Claude Combes

THE ART OF BEING A PARASITE

This book is packed with examples of the often astonishing forms which parasitism takes and of the intricate complexity of parasite life cycles. However, it is not just a collection of strange facts; it offers a thoughtful discussion, using the metaphor of arms races, of how natural selection works in the evolutionary process.

The phenomenon of parasitism is extraordinarily widespread in nature. Combes finds, indeed, that it is difficult to assign limits to the concept and to say what is, and what is not, parasitism. The distinction between parasitism and mutualism is often unclear. Moreover, a relationship which is initially parasitic may change to one of mutualism, or the reverse may occur.

Combes identifies three stages in the development of parasitism. In the first stage the parasite remains on the surface of its host. In the second, it penetrates into the host while still retaining a connection with the outside. In the third stage it becomes wholly endoparasitic and this may entail profound modifications in its structure and physiology, such as the loss of a digestive system. Parasites having no contact with the exterior clearly have to make special arrangements for reproduction and the infestation of new hosts.

Probably the most fascinating question that arises in connection with parasitism is how it may have arisen in an evolutionary sense. We cannot know this directly, since we cannot go back into the distant past to see what happened, but we can get clues in some cases by comparing parasites with related free-living species. The construction of plausible scenarios is often challenging, however, as Combes admits, especially when parasites have complicated life cycles involving three or even four different hosts.

Intuitively, one might suppose that having a complex life cycle would be disadvantageous. However, Combes provides examples which show just the opposite. For example, a fish parasite which infests the turbot has three hosts (a copepod, a goby, and the turbot), and it is more successful than a related parasite which lacks the goby phase. This is because turbot don't eat many copepods except when they are young but they do eat gobies, and gobies eat a lot of copepods. But there is not an invariable trend towards complexity; in other cases simplicity is selected.

Parasitism provides many examples of what Richard Dawkins has called the extended phenotype. For example, a group of bacteria called Wolbachia, found mainly in crustacea and insects, is confined to the cytoplasm of the host and cannot be cultured separately. They are transmitted in the maternal host line, probably because spermatozoa are too small to contain them. It would be an advantage for the bacteria if the hosts produced more females than males, and in fact the bacteria have acquired the means of bringing this about, including feminizing genes that act on the sexual glands of their male hosts and make them into ovaries.

What is perhaps even more surprising is that Wolbachia is a mutualist in some cases. A small wasp, which is itself parasitic, cannot reproduce unless it is infected with the bacteria. And some female fruit flies carry a mutation that makes them sterile, but the effect of this mutation is reversed, allowing them to become fertile again, if they are infected with Wolbachia. An interesting fact about Wolbachia is that it is closely related to the bacterium that gave rise to mitochondria in eukaryotic cells (and mitochondria are also transmitted almost exclusively in the maternal line).

We are sometimes told that it is a bad thing for a parasite to kill its host and that infectious organisms will therefore become less virulent with time. This comforting thought, however, is only a half-truth. Combes explains that there is no general answer to the question: what is optimal virulence? It all depends on the circumstances, though some rough rules can be deduced. For example, competition among different genotypes in a species nearly always leads to increased virulence. Combes thinks that this explains the marked virulence of the malarial parasite Plasmodium falciparum in humans.

Combes has a detailed discussion of the parasitic behaviour of various cuckoo species. An arms race has has clearly been at work here between the cuckoos and in the birds they parasitize. Some species of birds have acquired the ability to detect cuckoo eggs. Others have not, and this is difficult to explain; Combes suggests that the cost of detection may sometimes be more than it is worth, while in other cases cuckoo parasitism may have developed too recently for the victims to develop counter-measures. Parasitism of the dunnock, for example, may have begun as recently as the fourteenth century.

Parasitism is a fascinating subject, of literally vital importance to us (humans are the most highly parasitized species among all those that have been studied). As Combes remarks in his concluding chapter, we must expect that new human diseases will appear as parasites adapt to take advantage of the new opportunities that changes in the climate and in our way of life afford them.

The original French of the book has received an excellent translation by Daniel Simberloff, who is himself a biologist, which means that the text is not, as too often happens these days, marred by mistranslations.