What do you call a type of interaction where parasites live outside or inside the body of the host?

Origins of Parasitism and Complex Life Cycles

Few fossil parasites are known. They include schistosome eggs from ancient Egyptian mummies a few thousand years ago and galls on the arms of feather stars, probably produced by Myzostomida (parasitic annelids) from the Silurian and Devonian periods, 350–430 million years ago (Ma). Conclusions on the origins of parasitism and parasite life cycles must therefore be based on inferences from comparative studies of extant species. The Platyhelminthes have been studied most thoroughly, using DNA studies of several genes, in particular 18-S rDNA and 28-S rDNA, and phylogenetic systematics (cladistics). Phylogenetic systematics seeks to establish branching patterns in phylogeny on the basis of shared acquired characteristics (synapomorphies). Ultra-structural characteristics are of particular use because of their complexity. Cladistic and DNA studies by many authors have consistently shown that the Neodermata, the major groups of parasitic flatworms (Trematoda, Monogenea, and Cestoda), all share a common ancestor, i.e., are monophyletic. The Neodermata, or the Neodermata plus some of the parasitic turbellarians, are the sister group of a very large taxon, including most Turbellaria, with which they share a common ancestor. This means that the parasitic groups evolved very early in evolutionary history. Among the Neodermata, the trematodes are the sister group of the other Neodermata and, among the trematodes, the Aspidogastrea are the sister group of the other trematodes or Digenea. Three of the four families of Aspidogastrea occur in elasmobranchs, whereas almost all digeneans parasitize teleost fishes, amphibians, reptiles, birds, and mammals; very few species of Digenea have been recorded from elasmobranchs, to which they have secondarily adapted. Fossil records indicate that elasmobranchs are 450 My old and teleosts are 210 My old. This suggests that the Aspidogastrea are the oldest extant trematodes and possibly neodermatans. It also suggests that the simple life cycle of Aspidogastrea (Figure 5 is the original life cycle of trematodes, including a final and an intermediate host (which, in some species, is not obligatory), without multiplication of larval stages in the intermediate host. The complex life cycles of digenean trematodes, including a final and at least one, and up to three, intermediate hosts and several transport hosts, with multiplication of larval stages in the first intermediate host (Figure 6), may have evolved from this primitive kind of life cycle to make transmission to the final host more effective.

Among the crustaceans, most barnacles are free-living, attached to rocks or other hard substrata. Some barnacles live in a phoretic association, for instance with whales, attached to their skin and feeding on plankton in the environment. Other, closely related species have become parasites. Thus, Anelasma parasitizes the skin of sharks, processes of its stalk branching in the host's muscles and extracting food from it. All the approximately 120 species of rhizocephalans, also related to the barnacles, are parasites and strongly modified in adaptation to their way of life (see, e.g., Sacculina, Figure 1). This suggests that parasitism in the barnacles may have evolved from free-living to phoretic to parasitic.

Abstract

Parasitism is a pervasive phenomenon in nature involving, either as hosts or as parasites, virtually all species on earth. By definition, parasites are costly for their hosts as they divert resources for their growth, reproduction and survival with no rewards for the hosts. Parasitism is not restricted to a few taxonomic groups since a parasitic life style has evolved in viruses, bacteria, protozoa, invertebrate and vertebrate metazoan. This taxonomic diversity is, of course, also associated with a tremendous diversity of life cycles, host exploitation strategies, transmission modes and virulence levels. Given the cost of parasitism, hosts are expected to evolve defense mechanisms aiming at limiting the negative effect of parasitism on their fitness. In agreement with this view, hosts have evolved a series of morphological, physiological, behavioral adaptations to fight off parasitic attacks. On their side, parasites have responded to the selection pressures exerted by their hosts by evolving counteradaptations to overcome host defenses. These cycles of host–parasite adaptations–counteradaptations define the so-called coevolutionary process, one the most prominent characteristics of host–parasite interactions.

Parasites Are Everywhere

Parasitism is the most popular lifestyle on Earth. Roughly, half of plants and animal species are parasitic at some stage of their life cycle. Few species, if any, lack any parasites and most species have at least one host-specific parasite species. Even parasites have parasites. We know the most about humans, who host 342 parasite species, not including viruses and bacteria. Many of these only parasitize humans. Parasites tend to be more abundant in places where hosts are abundant and more diverse in places where hosts are diverse. For instance, more parasites species are found in the tropics than at high latitudes. While parasite diversity follows host diversity, parasitism may also select for diversity in host communities.

