Combes begins with arms races and the idea of "encounter" and "compatibility" filters that come in between parasites and successful exploitation of a host. The key difference between predator-prey and parasite-host relationships is that with parasitism two genomes survive; this allows for information transfer and phenotypes that are not just extended but interwoven.
With a sequences of species illustrating the changes accompanying increasing endoparasitism, prosobranch molluscs provide a case study for the evolution of parasitism. Combes also touches on some surprising examples of parasitic molecules and parasitic genomes.
Parasites can have complex life-cycles — there are trematodes with as many as four hosts — and varied forms, all of which have evolved under selection. Parasites can't find or follow hosts the way predators do prey, so they try to be in the right place at the right time to encounter them. Other tricks include "favorization", such as modifying intermediate hosts or their behaviour to make them more likely to be eaten, and changing the host's sex or the sex ratios of its offspring.
Birds and avian lice provide an example of host responses to parasites, which in this case include reallocation of resources between the current clutch and future reproduction. Humans are host to an "incredibly elevated number of parasites (relative to other species)", even allowing for their far more intense study.
Parasitism shades imperceptibly into mutualism. Combes surveys a range of mutualisms, looking at commensalism, phoresy (use of other organisms for transport), associations between bacteria and nematodes which cooperate in killing/digesting, pollinating wasps, cleaner fish, some examples of triple associations, and a range of nitrogen-fixing associations. Though ascription of "harmony" to nature is common, Combes argues that this is not found even in long-standing cell-organelle associations or between genes: "even parts of living organisms act as troublemakers when it is in their own interest".
Cuckoos provide an interesting example of a coevolutionary arms race and a test of the Red Queen hypothesis. Interestingly, young cuckoos don't inherit lice from their adoptive parents, giving them an ectoparasite-free start to life. Combes also looks at virulence and the question of whether optimal virulence will evolve.
Parasites may play a role in sexual selection, with a range of hypotheses as to why a female would prefer males with low parasite loads: less chance of becoming infected herself, better assistance raising young, and "good genes" for her offspring. In mammals, there is a curious relationship between parasitism, sexual dimorphism, and longevity.
A long chapter considers the distribution of parasites in space and time, both in their environment and within and between hosts. Combes also touches on cospeciation (the relationship between host and parasite phylogenetic trees), the role of parasites in speciation, and genetic variation for host resistance.
Having already touched on human responses to parasites in several chapters, Combes devotes a final chapter to "emerging diseases". Here he stresses the broader effects of human behavioural and ecological changes and not just the obvious hygiene and immune system angles.
The Art of Being a Parasite assumes little knowledge of biology — it is pitched at a level suitable for anyone who has read The Selfish Gene — but even biologists may find new ideas in it if they've never studied parasites. It will be an enjoyable read for anyone curious about evolutionary biology.
December 2005
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