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By Claude Combes
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ISBN: 0226114465
1 The Universe of Parasites
Living organisms produce four types of wealth: their matter (body, organs, etc.); their metabolism (chemical reactions, enzymes, etc.); their work (movement, care of young, etc.); and the products of their work (nests, houses). These assets are coded for, either directly or indirectly but without exception, by the organism's genome and constitute, in its broadest sense, the phenotype (Dawkins 1982).
As in all cases of riches and wealth, other living organisms often lust after these assets, the most sought after being those stored in the form of the organisms' bodies: each second on earth, in prairies and forests, in soils, in lakes and rivers, and in the deepest seas and oceans, billions of living organisms are preyed on by others who covet energy in this form. These are, of course, the predator-prey systems so often described in ecology texts.
Besides the energy exchange of predator-preysystems, however, energy exchanges also occur because of parasite-host systems: just as the predator takes energy from its prey, the parasite takes energy from its host. But one major difference between predator-prey and parasite-host systems is that in the former the actors are usually visible to each other, with scenes happening before our eyes even when played out at such vastly different scales as a lion capturing a buffalo or a spider trapping a fly. In parasite-host systems one of the protagonists is, at best, difficult to observe. Although there are a few exceptions, parasites are in general actors that play in the shadows--perhaps the reason they have been ignored until so recently by mainstream ecologists.
Yet other differences between predator-prey and parasite-host systems become visible when one looks at the level of individuals and how they interact. In predator-prey systems the interaction between the predator and its prey is instantaneous or nearly so (e.g., when a cat catches a mouse, when a fox eats a hen, or when a frog snatches an insect). At most the interaction is only as long as the time of pursuit or waiting and a period of digestion. Moreover, and in virtually all cases, the predator exploits only the first of the four energetic assets of its prey: its matter. In a parasite-host system, that is, when an organism lives on or in another (a tick on a dog, a fluke in a sheep's liver, etc.), the interaction is prolonged and often broken only by the death of one of the protagonists. Because of the length of the interaction, the parasite can exploit not only the material assets of the host but also the other three types of wealth produced by the host's genome: its metabolism, work, and products. Not only is host matter exploited as an energy source, it also becomes a habitat for the parasite.
Although at the level of the biosphere the global transfer of energy from hosts to parasites is negligible when compared with that of prey to predators, the parasite-host interaction may have consequences that reach far beyond the scale of the individual host because of the prolonged and durable nature of the interaction. Parasites, more subtly but not less significantly, can affect host populations in profound and significant ways (Anderson and May 1978a, 1978b; May and Anderson 1978).
Although at first one might see little or nothing in common between a virus, a mitochondrion, a trypanosome, a fluke, a tick, and a cuckoo's chick, what unites these organisms and gives them cohesion is the durable nature of the interaction between the one called the parasite and the one called the host. This is true no matter what the systematic position of the partners, no matter the way the interaction is borne out, and no matter even that the benefits and costs of the association may be unequally shared.
Because of the different nature of these prolonged energetically based associations, I have previously proposed the term "durable interactions" (Combes 1995) to describe all such associations between genomes that, either directly or through the intermediary of the phenotype, last for extended periods.
Figure 1.1 symbolizes the expression of the parasite's genome within the context of the host's phenotype and the expression of the host's genome within the context of the parasite's phenotype. Significantly, and because of the prolonged interaction of the protagonists, we can view the parasite-host association as a system --meaning the association takes on novel characteristics of its own that are not just the simple sum of its component parts. In short, these new characteristics are due to the interaction of the crossed phenotypes of the parasite and host, each of which may be interfering with the other and each of which is being expressed under the influence of the other's (Combes 2000).
Consequences of the Durable Interaction
The durable interaction has four major consequences, each linked to the fact that there are, side by side, two genomes. This fact makes it, in a sense, a superorganism possessing a "supergenome."
First Consequence: The Parasite's Genome Is Expressed in the Context of the Host's Phenotype
To communicate with each other the different parts of a living organism, as well as the different individuals of the same species, use signals (molecules coded directly or indirectly by genes) that are recognized by receptors (other molecules coded for by other genes). All organisms, from the simplest to the most complex in organization and function, use the same fundamental constitutive molecules, metabolic processes, information storage processes, and chemical systems in this communication, and an exchange of signals is made possible between the parasite and the host because of this remarkable unity of life.
In a parasite-host association, the signals produced by the genome of one of the partners may act on the phenotype of the other, thus crossing the species barrier and inducing morphological, anatomical, physiological, or behavioral changes in the recipient. The expression and extension of the parasite's genome into its host's in this way gave Dawkins (1982) one of the most striking illustrations of the concept of the extended phenotype, which is a phenotype envisioned to occur beyond the physical limits of the organism to which the genes belong. Among other examples of the extended phenotype, Dawkins cites galls--growths on plants within which certain insect larvae develop. These structures are the result of selection, in the insect genome, of genes able to manipulate the growth of the plant host tissues in their surroundings.
The possibility that a parasite's genome may influence the host phenotype, as in the case of galls, is not necessarily restricted to the action of signaling molecules, however, and in certain "sensitive organs," like those within the nervous system of animals, the parasite's physical presence alone may modify the physiology or behavior of the host.
The influences of a parasite's genes on host physiology and behavior in these ways are sometimes both profound and obvious, and they may favor either host-to-host transmission, the exploitation of the host, or escape from the host's immune system. In some cases, however, the para-site's influence is not very visible, and as a result its consequences may be underestimated. Given that all organisms are parasitized at some time during their life spans, one may wonder if in fact there is even one durable interaction that does not imply a manipulation of hosts, however subtle, by parasites. (Is there even one free-living animal that owes its physiology and behaviors solely to its own genes?)
Second Consequence: The Host Genome Is Expressed within the Context of the Parasite's Phenotype
As soon as a parasite-host system forms and lasts, there is a high probability that some of the genes (or gene combinations) making up the "supergenome" will be duplicated. This does not mean that such genes have an identical nucleotide sequence but rather means that they have similar or overlapping functions. When such double-usage genes exist there is a tendency for one of the two genes to stop being expressed over the course of evolution. This may happen either because mutations abrogate the function of one member of the pair, with the system surviving because of the second gene, or more simply because of the cessation of expression of one of the genes in one of the partners. Double-usage genes lost in this way may become pseudogenes (sequences not translated into proteins), or they may ultimately be deleted.
