compounds used in both humans [ 50 , 51 ] and domesticated animals [ 52 ].
New vacant niches are eventually tried by parasites as in the reports of enteric parasitism of human beings by Ancylostoma caninum adult worms [ 53 ], as well as the human infection by monogenetic trypanosomatids [ 54 , 55 ], normally found infecting insects.
Emergent diseases can both regulate the biodiversity of the wild life and threaten human beings [ 56 ] as well as other animals. Species invading new areas that leave parasites behind and encounter few new parasites can experience demographic overgrowth and become a pest [ 57 ]. In addition, invasive plant species that are more completely free from pathogens are more widely reported as harmful invaders of both agricultural and natural ecosystems.
This indicates that parasite loss in animal and plant species invading new areas may confer significant competitive advantage, rendering them pests menacing the new ecosystem biodiversity. Zoonosis such as brucelosis, leptospirosis, salmonelosis, tuberculosis, and echinococcosis can cause considerable mortality and morbidity to human beings.
It is worth noting that about two thirds of the emergent diseases had a zoonotic origin [ 58 ]. Parasitic diseases such as the different types of malaria had probably evolved from primate or avian infections [ 60 , 61 ]. The recent outbreak of avian Influenza in Hong-Kong, with some serious and even fatal human cases, brings to mind the pandemic of Influenza that caused the death of more than 20 million people and had an avian origin, whereas the emergent H1N1 appears to be derived from swine infections [ 62 ].
The cuckoo birds cuculids as Cuculus canorus L. Thus these species act as parasites and parasitoids or necrotrophs [ 63 ] at the same time. The parasitic infection, frequently deleterious at the individual level, can not only be advantageous for the populations, but even for the organisms individually [ 64 ].
These ecological relations can evolve into advantageous balances for both partners. Trophozoites of Entamoeba gingivalis and Trichomonas tenax, found in the human oral cavity, can help controlling the bacterial populations. Some bacteria of our intestinal flora produce compounds useful for our metabolism, including glycosylhydrolases required for the optimum digestive system functioning. Enteric bacteria also induce and regulate the expression of many genes in the gut, such as fucosyl transferase enzyme characteristic of mouse intestinal villi [ 65 ], colipase, which is important in nutrient absorption, angiogenin-4, which helps to form blood vessels, and Small proline-rich protein 2A Sprr2a , that fortify matrices that line the intestine [ 66 — 68 ].
These cells respond to B. There is growing recognition that microbial residents of the gastrointestinal tract might be important for both our understanding and treatment of obesity. However, many questions remain to be answered about the possible mechanisms [ 69 , 70 ]. The intestinal flora can be affected by nematode infection as Angiostrongylus costaricensis, in mice [ 73 ].
The human gut may present — bacterial species and the number of microorganisms associated to our mucosae can be tenfold higher than the total number of human cells around ten trillion, , summing up nearly 1. The pattern of the gut microflora is peculiar for each individual [ 74 ]. Whenever imbalanced, the intestinal flora can be highly harmful and thousands of children die every year due to bacteria such as enteropathogenic or enterotoxigenic Escherichia coli [ 75 — 77 ] it should be noted that multiple pathogens are often associates simultaneously [ 78 ].
However, the normal intestinal flora presenting bifidobacteria and lactobacilli has great metabolic importance, including the vitamin production. In general the excrements of an animal have more of certain vitamins than its food, a fact that explains why so many species carry out coprofagy. Vitamin K menaquinones is produced by intestinal bacteria such as Bacteroides, Eubacterium, Propionibacterium, Fusobacterium, Bifidobacterium, Lactobacillus, Clostridium, Enterococcus, Streptococcus, and others.
The lack of these bacteria in neonates kept in incubators or subjected to antibiotic therapy may lead to the deficiency of menaquinone-dependent coagulation factors and hemorrhagic disorders.