Parasitism

Parasitism of plant pathogens as a mechanism of biocontrol is usually associated with fungal biocontrol agents. Most evidence for this comes from field observations of infected fungal propagules such as spores or sclerotia. For example, oospores of Phytophthora and Pythium spp. are frequently found to be infected by Olpidiopsis gracilis, whilst sclerotia of R. solani are infected by the obligate sclerotial mycoparasite Verticillium biguttatum. The interaction between the mycoparasite and its host involves a sequence of processes encompassing location, contact, recognition, localized lysis, penetration, intracellular growth, and exit. Various chemical interactions are implicated in these processes, including involvement of lectins during the initial contact, and recognition between mycoparasite and the host fungus and a suite of different cell wall-degrading enzymes (e.g., β-1,3-glucanases, chitinases, proteinases, and lipases) during the penetration process. Other mechanisms of parasitism are associated with fungi such as Verticillium chlamydosporium and Paecilomyces lilacinus, which can infect the egg masses and cysts of the cereal cyst and root knot nematodes.

2.2.2.1 Parasitism

Parasitism is a nonmutual relationship between two organisms in which one benefits at the expense of the other. There are two types of parasites affecting living organisms: ectoparasites (living on the surface of host) and endoparasites (living in the body of host). Periphyton parasites can alter the physiology and behavior of the host, resulting in changes in density, survival rates, life span, and growth rates (Thomas et al., 2011). The effect of parasitism on aquatic communities, especially on periphytic communities, is poorly described and studied, which might be due to their small size and difficulty in determining the energy transfer between host and parasite (Combes, 2001; Dobson and Hudson, 1986). Thus, the role of one of the most influential communities in aquatic foodwebs is sometimes ignored (Lafferty et al., 2006; Marcogliese and Cone, 1997).

The periphytic community is either affected by organisms infected with parasites or they are themselves affected by a parasite. To determine the rate of parasitism in periphytic communities and zooplanktons, Wolska (2013) studied two lakes in Drawa National Park, Poland, for 3 years and observed that 0.8% of Chydorus sphaericus (Cladocera, Chydoridae) was infected by Saprolegnia sp. (chromistan fungal analogues, kingdom Chromista) and 1.2% of Brachionus calyciflorus (Rotifera) was infected by protozoan Microsporidium sp. (Fig. 2.3), while 5% of a population of nematodes was infected by Pythium sp. They did not explain the effect of these parasites on the periphytic communities.

Periphytic communities are also affected by the parasitism of grazers and other organisms feeding on them. Snails are the dominant grazers of periphytic communities and can affect algal biomass, community composition, and primary production (Bernot and Turner, 2001; Lamberti et al., 1989). The snail Physa acuta infected with trematodes Posthodiplostomum minimum had higher rates of grazing on periphyton (almost 20% higher) compared with the uninfected snails. Cladophora glomerata (algae) was more dominant after grazing by infected snails, whereas diatoms and blue-green algae were dominant in the biofilms grazed by snails with lower infection levels (Bernot and Lamberti, 2008).

Enhanced Susceptibility to Other Factors

Parasitism may make hosts more susceptible to predation [Godwin & ODell, 1981 (p. 383); Jones, 1987] or disease (Godwin & Shields, 1984). Such events, occurring after parasitoid attack, do not change actual parasitoid-caused losses. Such factors may, however, obscure the actual rate of parasitoid attack, with deaths of parasitized hosts later eaten by predators being assigned in life tables to secondary agents of mortality instead of to parasitism. These deaths can be assigned correctly to the original cause (parasitism) by careful design of the sampling scheme, particularly by measuring recruitment, as discussed earlier. A more complicated situation arises in evaluating natural enemies of plants, because death may result from several factors acting together. In some cases, the presence of one factor can enhance the detrimental effect of another (Huffaker, 1953; Andres & Goeden, 1971; Harris, 1974). One approach to quantifying the relative contributions and interactions of these multiple factors is to use field experimental plots with different combinations of natural enemies (McEvoy et al., 1990, 1993).

The presence of parasitoids in systems can also lead to healthy individuals experiencing greater mortality from other factors. For example, Ruth et al. (1975) noted that when greenbugs, Schizaphis graminum (Rondani), were exposed to the braconid Lysiphlebus testaceipes (Cresson), 41.0 to 62.0% of the aphids left their feeding sites, often falling to the soil. Such aphids were more likely to die due to high soil temperature before reestablishing themselves on plants than were undisturbed aphids. Pea aphids also leave their host plants when disturbed by parasitoids (Tamaki et al., 1970).