In general parasites and not hosts lose genes, which explains the observed regression of functions otherwise ensured by the host genome in many parasites. That is, the direct consequence of the extension of the host's phenotype into the parasite is the exploitation of the host genome. This is attested to by the fact that all parasite descriptions emphasize morphological simplifications and that parasites save on numerous morphological and functional accessories, such as organs of locomotion, digestive and enzymatic systems, and sense organs because their hosts can take care of the corresponding functions of obtaining food, digestion, and avoiding enemies. An example of organs being lost through this process is the disappearance of the digestive tract in cestodes, while an example of the resulting functional dependence of parasites on their hosts is the lack of the enzymes necessary for purine metabolism in all known parasitic protozoa and some parasitic metazoa, such as the schistosomes. In all these organisms purine metabolism must be ensured by the hosts' enzymes.
What happened to the genes that coded for digestive systems or the enzymes of purine metabolism in the ancient ancestors of current parasites is still an unanswered question. Nevertheless, when such genes are truly lost by the parasite, the survival of the species depends, from then on, strictly on the host. The parasite is "linked" to the host genome and can no longer survive without that host.
Third Consequence: Innovative Genes
Although parasites often depend on host genes for important functions, nothing prevents the host from exploiting the parasite's genome if similar or better genes exist in the parasites. In this case the loss of a double-usage gene may happen in the host, which then becomes as dependent for survival on the presence of the parasite as the parasite is on the host. In this case the parasite is referred to as a mutualist, and the association constitutes mutualism.
Thus parasitism and mutualism can be differentiated not only by energetic constraints but also by the fate of double-usage genes: if gene expression stops only on one side, there is parasitism; if different genes on each side stop being expressed, there is mutualism. Cheng (1991) expressed this difference nicely by emphasizing a unilateral physiological dependence in the case of parasitism and a bilateral dependence in mutualism. This distinction was further clarified by Smith (1992): "In parasitism, hosts are exploited by parasites; in symbiosis, hosts always exploit their symbionts, although simultaneous exploitation of host by symbiont may occur in certain associations."
An advantageous situation for the host occurs when the parasite brings not simply a "better" gene but a "new" gene or genes that code for a novel function, such as a new synthetic or metabolic pathway. In acquiring such "innovative" parasite genes the host makes "an evolutionary leap" in the sense that the new function is gained virtually at once and without patient selection and adjustment. Viewed in this way, parasitism is certainly not a marginal process in biological evolution (see Szathmary and Maynard Smith 1995). At least in the first stages of life, and as evidenced by the mi-tochondrion--the central piece of eukaryotic cell oxidative metabolism and itself an "ancient bacterium"--the acquisition of innovative genes via such a durable interaction likely has played an essential role in the process resulting in the evolution of the more complex life forms themselves.
Obviously, innovative genes coding for novel functions may also have appeared via mutation in one of the partner species after the parasite-host relationship was initiated. In this case the gene may be exploited by both species.
Regardless of the source of the exploited genes, however, selection will not occur under the same conditions in parasitic and mutualistic associations (fig. 1.2).
In a parasitic association the system receives resources from the outside, and both partners are in competition for these resources. This competition puts very strong selective pressures on both the parasite and host, with each constituting separate units of selection. These selective pressures can be far stronger than those pressures between the association and the other units of selection affecting it in the ecosystem.
In a mutualistic association, on the other hand, the selective pressures between the partners becomes less important (although not nonexistent), and the association itself forms the major unit of selection (see Maynard Smith 1989c). In this case the most notable pressure results from the unit's interacting with other entities of selection in the ecosystem.
Fourth Consequence: Gene Exchange
The prolonged association between two organisms with different genomes provides an ideal mechanism for the exchange of genes between associated members. Although we know they exist, however, little is known about such transfers in nature. At least in durable interactions of very ancient origin (such as the ones linking mitochondria and chloroplasts to eukaryotic cells), some exchanges of genes have occurred during evolution. It is thought that such exchanges may involve mobile DNA elements, viruses, bacteria such as Wolbachia, or still other as yet unidentified mechanisms, and it is suspected that these exchanges may have played a major role in numerous evolutionary processes, one of the major ones being the evolution of the mechanisms by which parasites escape host immune systems.
The Frontiers of the Durable Interaction
Although some workers spend a good bit of time debating whether specific organisms should or should not be classified as parasites, the more encompassing concept of a durable interaction removes all ambiguity and allows us to bring together, alongside parasitism and mutualism, associations such as inquilism (obtaining habitat without taking food), phoresy (obtaining transportation for a set period), and parasitoidism (a durable interaction terminated by the assassination of the host). This concept also allows one to exclude without hesitation organisms whose interaction exists only for the short time of a meal. It is not reasonable to classify as parasitic organisms such as mosquitoes or tsetse flies just because, like parasites, they consume a fraction of an organism without killing it. If we accept mosquitoes as parasites, then we should call the cow that eats grass without killing it, the sparrow that eats cherries without swallowing the entire cherry tree, and all other herbivores, parasites as well. Mosquitoes, tsetse flies, and other insects find their place in parasitology textbooks as vectors of parasites, not as parasites themselves, and it is only when some such species succumbs to the attraction of a habitat provided by another organism, or to taking food exclusively from the same host, or to obtaining a convenient mode of transportation that it would acquire the rights to the parasitic world. Ticks, for example, spend enough time on their hosts so that a typical durable interaction is established--they make molecules that affect the host phenotype by rendering the blood meal both easier and longer lasting: "Tick saliva contains a cocktail of pharmacologically active compounds (e.g. immuno-suppressants, analgesics, anticoagulants, antiplatelet aggregatory compounds)" (Bowman, Dillwith, and Sauer 1996).
As always in biology, however, there are marginal situations that are difficult to classify. Although it is clear that a bee that gathers pollen from flower to flower has nothing to do with parasitism, it is not unreasonable to consider as parasitic the caterpillar of a butterfly who spends its entire larval life on the same nourishing plant.
We should perhaps add another comment about parasitoids, which, after a phase of "classical parasitism" when genomes interact, then kill their host. The best known are insect parasitoids of other insects, but we must also include in this group some viruses (bacteriophages) that, after an initial interaction period, kill their bacterial hosts. Although the end of the association resembles that of predator and prey, the relationship between parasitoids and their victims must be classified among durable interactions because the period of interaction shows numerous facets of the extended phenotype, most notably the forced insidious entry of the parasite genome into the host phenotype.
Last, what fate should we reserve for the word "symbiosis," which literally signifies "life together" and therefore notably applies to the concept of a durable interaction? The word was created at the end of the nineteenth century by the German botanist Heinrich Anton de Bary to designate all associations of two species living together, including parasitism, mutualism, inquilism, and so forth. This is the sense that is always used by certain authors, such as Cheng (1970) and other American workers. Often, however, the appellation is more restrictive and applied only to associations said to be "with reciprocal benefits," here called mutualism. Because of this dichotomous usage, I will make limited use of the term symbiosis, which is also the choice made by Bronstein (1994a): "To reduce semantic confusion, I will use the term mutualism exclusively."
