PARASITES AND PARASITISM

Parasites are often described as occupying the third great environment, -aquatic, -terrestrial -parasitic, the body of another organism. So perhaps the first question about parasitism is how successful is it as a way of life? To some extent this depends on how you define parasitism, but all the major animal groups, except possibly the vertebrates (although some deep sea fish have parasitic males, and lampreys may be considered parasitic) have parasitic members, there are even parasitic cnidarians. It has been estimated that more than 50% of all known species are parasitic at some stage of their life cycle. Just as important as how many species of parasite are there, is how many plants and animals are themselves parasitized as individuals and the answer must approach 100%.

Parasitism is a form of animal association, but can we define it more rigorously, how does our concept of parasitism differ from other associations, say prey/predator interactions.

Start with some definitions:

Symbiosis means literally living together. Coined in 1876 by DeBary, to describe two species of organisms that lived together, with no implication regarding the length or outcome of the association. So symbiosis as originally conceived covered a range of intimate interactions between organisms-the most common ones being mutualism, commensalism and parasitism. So symbiosis was an overarching term, there has been a move to restrict symbiosis to a particular sort of association, where both partners are seen to benefit, but most modern literature has now returned to using symbiosis as an umbrella term for organisms that live together. Using this concept then:

Mutualism, highly interdependent association, to the extent that the two associates cannot survive without one another. Example flagellate protozoa/termites or ruminants and rumen protozoa. In each case the protozoa have the enzymes that convert cellulose to glucose, the host provides a low redox potential environment. Two way benefit, no harm = Symbiosis of some authors.

Commensalism involves one way benefit, but as in the case of mutalism no harm is exerted in either direction. Clown Fish and sea anemone. The sea anemone provides protection against predators, the clown fish is highly evolved to survive the cnidarian nematocysts. Its external mucus layer is much thicker than that of related species and the chemical composition of clown fish mucus is different. Clown fish mucus consists largely of neutral polysaccharides and lacks the acidic sialic acid groups which trigger nematocyst discharge (although this makes the fish more susceptible to fungal infection). Commensalism usually involves a feeding relationship and generally does not involve metabolic independence. E.g. polychaete and hermit crabs.

Parasitism. Classical definition - intimate relationship between two organisms in which one (the parasite) lives on, off or at the expense of the other (host). This implies that one of the partners benefits, the other is harmed. One problem with this simple definition is that harm is a very difficult thing to quantify, the same problem applies to the definition of mutualism and commensalism. In animal associations it is often assumed that one organism is benefiting or not without any real evidence.

Rats, infected with the intermediate stages of a tapeworm called Spirometra grow larger than uninfected rats. The tapeworm larva produces an analogue of vertebrate growth hormone-is the growth boost harming the host or is it good for the host? Similarly many molluscs, when infected with the intermediate stages of Digenetic flukes develop thicker, heavier shells, which could be deemed an advantage. On closer investigation some of the classic examples of mutualism seem more like an armed standoff than mutual benefit. Given the right conditions many organisms which harbour symbiotic algae - like for example green hydra will digest the algae and carry on quite happily. Many trees have associated with their roots fungal mycorrhiza. The fungi get organic nutrients from the plant via the phloem, and in nutrient poor soil the trees seem to benefit by increased nutrient uptake, particularly phosphate by the fungus. But if soil nutrient levels are good it appears much more like a parasitic invasion by the fungus with the tree attempting to wall off infected cells. Depending on external conditions, the association switches between mutualism and parasitism.

So the simple definition of parasitism where one of the partners benefits and the other is harmed is not really adequate and also it does not really differentiate between a parasite and a predator or a parasite and a micro-predator. e.g. mosquito.

In order to develop the concept of the host-parasite relationship different people have added to the classical definition that 'the parasite is metabolically or physiologically dependent on the host'. Or that there is 'genetic complementation between the parasite and its host'. That is that the parasite has lost the genetic ability to make certain vital metabolic intermediates and has to rely on the hosts genome for this or it may have to rely on the host genome to provide vital developmental stimuli. In extreme cases part of the parasites genome may have been lost and become integrated into that of the host.

A more recent definition or perhaps description of parasitism is that given by Crofton.

Ecological relationship between two different organisms, one designated the parasite, the other the host.
The parasite is physiologically or metabolically dependent upon its host.
Heavily infected hosts will be killed by their parasites.
The reproductive potential of the parasite exceeds that of their hosts.
There is an overdispersed frequency distribution of parasites within the host population. That is, the parasite population is not evenly distributed amongst the host population nor is it randomly distributed but clumped, so some hosts have a lot of parasites, most have very few.

Let's look at some of these points in more detail.

Parasitism is, like most other animal associations defined in terms of two different species, who form a regular association, although this seems sensible, and it does exclude consideration of the mammalian foetus as being parasitic upon its mother, there are some very interesting immunological parallels between the mechanisms the foetus uses to avoid being rejected by the immune response of its mother and the ways in which the parasites of mammals seek to avoid their hosts immune response. Also in a number of deep-sea fish, the males are tiny and become parasitic on the females, nothing is known about the physiological basis of this.

