Parasite life cycles: evolution and consequences

Where and why do complex life cycles come from?

Parasite life cycles: they're cool, and seemingly improbable, natural history ... many parasites (as we will see in a bit, after the inevitable digression) have what seem to be ridiculously baroque ways of producing the next generation of offspring, involving transfers between multiple hosts. Complex life cycles involve shifts between hosts, but can also involve a succession of physiologically or morphologically different stages within a single host (e.g. using different tissues). There is a close parallel between complex life cycles in parasites and metamorphosis, e.g. in amphibians or lepidoptera. In each case, organisms undergo major physiological/morphological rearrangement as part of their life cycle.

Definitions and examples

Many parasites (especially "classical" metazoan parasites) go through multiple species in their lifetimes. Life cycle complexity is the use of multiple host species in serial (all host species must be used in sequence to complete a single parasite life cycle), while specificity is the use of multiple host species in parallel (individual parasites can pick one of several hosts to complete a particular life cycle stage).

Parasites that use only a single host species in their life are called monoxenic;
those with multiple hosts are called heteroxenic.
Definitive hosts are those in which sexual reproduction takes place (there is some reason to argue that definitive hosts are special, since sexual reproduction can only occur once in the life cycle, but a parasite could shift its definitive stage from one host to another);
intermediate hosts are all the others.
Paratenic hosts are hosts that are used only for transport; no life cycle stages are completed within the host.
Vectors are hosts that facilitate transport from one host to another, although what is a "vector" and what is not depends on your focus. To a mosquito, a human might serve as a vector for malaria to get from one mosquito to another!

The malaria parasite provides an example of a complex life cycle with two hosts and multiple life stages within each host. Combes (p. 590) provides a good description and picture of the sequence from sporozoites, hepatocytes (human liver), merozoites (human red blood cells), gametocytes (mosquito guts), ookinetes (travel to mosquito salivary glands), back to sporozoites. Sexual reproduction takes place in the mosquito, which is therefore the definitive host. Asexual reproduction occurs at several points around the cycle, within both humans and mosquitos.

Other examples of transmission include:

Direct transmission: most viruses, bacteria; many plant fungi; many intestinal nematodes
Two hosts/one intermediate host: e.g. Schistosoma mansoni (trematode), causes human schistosomiasis: human (or rodents, cattle, baboons, dogs) to snail. By some definitions, this could also include classical vector-borne parasites: malaria (protozoan), filarial worms
multiple intermediate hosts: e.g. Paragonimus (another trematode): mammals to snails to crayfish. Alaria spp.: wild carnivores, snails, tadpoles, mice/rats/snakes (paratenic) Combes (p. 38) mentions Halipegus ovocaudatus, a trematode which has a four-host cycle from amphibian to mollusk to crustacean to insect.

Q: is there a limitation on the number of hosts in a life cycle? Why doesn't it keep increasing? Is this obvious, or not?

Transition methods:

passive movement followed by uptake of eggs/larvae by feeding, inhalation, etc.
active locomotion (by eggs/larvae/parent), followed by penetration of the host and possible migration within the host
next host feeds on the previous host (predation or incidental: behaviorally mediated or not). It makes sense that trophic transmission is common, since trophic interactions are probably the most common way that individuals of different species come into close physical contact with each other in the wild.

Why??

Complex life cycles seem hard to justify on the face of it. Why would an organism employ such a dicey strategy? This question has led to creationist arguments, but for now let's stick to the evolutionary ones ... We come up with the same classes of answers that always come up in response to evolutionary "why" questions: adaptationist and drift/neutral arguments.

neutral arguments say that organisms found themselves switching by hosts essentially by accident (e.g. when the host they were in was swallowed by an individual of another species). Once a lineage of parasites was stuck in this cycle, they could lose the ability to have a shorter cycle via mutation and drift.
there are several kinds of adaptationist arguments:
- organisms that find themselves in other hosts (as in the example above) could experience tradeoffs that encouraged the evolution of obligately complex life cycles
- adding another host could actually be advantageous, providing transport between hosts or allowing parasites to limit their virulence within different life stages;
- Smith Trail has suggested "host suicide" as a host adaptation (committing suicide to lessen the risks of parasitism for one's kin) that could then be perverted and turned to advantage by parasites.

How?

Testing these hypotheses also brings us back to a familiar refrain. There are essentially four ways of testing hypotheses on parasite evolution:

Broad comparative: use a large database to try to look at ecological and evolutionary correlates of the trait in question (in this case, life cycle complexity) to see whether the patterns that emerge either support available hypotheses or suggest new ones;
Narrow comparative: test a closely related set of species in similar environments that show some interesting difference in parasitism, and try to infer the reasons for their differences;
Experimental: manipulate organisms in the field or in the laboratory;
Phylogenetic: test the relationship between the phylogeny of some group and the pattern of changes in parasitism.

For this particular case, we have examples of two of the above:

Combes discusses two examples (pp. 159-163) of "narrow" comparative approaches to life cycle complexity. I briefly discussed his example of Bothriocephalus, where there are two closely related parasites (gregarius and barbatus) in similar ecological situations (on turbot and brill in similar environments) that behave differently (barbatus has a 2-host cycle, gregarius has a 3-host cycle including gobies as a paratenic host). This supports one of the adaptive arguments above.
Combes (p. 165) discusses the evolution of shorter life cycles in Alloglossidium; the following phylogeny suggests that a 3-host cycle is ancestral. (Note that drawing the same phylogeny this way would be equivalent.) Of course, this doesn't tell us why it happens, just that it happens. Combes waves his hands a bit about possible reasons for the shortening in this and other systems. Q: how could you go about testing/establishing hypotheses for why this had happened?

Background from Morand et al. 1995