The associations that lead to durable interactions are infinitely numerous in the living world. In fact no organism exists, and none may ever have existed (except at the very beginning of life), that does not establish or is not subjected to a durable interaction with at least one other organism. All living organisms are involved in parasitism, either as hosts or as parasites themselves (Price 1980), and these interactions continue to play an essential and major role in biological evolution and the functioning of the biosphere as we know it.
Why Parasites?
In the "beginning," the ancestors of organisms currently living in association with each other were free-living and not connected. Because in evolution changes most often relate to cost-benefit relationships, we must therefore consider two things: why once free-living organisms found more advantages than disadvantages in adopting the parasitic mode of life, and why free-living organisms that became hosts either were unable to eliminate the parasites or found advantage in such a situation themselves.
To understand why a free-living organism acquires a parasitic lifestyle via selection, one can first consider two free-living species that share the same environment at a given time, then wonder about the advantage that some individuals of one of the two species (call it A) have in taking the second species (B) as their living habitat. It is not enough to say that individuals of species B constitute environments; one must also demonstrate that individuals of species A that possess genes inducing the choice of B as a living milieu benefit from an increased fitness compared with those that remain free-living.
There are three main advantages that individuals of B can give to individuals of A (fig. 1.3): habitat, motility, and energy.
Habitat
As long as a species is free-living its members are subject to fluctuations in the environment and to the aggression of other free-living organisms. If certain individuals of this species take individuals of another species for their habitat, we may speculate that they might immediately benefit in two ways: they would occupy a more stable milieu than the exterior environment, and they would be sheltered from the predators and competitors they might otherwise face while free-living.
One cannot contest the fact that a living environment is stable. Living organisms possess mechanisms to ensure homeostasis, or the consistency of a number of physicochemical parameters. Blood composition, for example, is maintained with amazingly little variation, and in many organisms, such as birds or mammals, temperature remains constant. Therefore it is more "comfortable" to live inside a polar bear or desert rat than in the environments where the polar bear and rat live. This may be one reason most parasites have shortened their stay in the external environment as much as possible and also why some have rid themselves of this phase entirely.
That a living environment provides protection from predators, though, deserves more discussion. First of all, this is not necessarily true so long as individuals of A remain outside individuals of B--if they are ectoparasites. It is well known that cleaner fish pick off and eat the ectoparasites of other fish and that cleaner birds peck ectoparasites from the fur of mammals. Whittington (1996) showed that some fish ectoparasites even select for camouflage (i.e., for a transparent body and colored spots) that provides some protection from cleaner fish, and Euzet and Combes (1998) have suggested that the pressures exerted by such predation may in some cases have induced the passage from ecto- to meso- or even endoparasitism in monogeneans. Relative to these worms' habitat these authors write: "If, in a population of a given species, there is a polymorphism of habitat preference, some individuals may remain on the skin while others tend to penetrate inside the body. A process of natural selection can then give rise either to a gradual change in the habitat of the whole population or to two different populations (which may later evolve into separate species)."
In short, then, protection from predators is provided only if individuals of species A find refuge inside individuals of species B. Further, and in an amazing turn but with very few exceptions, parasites are protected from predation in another way: they do not tend to eat each other. Parasites live in a miraculously pacifist world where there are no prey and no predators and where, at the most, bacteria may be absorbed by parasites much bigger than they are. In other words, all parasites are at the same trophic level. As soon as an organism lives on the gill of a fish, in the bladder of a frog, the duodenum of a mammal, or in the tissues of a seed, no other organism will pursue or devour it. In evolutionary terms, it is free to leave aside the apparatus, including sensorial and locomotor organs, that allowed its free-living ancestors to detect and flee enemies. To illustrate the protection given to parasites by this mode of existence, Domitien Debouzie (personal communication) gives an estimation of the mortality rate in the chestnut weevil: as long as these parasitic insects are inside the chestnut the mortality rate is low, but as soon as they reach the ground to complete their development they fall victim to all sorts of predators and mortality increases dramatically (fig. 1.4).
Overall, then there are two clear advantages to having a living habitat: the stability of the environment and protection against predators.
There are, however, two objections to this assessment. First, although the living environment is stable it is also mortal; second, even though the parasite no longer has specific predators, it nevertheless inherits the predators of the host (all the parasites of a mouse should logically be digested when eaten by a cat). There are two responses to these objections:
Relative to the first objection, to live in a mortal habitat may not be as much of a disadvantage as it at first seems. Parasites themselves are mortal, and therefore establishing a durable interaction would not yield an infinite interaction for the individual. The problem is avoided by parasites' having life cycles that allow their descendants to infect the descendants of their hosts. All living organisms disperse their descendants (seeds get carried away by the wind, birds leave their nests, etc.), and for parasites dispersion out of the founding host is precisely the way to escape the dilemma of host death.
As for the second objection, it is true that virtually all host species (except top consumers) have predators. In each case, however, mechanisms have been selected so that predation does not usually imperil the host species, and parasites are in danger only if the host species is itself in peril. In fact there is even another possibility--that the parasite may take advantage of its host's being eaten by a predator (a mouse eaten by a cat, for example) by surviving in the predator. The parasite in this case wins twice, since it can successively exploit both the prey and the predator (the mouse and then the cat). Evolutionarily, it is then in the interest of the parasite that the cat eats the mouse. Certain parasites have used this as a means to navigate up the food chain and reproduce only in the top consumer, that is, in the host that has the fewest or no predators.
Still another argument in favor of the "security" advantage obtained by occupying a host as a habitat is that in nature any shelter is rapidly exploited by living organisms. For example, rocky coasts and coral reefs harbor a multitude of fixed or not very mobile animals such as sponges, corals, ascidians, and mollusks. These organisms increase the "porosity" of the physical environment, and these new niches are themselves colonized by an impressive list of tenants such as protozoans, planarians, copepods, amphipods, and annelids. Relative to cool ocean waters, the hosts of parasites are luxurious shelters that bring not just safety but also room and board.
Mobility
In many cases (almost all when the habitat is an animal) a living habitat is mobile. Based on this fact we can then ask, Could mobility itself have been the initial advantage obtained by acquiring a living environment?
The dispersion of propagules (a general term designating all forms, such as eggs and larvae, that serve in dissemination) is one of the major parameters of success of living organisms. If in a population certain individuals have a greater capacity to disperse than others, then their or their offspring's chances of survival may be increased, either by an increase in the probability of finding a suitable habitat, by the conquering of new areas, or by the reduction of intraspecific competition. Mobility in this sense is very important for a species, and the less mobile adults are, the more likely it is that some elaborate means of dispersion for its propagules has been selected. For example, plants or fixed aquatic animals ensure the dispersion of their gametes or planktonic larvae by developing various appendages and lift devices, such as bristles, blades, or umbrellas, that allow them to be carried away by the wind or to drift with the currents. The classical examples of such dispersal mechanisms are of course plants, which ensure the dispersion of their pollen by insect pollinators and their seeds by vertebrates (i.e., by hooking on to the fur or passing through the digestive system). When an organism is not very mobile it can improve the dispersion of its propagules by making them more mobile than itself.