In addition to effects on individual hosts, the presence of parasitoids may cause changes at population levels in other mortality factors. For example, introduction of exotic parasitoids suppressed winter moth, Operophtera brumata (Linnaeus), in British Columbia (Embree & Otvos, 1984), but apparently did so by making ground-inhabiting pupal predators more effective (Roland, 1988).

While the preceding types of losses are properly assignable in a life table to the actual cause of death, it is important to be aware of any enhancement in levels of mortality caused by the presence of a natural enemy. This enhancement may be significant and must be considered when evaluating the overall impact of a natural enemy in a system.

Parasite Diversity

Parasitism has evolved at least 223 times in 15 of 35 recognized animal phyla (Weinstein and Kuris, 2016). It is believed that parasitism evolved through a variety of opportunistic circumstances: from using larger animals for food, shelter, increasing dispersal potential, and maintaining more consistent environmental conditions by living in close proximity (Poulin and Morand, 2004). There are also cases of parasites that are closely related to their hosts—even within the same species. For example, ceratoid angler fish have adopted parasitism to solve the problem of reproduction in the darkness of the ocean depths. In some species, once the male locates the female, he latches on to her and eventually fuses to her, providing sperm to fertilize her eggs. As he is then permanently attached, he derives nutrients from the female (Pietsch, 2005).

Hosts may have one to many species of parasites. For example, Thyrsites atun, a predatory species of snake mackerel that occurs in the southern hemisphere, has been found to host 16 species of parasites (Nunkoo et al., 2016). Such data have led researchers to the conclusion that there are more parasitic species than host species (Toft, 1986; Poulin, 2014). Even so, of all described animal species, it is estimated that only 5% are parasitic (Costello, 2016). There have been many discussions about why there is this lack of described parasitic species, particularly referencing; their cryptic lifestyle and the difficulty in locating and identifying parasitic species; the lack of research in large geographic regions, for example, the deep ocean; the predicted hyper diversity; a paucity of parasite taxonomists; the use of as yet unrecognized synonyms; and under-sampling even within well studied taxa (e.g., birds and elasmobranchs) (Rohde, 2002; Caira and Jensen, 2014; Chaudhary et al., 2016; Poulin and Presswell, 2016; Jorge and Poulin, 2018).

With the introduction of data-centred science (Kelling et al., 2009) and a renewed effort to determine how many species there are in the world, analyses by some researchers have concluded that most species on earth have been named (Costello et al., 2012, 2013a; Costello and Chaudhary, 2017). Costello et al. (2015) analyzed the trends in rates of description for 32,000 fish species globally. They discovered that the species to be first described tended to be more widespread and larger in size and occurred in shallower depths and near more developed countries (e.g., northern hemisphere). In analyzing trends in rates of description for parasites in both marine and terrestrial ecosystems, Costello (2016) found that most molluscs, crustaceans, ticks, fleas, and insects had decreasing rates of description since the year 2000, with the peak discovery period for helminths and microsporidians occurring in the 1970s. This suggests that most parasites have been named and that further surveys for parasitic diversity will demonstrate that parasitic species discoveries may not yield as many species as non-parasitic taxa (Costello, 2016), challenging current predictions (Poulin, 2014).

Parasitism

Parasitism can be a potentially important process influencing demographic patterns and the small-scale spatial distribution of sandy-beach macrofauna. Trematodes and cestodes are the most common parasites infesting sandy-beach mollusks, both gastropods and bivalves. Some groups of crustaceans also tend to be infected, including decapods such as Emerita. The mollusk or crustacean acts as intermediate host and the final host is commonly a fish or bird. Plant parasitic nematodes are important components of the energy flow and trophic relations in coastal dunes (see Chapter 13).

Poulin and Rate (2001) and Poulin and Latham (2002) demonstrated that parasites affected the burrowing depth of Talorchestia quoyana on New Zealand beaches. Amphipods that harboured larger parasites burrowed deeper than expected based on their body size. Rasmussen and Randhawa (2015) studied the abundance and biomass of a mermithid parasite in sand hoppers (Bellorchestia quoyana), both within and among six disconnected beaches in New Zealand, and found that geographic isolation was responsible for minor differences in parasite populations compared with host size, the most important predictor of mermithid parasite abundance. Epibiont abundance, kelp patch mass, and host density were poor predictors of abundance and of parasite biomass in hosts.