Sometimes people add that the parasite is the smaller and the host the larger of the two organisms. This is generally true, although in some fish parasites, the plerocercoid stage of the tapeworm that lives in the body cavity of the fish can be heavier than the host. Size to a certain extent distinguishes parasites from predators, as predators are usually, but not always, larger than their prey. Any one parasite usually only infect a few different species of host during its life cycle (their are a few 4 host life cycles, no 5 host life cycles), this is in contrast to predators which usually eat a range of different prey species.
Physiological or metabolic dependence of the parasite on its host is central to most attempts to define parasitism. It does not of course distinguish parasitism from mutualism.
Heavily infected hosts are killed, this introduces the concept of the cost to the host population of parasitism.
Parasites have a higher reproductive potential than their hosts, this distinguishes parasites from predators. Predators have a lower reproductive potential than their prey, and are less numerous, whilst parasites have a higher reproductive potential and are more numerous.
Overdispersed or clumped frequency distribution is important in that it is something that can be quantified and we shall return to it when we look at parasite populations. This frequency distribution helps to exclude micro-predators from our definition.

No definition of parasitism is ever going to be completely satisfactory if we try hard enough we can always find an exception and there are always going to be grey areas where parasitism, mutualism and commensalism overlap.

But it is a mistake to think of animal associations forming a linear sequence with commensalism leading to parasitism leading to mutualism. Each association is independent with different endpoints. People have argued that for parasitism to evolve the two species must have been living in close association, possibly in a prey-predator relationship. In the early stages of association the host and parasite are not going to be well adapted to each other so you might expect recently evolved parasites to be virulent and cause a lot of host damage, but gradually the host would evolve to be more tolerant of the parasite and so you might expect a series.

Acute --> Chronic --> Mutualism?

Equally you can argue that a parasite that elicits a very strong host response is not likely to get established in the first place and it is much more likely in the early stages of the evolution of a parasitic association that the parasite would cause little if any host response and that virulence is something that evolved later. It is just as likely that a mutualistic association will evolve into parasitism as a commensal relationship and although some parasitic relationships may evolve into mutualistic ones, they may equally well not.

Once a parasitic association has evolved, say a nematode in a fish, the parasite could radiate within the body of the host to occupy new niches, so you could get new species of parasite evolving from the original progenitor. The concept of the parasite niche is one that has undergone quite a lot of revision lately. The original concept was that the host could be divided up into a large number of separate niches, each one being a separate entity that might or might not be occupied by a parasite. In the same way in free-living animals you might describe a niche for a large carnivore which might be filled with a bear in one ecosystem or a tiger in another. They occupy a particular niche, but even if they are not there, the niche still exists.

A more compelling concept is that the parasite creates its own niche. It is the parasite that determines the niche not the host. A particular parasite may occupy a specific site and utilize certain host resources and this defines its niche. So a niche is a description of the parasites requirements, not of host attributes. One thing parasite ecologists are agreed on is that current parasites have not exhausted the number of possible host niches. So there is still plenty of room left for new parasite species.

Another way of course that parasites can be acquired is by host capture, when the parasite transfers from one host to another one in the same ecosystem. Since parasites can effect the reproductive success of their hosts, either by removing resources or by ultimately killing the host, parasites can exert an influence on host evolution. We will talk about the influence of hosts on parasite evolution in a later lecture. So parasites can influence host evolution.

Macroevolution: Animals show a high degree of protein polymorphism. That is, if you take virtually any protein you find that there are a large number of different isoforms. These isoforms differ by perhaps just a few amino acid residues, different individuals have different isoforms, but the isoforms seem to be biologically identical. Where is the driving force coming from to maintain this high degree of protein heterogeneity? One suggestion is that most of this polymorphism represents neutral mutations. The proteins biological function is not altered by these mutations so they are neither selected for nor selected against. An alternative explanation is that protein polymorphism is a host response to parasitism. If every individual had identical proteins, a parasite could evolve a surface coat that was identical to one of these proteins and so hosts would not recognize the parasite as foreign and would not mount any defensive immune attack. Host polymorphism prevents the parasite using molecular mimicry. The main process which maintains polymorphism in animals is of course sexual reproduction, so parasites may be one of the driving influences behind the evolution of sex.

Micro-evolution: Parasites may also have a role in sexual selection. In many bird species the males have brightly coloured plumage and females select males with the biggest and brightest feathers. To grow this plumage is a considerable metabolic investment for males and may also make them more vulnerable to predation. One explanation is that it is a red queen effect, females prefer males with big tails so males evolve bigger and bigger tails. Females mate with males with big tails so their own sons will have big tails and so be more successful in their turn.

A second explanation is that females use the condition of the male plumage to inform her of the physiological fitness of the male. Only healthy birds can grow a big tail, and female birds because they invest so much in reproduction want to make sure that they mate with only the fittest males. There is some experimental evidence that heavily parasitized individuals cannot grow the requisite plumage, so females can use the state of the male plumage to ensure that they mate with parasite free-males. A similar argument can be put forward for birds that have an energetic courting display where the males jump up and down (lek system).

There is also some evidence in mice that females discriminate against parasitized males, and that the cue may be smell.

So parasites then may influence the evolution of their hosts.

Useful definitions:

Ectoparasite-: lives on surface.
Endoparasite-: live inside host.
Mesoparasite-: penetrates external openings - buccal cavity, cloaca, external ear.
Definitive host-: where parasite reaches sexual maturity.
Intermediate host-: required by parasite to complete its life cycle. Usually undergoes morphological or physiological change in it.
Paratenic host-: optional transport host - no detectable morphological change in parasite
Vector-: host that plays an active role in transmission, can be a definitive or an intermediate host.