Associating oneself durably to a mobile organism, as opposed to associating one's pollen or seeds, amounts to selecting an even more efficient mechanism of dispersion: instead of hooking propagules on to a vehicle, their producer (the adult organism) attaches itself to the vehicle and thus disperses its young throughout the host's travels. All parasites in the digestive tract of a mammal have their eggs or larvae dispersed more or less constantly in this manner as the living vehicle travels: all bird parasites fly with their hosts, and all fish parasites swim with theirs. This could explain why entire groups of parasites are restricted to mobile animal hosts and why they tend to disdain immobile plant hosts. When parasites do exploit immobile hosts such as plants or sedentary animals, their dispersion is ensured by different processes according to the group. For example, in insects parasitic of other insects and crustaceans from the monstrillid group, only the larvae are parasitic: in these cases dispersion is ensured by mobile adults, whereas in helminths with heteroxenous life cycles one of the hosts is often not very mobile and another acts as a vector to ensure dispersion.
The advantage of host mobility for dissemination and the resultant outcrossing of parasites is testified to by observations such as those of Bursten, Kimsey, and Owings (1997), who showed that male fleas prefer to parasitize very young squirrels (Spermophilus beecheyi) that will soon be dispersing away from their maternal nest.
Energy
Paradoxically, only prokaryotes are true autotrophs--making complex biomolecules either by capturing the energy of the sun (photosynthesis) or by harnessing it from naturally occurring mineral compounds in a process called chemosynthesis. When eukaryotes are photosynthetic, they owe their ability to synthesize their own food to their association with chloroplasts, themselves almost certainly distant descendants of once free-living prokaryotic organisms.
When one is big and not autotrophic, the most natural way to obtain energy is to swallow something smaller than oneself. When one is small and also not autotrophic, one may certainly look to devour something smaller than oneself, but a more elegant solution is to eat, without destroying it completely, something bigger.
Parasites either hijack part of the food of their host or feed on their host's nutritious tissues and fluids, which allows the parasite to decrease the allocation of its own resources to nutritional functions and may lead, for example, to a simplification or loss of the digestive system. In short, the parasite can be simple because it exploits complicated hosts.
The Sum
The question stated earlier was, What adaptive advantage did free-living organisms obtain by engaging in a parasitic lifestyle? Furthermore, between habitat, mobility, and energy, is it really possible to make such a choice?
In the beginning of a durable association, habitat, mobility, and energy may each have, in theory, represented a distinct advantage. Later one or both of the other advantages may have been added to the package, with most parasites today taking advantage of all three at the same time, courtesy of their hosts. Taking food becomes, for example, an almost immediate consequence of the association simply because the usual prey of the newly associated organism becomes less accessible or even unavailable and because the new habitat provides a readily available source of food that does not require spending energy to forage.
Parasitism may even be ineluctable, as suggested by the works of the computer scientist Tom Ray. Ray built a series of programs that compete with each other, that reproduce, and that are subject to random mutations in each generation just as in living organisms. Since there was competition in the system, the "best" programs prospered at the expense of others. In an amazing but not at all surprising way, the system quickly gave rise to true parasites--including shortened programs that borrowed missing instructions from others. Even more remarkable, the programs that remained normal (the hosts) rapidly developed new instructions protecting them from the parasitic programs, which in turn modified themselves to elude this host strategy. Thus all the ingredients for a true parasite-host association occurred, including reciprocal selective pressures. This leads one to wonder if parasitism, as much as reproduction or diversity, belongs to the definition of life. Competition for resources, whether matter, energy, space, power, or even computerized information, incites parasitism.
How Parasites?
If the conveniences of a parasitic life seem multiple, the inconveniences are also real. Nevertheless, what we sometimes see as difficulty in the parasitic lifestyle may be an anthropomorphic and naive vision of the problem. There is no doubt, however, that whatever the apparent disadvantages of a parasitic lifestyle, the cost-benefit ratio of a successful interaction is such that the advantages have won out over the disadvantages. That is, an organism becomes parasitic the same way others become marine, terrestrial, or cave dwelling--by providing, generation after generation, the possibility for natural selection to sort the best adapted from the less fit.
Continues...
Acknowledgments
Part 1 - Who in Whom: The Diversity of Durable Interactions
1.The Universe of Parasites
2.Specialization in Parasites
3. The Fragmented Nature of Parasite Populations and Communities
4. Parasite Distribution
5. Diversity in Time
Reflections
Part 2 - Genes in Durable Interactions
6. Parasite-Host Coevolution
7. Genes to Encounter
8. Genes to Avoid
9. Genes to Kill
10. Genes to Survive
11. How Do Coevolutions Evolve?
Reflections
Part 3 - Durable Interactions and Biosphere
12. Parasites against Their Conspecifics
13. Parasites against Competing Species
14. Parasites and Host Individuals
15. Parasites and Host Populations
16. Parasites and Host Ecosystems
17. Parasites and Environment
18. Parasites and Sex
19. Mutualism
20. Parasitism and Humanity
Reflections
Conclusion
References
Index
Parasitism: The Ecology and Evolution of Intimate Interactions available in Hardcover
Parasitism: The Ecology and Evolution of Intimate Interactions
by Claude Combes, Isaure de Buron, Vincent A. Connors
Claude Combes
- ISBN-10:
- 0226114457
- ISBN-13:
- 9780226114453
- Pub. Date:
- 08/15/2001
- Publisher:
- University of Chicago Press
- ISBN-10:
- 0226114457
- ISBN-13:
- 9780226114453
- Pub. Date:
- 08/15/2001
- Publisher:
- University of Chicago Press
Parasitism: The Ecology and Evolution of Intimate Interactions
by Claude Combes, Isaure de Buron, Vincent A. Connors
Claude Combes
Hardcover
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Overview
In Parasitism, Claude Combes explores the fascinating adaptations parasites have developed through their intimate interactions with their hosts. He begins with the biology of parasites—their life cycles, habitats, and different types of associations with their hosts. Next he discusses genetic interactions between hosts and parasites, and he ends with a section on the community ecology of parasites and their role in the evolution of their hosts. Throughout the book Combes enlivens his discussion with a wealth of concrete examples of host-parasite interactions.