The direct effects of a changing environment, including warming, could enhance disease expression in cases of marine populations and pathogen abundance (see Chapter 16). Pathogens have been mentioned as potential causative factors of mass mortalities in the yellow clam M. mactroides in South American Atlantic sandy beaches: parasites and necrosis in gills and stomachs were found during mass mortality events (Cremonte and Figueras, 2004; Fiori et al., 2004) and in the congeneric M. donacium on Pacific coasts (Riascos et al., 2011). In M. donacium, a lower body condition index was related to the level of infestation by a parasitic polychaete that increased its prevalence under increasing temperatures during a warm El Niño phase (Riascos et al., 2008).

Evolution of the Degree of Parasitism

The evolution of parasitism has been difficult to study because intermediate evolutionary stages between non-parasitic ancestor and extremely derived holoparasites are often missing. The variability in the degree of parasitism and the multiple origins of parasitism make these plants ideal for studying the evolutionary origins of parasitism and the often rapid canalization of parasitic traits. The degree of parasitism refers to increases in the dependence that parasitic plants have on their hosts. Aspects of the degree of parasitism include the amount of carbon, water, or sugar obtained from the host, as well as major changes in the way that parasitic plants relate to a host. These major shifts include the evolution of stem parasitism or the evolution of an endophytic life history. The evolutionary factors that have influenced these events remain one of the most important questions about parasitic plants.

Changes in the degree of hetrotrophy represents one of the most interesting and best-documented cases of quantitative evolution of parasitism. Some hemiparasitic root parasites and mistletoes are almost entirely autotrophic—that is, they obtain a small fraction of their carbohydrates from their host whereas holoparasitism (100% heterotrophic) occupies a presumably irreversible end-point of this quantitative scale. Most clades of parasitic plants are entirely hemiparasitic or entirely holoparasitic. Krameriaceae are all hemiparasites, while the Hydnoraceae, Rafflesiaceae, Apodanthaceae, Mitrastemonaceae, Cytinaceae, Lennoaceae, Cynomoriaceae, and Balanophoraceae are entirely holoparasitic. Cassytha and Cuscuta are often called holoparasites, although these species have very low amounts of chlorophyll. Cassytha species are yellow-green in color, while Cuscuta species are more orange-yellow. In Cuscuta, chloroplasts are less than 10% as numerous as in autotrophic plants but the green color is masked by yellow pigments.

Members of the order Santalales are mostly hemiparasitic, but at least one species represents a very advanced stage of parasitism. In Arceuthobium, the endophyte is extremely well developed and the leaves are reduced to scales. The most derived parasite in the Sandalwoods is found in the endophytic parasite, Tristerix aphyllus. Tristerix aphyllus is a parasite of columnar desert cacti, whose endophytic life history may allow the parasite to escape the hot and desiccating desert conditions. Curiously, T. aphyllus and all Arceuthobium species retain some chlorophyll, and in spite of these extreme advances toward parasitism, true holoparasites are absent in the order.

In contrast to the conditions in Santalales, within Orobanchaceae, holoparasitism has evolved on several occasions. In fact, some species include hemiparasitic and holoparasitic populations and the degree of heterotrophy varies substantially. Peter Atsatt (1970) was able to produce holoparasites in a few generations in artificial selection experiments. This suggests that the complete evolutionary loss of autotrophy, as seen repeatedly in Orobanchaceae, may be relatively common in nature. One obvious conclusion is that holoparasitism is more likely to evolve in root parasites than in stem parasites. Since root parasites are often found in the dark understory, the selective advantage of retaining functional chloroplasts in root parasites may be much weaker than for sunbathed stem parasites. In fact, holoparasitism in beech drops (Epifagus virginiana, Orobanchaceae) is clearly irreversible because entire sections of the genome that contain the genetic instructions for photosynthesis have been deleted.

The evolution of the mistletoe life history represents a different kind of innovation in the degree of parasitism that is different from the evolutionary loss of chlorophyll. Stem parasitism may have evolved more than once within the Sandalwoods; two families, Santalaceae and Loranthaceae, have both stem and root parasites. It is possible that these represent paraphyletic taxa, but it is also possible that study of intermediates between root and stem parasites in Santalales will lead to an understanding of the evolutionary forces that led to the evolution of stem parasitism from root parasitism.