Product Details
| ISBN-13: | 9780226114453 |
|---|---|
| Publisher: | University of Chicago Press |
| Publication date: | 08/15/2001 |
| Series: | Interspecific Interactions |
| Edition description: | 1 |
| Pages: | 552 |
| Product dimensions: | 6.00(w) x 9.00(h) x 1.80(d) |
About the Author
Claude Combes is a professor of animal biology and director of the Centre de Biologie et Écologie Tropicale et Méditerranéenne at the Université de Perpignan, France. He is the author of La Vie and coauthor of Encylopedia Reference of Parasitology.
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Parasitism: the Ecology and Evolution of Intimate Interactions ; Translated by Isaure De Buron and Vincent A. Connors ; With a New Foreword by Daniel Simberloff.
By Claude Combes
University of Chicago Press
Copyright © 2001 Claude CombesAll right reserved.
ISBN: 0226114465
1 The Universe of Parasites
Parasites affect the life and death of practically every other organism.
--Price, 1980The Notion of the Durable Interaction
Living organisms produce four types of wealth: their matter (body, organs, etc.); their metabolism (chemical reactions, enzymes, etc.); their work (movement, care of young, etc.); and the products of their work (nests, houses). These assets are coded for, either directly or indirectly but without exception, by the organism's genome and constitute, in its broadest sense, the phenotype (Dawkins 1982).
As in all cases of riches and wealth, other living organisms often lust after these assets, the most sought after being those stored in the form of the organisms' bodies: each second on earth, in prairies and forests, in soils, in lakes and rivers, and in the deepest seas and oceans, billions of living organisms are preyed on by others who covet energy in this form. These are, of course, the predator-prey systems so often described in ecology texts.
Besides the energy exchange of predator-preysystems, however, energy exchanges also occur because of parasite-host systems: just as the predator takes energy from its prey, the parasite takes energy from its host. But one major difference between predator-prey and parasite-host systems is that in the former the actors are usually visible to each other, with scenes happening before our eyes even when played out at such vastly different scales as a lion capturing a buffalo or a spider trapping a fly. In parasite-host systems one of the protagonists is, at best, difficult to observe. Although there are a few exceptions, parasites are in general actors that play in the shadows--perhaps the reason they have been ignored until so recently by mainstream ecologists.
Yet other differences between predator-prey and parasite-host systems become visible when one looks at the level of individuals and how they interact. In predator-prey systems the interaction between the predator and its prey is instantaneous or nearly so (e.g., when a cat catches a mouse, when a fox eats a hen, or when a frog snatches an insect). At most the interaction is only as long as the time of pursuit or waiting and a period of digestion. Moreover, and in virtually all cases, the predator exploits only the first of the four energetic assets of its prey: its matter. In a parasite-host system, that is, when an organism lives on or in another (a tick on a dog, a fluke in a sheep's liver, etc.), the interaction is prolonged and often broken only by the death of one of the protagonists. Because of the length of the interaction, the parasite can exploit not only the material assets of the host but also the other three types of wealth produced by the host's genome: its metabolism, work, and products. Not only is host matter exploited as an energy source, it also becomes a habitat for the parasite.
Although at the level of the biosphere the global transfer of energy from hosts to parasites is negligible when compared with that of prey to predators, the parasite-host interaction may have consequences that reach far beyond the scale of the individual host because of the prolonged and durable nature of the interaction. Parasites, more subtly but not less significantly, can affect host populations in profound and significant ways (Anderson and May 1978a, 1978b; May and Anderson 1978).
Although at first one might see little or nothing in common between a virus, a mitochondrion, a trypanosome, a fluke, a tick, and a cuckoo's chick, what unites these organisms and gives them cohesion is the durable nature of the interaction between the one called the parasite and the one called the host. This is true no matter what the systematic position of the partners, no matter the way the interaction is borne out, and no matter even that the benefits and costs of the association may be unequally shared.
Because of the different nature of these prolonged energetically based associations, I have previously proposed the term "durable interactions" (Combes 1995) to describe all such associations between genomes that, either directly or through the intermediary of the phenotype, last for extended periods.
Figure 1.1 symbolizes the expression of the parasite's genome within the context of the host's phenotype and the expression of the host's genome within the context of the parasite's phenotype. Significantly, and because of the prolonged interaction of the protagonists, we can view the parasite-host association as a system --meaning the association takes on novel characteristics of its own that are not just the simple sum of its component parts. In short, these new characteristics are due to the interaction of the crossed phenotypes of the parasite and host, each of which may be interfering with the other and each of which is being expressed under the influence of the other's (Combes 2000).
Consequences of the Durable Interaction
The durable interaction has four major consequences, each linked to the fact that there are, side by side, two genomes. This fact makes it, in a sense, a superorganism possessing a "supergenome."
First Consequence: The Parasite's Genome Is Expressed in the Context of the Host's Phenotype
To communicate with each other the different parts of a living organism, as well as the different individuals of the same species, use signals (molecules coded directly or indirectly by genes) that are recognized by receptors (other molecules coded for by other genes). All organisms, from the simplest to the most complex in organization and function, use the same fundamental constitutive molecules, metabolic processes, information storage processes, and chemical systems in this communication, and an exchange of signals is made possible between the parasite and the host because of this remarkable unity of life.
In a parasite-host association, the signals produced by the genome of one of the partners may act on the phenotype of the other, thus crossing the species barrier and inducing morphological, anatomical, physiological, or behavioral changes in the recipient. The expression and extension of the parasite's genome into its host's in this way gave Dawkins (1982) one of the most striking illustrations of the concept of the extended phenotype, which is a phenotype envisioned to occur beyond the physical limits of the organism to which the genes belong. Among other examples of the extended phenotype, Dawkins cites galls--growths on plants within which certain insect larvae develop. These structures are the result of selection, in the insect genome, of genes able to manipulate the growth of the plant host tissues in their surroundings.
The possibility that a parasite's genome may influence the host phenotype, as in the case of galls, is not necessarily restricted to the action of signaling molecules, however, and in certain "sensitive organs," like those within the nervous system of animals, the parasite's physical presence alone may modify the physiology or behavior of the host.
The influences of a parasite's genes on host physiology and behavior in these ways are sometimes both profound and obvious, and they may favor either host-to-host transmission, the exploitation of the host, or escape from the host's immune system. In some cases, however, the para-site's influence is not very visible, and as a result its consequences may be underestimated. Given that all organisms are parasitized at some time during their life spans, one may wonder if in fact there is even one durable interaction that does not imply a manipulation of hosts, however subtle, by parasites. (Is there even one free-living animal that owes its physiology and behaviors solely to its own genes?)
Second Consequence: The Host Genome Is Expressed within the Context of the Parasite's Phenotype
As soon as a parasite-host system forms and lasts, there is a high probability that some of the genes (or gene combinations) making up the "supergenome" will be duplicated. This does not mean that such genes have an identical nucleotide sequence but rather means that they have similar or overlapping functions. When such double-usage genes exist there is a tendency for one of the two genes to stop being expressed over the course of evolution. This may happen either because mutations abrogate the function of one member of the pair, with the system surviving because of the second gene, or more simply because of the cessation of expression of one of the genes in one of the partners. Double-usage genes lost in this way may become pseudogenes (sequences not translated into proteins), or they may ultimately be deleted.
In general parasites and not hosts lose genes, which explains the observed regression of functions otherwise ensured by the host genome in many parasites. That is, the direct consequence of the extension of the host's phenotype into the parasite is the exploitation of the host genome. This is attested to by the fact that all parasite descriptions emphasize morphological simplifications and that parasites save on numerous morphological and functional accessories, such as organs of locomotion, digestive and enzymatic systems, and sense organs because their hosts can take care of the corresponding functions of obtaining food, digestion, and avoiding enemies. An example of organs being lost through this process is the disappearance of the digestive tract in cestodes, while an example of the resulting functional dependence of parasites on their hosts is the lack of the enzymes necessary for purine metabolism in all known parasitic protozoa and some parasitic metazoa, such as the schistosomes. In all these organisms purine metabolism must be ensured by the hosts' enzymes.
What happened to the genes that coded for digestive systems or the enzymes of purine metabolism in the ancient ancestors of current parasites is still an unanswered question. Nevertheless, when such genes are truly lost by the parasite, the survival of the species depends, from then on, strictly on the host. The parasite is "linked" to the host genome and can no longer survive without that host.
Third Consequence: Innovative Genes
Although parasites often depend on host genes for important functions, nothing prevents the host from exploiting the parasite's genome if similar or better genes exist in the parasites. In this case the loss of a double-usage gene may happen in the host, which then becomes as dependent for survival on the presence of the parasite as the parasite is on the host. In this case the parasite is referred to as a mutualist, and the association constitutes mutualism.
Thus parasitism and mutualism can be differentiated not only by energetic constraints but also by the fate of double-usage genes: if gene expression stops only on one side, there is parasitism; if different genes on each side stop being expressed, there is mutualism. Cheng (1991) expressed this difference nicely by emphasizing a unilateral physiological dependence in the case of parasitism and a bilateral dependence in mutualism. This distinction was further clarified by Smith (1992): "In parasitism, hosts are exploited by parasites; in symbiosis, hosts always exploit their symbionts, although simultaneous exploitation of host by symbiont may occur in certain associations."
An advantageous situation for the host occurs when the parasite brings not simply a "better" gene but a "new" gene or genes that code for a novel function, such as a new synthetic or metabolic pathway. In acquiring such "innovative" parasite genes the host makes "an evolutionary leap" in the sense that the new function is gained virtually at once and without patient selection and adjustment. Viewed in this way, parasitism is certainly not a marginal process in biological evolution (see Szathmary and Maynard Smith 1995). At least in the first stages of life, and as evidenced by the mi-tochondrion--the central piece of eukaryotic cell oxidative metabolism and itself an "ancient bacterium"--the acquisition of innovative genes via such a durable interaction likely has played an essential role in the process resulting in the evolution of the more complex life forms themselves.
Obviously, innovative genes coding for novel functions may also have appeared via mutation in one of the partner species after the parasite-host relationship was initiated. In this case the gene may be exploited by both species.
Regardless of the source of the exploited genes, however, selection will not occur under the same conditions in parasitic and mutualistic associations (fig. 1.2).
In a parasitic association the system receives resources from the outside, and both partners are in competition for these resources. This competition puts very strong selective pressures on both the parasite and host, with each constituting separate units of selection. These selective pressures can be far stronger than those pressures between the association and the other units of selection affecting it in the ecosystem.
In a mutualistic association, on the other hand, the selective pressures between the partners becomes less important (although not nonexistent), and the association itself forms the major unit of selection (see Maynard Smith 1989c). In this case the most notable pressure results from the unit's interacting with other entities of selection in the ecosystem.
Fourth Consequence: Gene Exchange
The prolonged association between two organisms with different genomes provides an ideal mechanism for the exchange of genes between associated members. Although we know they exist, however, little is known about such transfers in nature. At least in durable interactions of very ancient origin (such as the ones linking mitochondria and chloroplasts to eukaryotic cells), some exchanges of genes have occurred during evolution. It is thought that such exchanges may involve mobile DNA elements, viruses, bacteria such as Wolbachia, or still other as yet unidentified mechanisms, and it is suspected that these exchanges may have played a major role in numerous evolutionary processes, one of the major ones being the evolution of the mechanisms by which parasites escape host immune systems.
The Frontiers of the Durable Interaction
Although some workers spend a good bit of time debating whether specific organisms should or should not be classified as parasites, the more encompassing concept of a durable interaction removes all ambiguity and allows us to bring together, alongside parasitism and mutualism, associations such as inquilism (obtaining habitat without taking food), phoresy (obtaining transportation for a set period), and parasitoidism (a durable interaction terminated by the assassination of the host). This concept also allows one to exclude without hesitation organisms whose interaction exists only for the short time of a meal. It is not reasonable to classify as parasitic organisms such as mosquitoes or tsetse flies just because, like parasites, they consume a fraction of an organism without killing it. If we accept mosquitoes as parasites, then we should call the cow that eats grass without killing it, the sparrow that eats cherries without swallowing the entire cherry tree, and all other herbivores, parasites as well. Mosquitoes, tsetse flies, and other insects find their place in parasitology textbooks as vectors of parasites, not as parasites themselves, and it is only when some such species succumbs to the attraction of a habitat provided by another organism, or to taking food exclusively from the same host, or to obtaining a convenient mode of transportation that it would acquire the rights to the parasitic world. Ticks, for example, spend enough time on their hosts so that a typical durable interaction is established--they make molecules that affect the host phenotype by rendering the blood meal both easier and longer lasting: "Tick saliva contains a cocktail of pharmacologically active compounds (e.g. immuno-suppressants, analgesics, anticoagulants, antiplatelet aggregatory compounds)" (Bowman, Dillwith, and Sauer 1996).
As always in biology, however, there are marginal situations that are difficult to classify. Although it is clear that a bee that gathers pollen from flower to flower has nothing to do with parasitism, it is not unreasonable to consider as parasitic the caterpillar of a butterfly who spends its entire larval life on the same nourishing plant.
We should perhaps add another comment about parasitoids, which, after a phase of "classical parasitism" when genomes interact, then kill their host. The best known are insect parasitoids of other insects, but we must also include in this group some viruses (bacteriophages) that, after an initial interaction period, kill their bacterial hosts. Although the end of the association resembles that of predator and prey, the relationship between parasitoids and their victims must be classified among durable interactions because the period of interaction shows numerous facets of the extended phenotype, most notably the forced insidious entry of the parasite genome into the host phenotype.
Last, what fate should we reserve for the word "symbiosis," which literally signifies "life together" and therefore notably applies to the concept of a durable interaction? The word was created at the end of the nineteenth century by the German botanist Heinrich Anton de Bary to designate all associations of two species living together, including parasitism, mutualism, inquilism, and so forth. This is the sense that is always used by certain authors, such as Cheng (1970) and other American workers. Often, however, the appellation is more restrictive and applied only to associations said to be "with reciprocal benefits," here called mutualism. Because of this dichotomous usage, I will make limited use of the term symbiosis, which is also the choice made by Bronstein (1994a): "To reduce semantic confusion, I will use the term mutualism exclusively."
The associations that lead to durable interactions are infinitely numerous in the living world. In fact no organism exists, and none may ever have existed (except at the very beginning of life), that does not establish or is not subjected to a durable interaction with at least one other organism. All living organisms are involved in parasitism, either as hosts or as parasites themselves (Price 1980), and these interactions continue to play an essential and major role in biological evolution and the functioning of the biosphere as we know it.
Why Parasites?
In the "beginning," the ancestors of organisms currently living in association with each other were free-living and not connected. Because in evolution changes most often relate to cost-benefit relationships, we must therefore consider two things: why once free-living organisms found more advantages than disadvantages in adopting the parasitic mode of life, and why free-living organisms that became hosts either were unable to eliminate the parasites or found advantage in such a situation themselves.
To understand why a free-living organism acquires a parasitic lifestyle via selection, one can first consider two free-living species that share the same environment at a given time, then wonder about the advantage that some individuals of one of the two species (call it A) have in taking the second species (B) as their living habitat. It is not enough to say that individuals of species B constitute environments; one must also demonstrate that individuals of species A that possess genes inducing the choice of B as a living milieu benefit from an increased fitness compared with those that remain free-living.
There are three main advantages that individuals of B can give to individuals of A (fig. 1.3): habitat, motility, and energy.
Habitat
As long as a species is free-living its members are subject to fluctuations in the environment and to the aggression of other free-living organisms. If certain individuals of this species take individuals of another species for their habitat, we may speculate that they might immediately benefit in two ways: they would occupy a more stable milieu than the exterior environment, and they would be sheltered from the predators and competitors they might otherwise face while free-living.
One cannot contest the fact that a living environment is stable. Living organisms possess mechanisms to ensure homeostasis, or the consistency of a number of physicochemical parameters. Blood composition, for example, is maintained with amazingly little variation, and in many organisms, such as birds or mammals, temperature remains constant. Therefore it is more "comfortable" to live inside a polar bear or desert rat than in the environments where the polar bear and rat live. This may be one reason most parasites have shortened their stay in the external environment as much as possible and also why some have rid themselves of this phase entirely.
That a living environment provides protection from predators, though, deserves more discussion. First of all, this is not necessarily true so long as individuals of A remain outside individuals of B--if they are ectoparasites. It is well known that cleaner fish pick off and eat the ectoparasites of other fish and that cleaner birds peck ectoparasites from the fur of mammals. Whittington (1996) showed that some fish ectoparasites even select for camouflage (i.e., for a transparent body and colored spots) that provides some protection from cleaner fish, and Euzet and Combes (1998) have suggested that the pressures exerted by such predation may in some cases have induced the passage from ecto- to meso- or even endoparasitism in monogeneans. Relative to these worms' habitat these authors write: "If, in a population of a given species, there is a polymorphism of habitat preference, some individuals may remain on the skin while others tend to penetrate inside the body. A process of natural selection can then give rise either to a gradual change in the habitat of the whole population or to two different populations (which may later evolve into separate species)."
In short, then, protection from predators is provided only if individuals of species A find refuge inside individuals of species B. Further, and in an amazing turn but with very few exceptions, parasites are protected from predation in another way: they do not tend to eat each other. Parasites live in a miraculously pacifist world where there are no prey and no predators and where, at the most, bacteria may be absorbed by parasites much bigger than they are. In other words, all parasites are at the same trophic level. As soon as an organism lives on the gill of a fish, in the bladder of a frog, the duodenum of a mammal, or in the tissues of a seed, no other organism will pursue or devour it. In evolutionary terms, it is free to leave aside the apparatus, including sensorial and locomotor organs, that allowed its free-living ancestors to detect and flee enemies. To illustrate the protection given to parasites by this mode of existence, Domitien Debouzie (personal communication) gives an estimation of the mortality rate in the chestnut weevil: as long as these parasitic insects are inside the chestnut the mortality rate is low, but as soon as they reach the ground to complete their development they fall victim to all sorts of predators and mortality increases dramatically (fig. 1.4).
Overall, then there are two clear advantages to having a living habitat: the stability of the environment and protection against predators.
There are, however, two objections to this assessment. First, although the living environment is stable it is also mortal; second, even though the parasite no longer has specific predators, it nevertheless inherits the predators of the host (all the parasites of a mouse should logically be digested when eaten by a cat). There are two responses to these objections:
Relative to the first objection, to live in a mortal habitat may not be as much of a disadvantage as it at first seems. Parasites themselves are mortal, and therefore establishing a durable interaction would not yield an infinite interaction for the individual. The problem is avoided by parasites' having life cycles that allow their descendants to infect the descendants of their hosts. All living organisms disperse their descendants (seeds get carried away by the wind, birds leave their nests, etc.), and for parasites dispersion out of the founding host is precisely the way to escape the dilemma of host death.
As for the second objection, it is true that virtually all host species (except top consumers) have predators. In each case, however, mechanisms have been selected so that predation does not usually imperil the host species, and parasites are in danger only if the host species is itself in peril. In fact there is even another possibility--that the parasite may take advantage of its host's being eaten by a predator (a mouse eaten by a cat, for example) by surviving in the predator. The parasite in this case wins twice, since it can successively exploit both the prey and the predator (the mouse and then the cat). Evolutionarily, it is then in the interest of the parasite that the cat eats the mouse. Certain parasites have used this as a means to navigate up the food chain and reproduce only in the top consumer, that is, in the host that has the fewest or no predators.
Still another argument in favor of the "security" advantage obtained by occupying a host as a habitat is that in nature any shelter is rapidly exploited by living organisms. For example, rocky coasts and coral reefs harbor a multitude of fixed or not very mobile animals such as sponges, corals, ascidians, and mollusks. These organisms increase the "porosity" of the physical environment, and these new niches are themselves colonized by an impressive list of tenants such as protozoans, planarians, copepods, amphipods, and annelids. Relative to cool ocean waters, the hosts of parasites are luxurious shelters that bring not just safety but also room and board.
Mobility
In many cases (almost all when the habitat is an animal) a living habitat is mobile. Based on this fact we can then ask, Could mobility itself have been the initial advantage obtained by acquiring a living environment?
The dispersion of propagules (a general term designating all forms, such as eggs and larvae, that serve in dissemination) is one of the major parameters of success of living organisms. If in a population certain individuals have a greater capacity to disperse than others, then their or their offspring's chances of survival may be increased, either by an increase in the probability of finding a suitable habitat, by the conquering of new areas, or by the reduction of intraspecific competition. Mobility in this sense is very important for a species, and the less mobile adults are, the more likely it is that some elaborate means of dispersion for its propagules has been selected. For example, plants or fixed aquatic animals ensure the dispersion of their gametes or planktonic larvae by developing various appendages and lift devices, such as bristles, blades, or umbrellas, that allow them to be carried away by the wind or to drift with the currents. The classical examples of such dispersal mechanisms are of course plants, which ensure the dispersion of their pollen by insect pollinators and their seeds by vertebrates (i.e., by hooking on to the fur or passing through the digestive system). When an organism is not very mobile it can improve the dispersion of its propagules by making them more mobile than itself.
Associating oneself durably to a mobile organism, as opposed to associating one's pollen or seeds, amounts to selecting an even more efficient mechanism of dispersion: instead of hooking propagules on to a vehicle, their producer (the adult organism) attaches itself to the vehicle and thus disperses its young throughout the host's travels. All parasites in the digestive tract of a mammal have their eggs or larvae dispersed more or less constantly in this manner as the living vehicle travels: all bird parasites fly with their hosts, and all fish parasites swim with theirs. This could explain why entire groups of parasites are restricted to mobile animal hosts and why they tend to disdain immobile plant hosts. When parasites do exploit immobile hosts such as plants or sedentary animals, their dispersion is ensured by different processes according to the group. For example, in insects parasitic of other insects and crustaceans from the monstrillid group, only the larvae are parasitic: in these cases dispersion is ensured by mobile adults, whereas in helminths with heteroxenous life cycles one of the hosts is often not very mobile and another acts as a vector to ensure dispersion.
The advantage of host mobility for dissemination and the resultant outcrossing of parasites is testified to by observations such as those of Bursten, Kimsey, and Owings (1997), who showed that male fleas prefer to parasitize very young squirrels (Spermophilus beecheyi) that will soon be dispersing away from their maternal nest.
Energy
Paradoxically, only prokaryotes are true autotrophs--making complex biomolecules either by capturing the energy of the sun (photosynthesis) or by harnessing it from naturally occurring mineral compounds in a process called chemosynthesis. When eukaryotes are photosynthetic, they owe their ability to synthesize their own food to their association with chloroplasts, themselves almost certainly distant descendants of once free-living prokaryotic organisms.
When one is big and not autotrophic, the most natural way to obtain energy is to swallow something smaller than oneself. When one is small and also not autotrophic, one may certainly look to devour something smaller than oneself, but a more elegant solution is to eat, without destroying it completely, something bigger.
Parasites either hijack part of the food of their host or feed on their host's nutritious tissues and fluids, which allows the parasite to decrease the allocation of its own resources to nutritional functions and may lead, for example, to a simplification or loss of the digestive system. In short, the parasite can be simple because it exploits complicated hosts.
The Sum
The question stated earlier was, What adaptive advantage did free-living organisms obtain by engaging in a parasitic lifestyle? Furthermore, between habitat, mobility, and energy, is it really possible to make such a choice?
In the beginning of a durable association, habitat, mobility, and energy may each have, in theory, represented a distinct advantage. Later one or both of the other advantages may have been added to the package, with most parasites today taking advantage of all three at the same time, courtesy of their hosts. Taking food becomes, for example, an almost immediate consequence of the association simply because the usual prey of the newly associated organism becomes less accessible or even unavailable and because the new habitat provides a readily available source of food that does not require spending energy to forage.
Parasitism may even be ineluctable, as suggested by the works of the computer scientist Tom Ray. Ray built a series of programs that compete with each other, that reproduce, and that are subject to random mutations in each generation just as in living organisms. Since there was competition in the system, the "best" programs prospered at the expense of others. In an amazing but not at all surprising way, the system quickly gave rise to true parasites--including shortened programs that borrowed missing instructions from others. Even more remarkable, the programs that remained normal (the hosts) rapidly developed new instructions protecting them from the parasitic programs, which in turn modified themselves to elude this host strategy. Thus all the ingredients for a true parasite-host association occurred, including reciprocal selective pressures. This leads one to wonder if parasitism, as much as reproduction or diversity, belongs to the definition of life. Competition for resources, whether matter, energy, space, power, or even computerized information, incites parasitism.
How Parasites?
If the conveniences of a parasitic life seem multiple, the inconveniences are also real. Nevertheless, what we sometimes see as difficulty in the parasitic lifestyle may be an anthropomorphic and naive vision of the problem. There is no doubt, however, that whatever the apparent disadvantages of a parasitic lifestyle, the cost-benefit ratio of a successful interaction is such that the advantages have won out over the disadvantages. That is, an organism becomes parasitic the same way others become marine, terrestrial, or cave dwelling--by providing, generation after generation, the possibility for natural selection to sort the best adapted from the less fit.
Continues...
Excerpted from Parasitism: the Ecology and Evolution of Intimate Interactions ; Translated by Isaure De Buron and Vincent A. Connors ; With a New Foreword by Daniel Simberloff. by Claude Combes Copyright © 2001 by Claude Combes. Excerpted by permission.
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Table of Contents
Foreword, Daniel SimberloffAcknowledgments
Part 1 - Who in Whom: The Diversity of Durable Interactions
1.The Universe of Parasites
2.Specialization in Parasites
3. The Fragmented Nature of Parasite Populations and Communities
4. Parasite Distribution
5. Diversity in Time
Reflections
Part 2 - Genes in Durable Interactions
6. Parasite-Host Coevolution
7. Genes to Encounter
8. Genes to Avoid
9. Genes to Kill
10. Genes to Survive
11. How Do Coevolutions Evolve?
Reflections
Part 3 - Durable Interactions and Biosphere
12. Parasites against Their Conspecifics
13. Parasites against Competing Species
14. Parasites and Host Individuals
15. Parasites and Host Populations
16. Parasites and Host Ecosystems
17. Parasites and Environment
18. Parasites and Sex
19. Mutualism
20. Parasitism and Humanity
Reflections
Conclusion
References
Index
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