The Art of Being a Parasite (ISBN 0226114384)

OF "WORMS" AND MEN:
The Art of Being a Parasite. Claude Combes, translated by Daniel Simberloff. The University of Chicago Press, Chicago, IL, 2005. 291 pp. $25.00 (0226114384 paper). Parasitology books are traditionally compendia of the bizarre and macabre-page after page of sinister pathogens infecting obscure hosts and undergoing complex metamorphoses via stages with esoteric names. Combes's book is appropriately replete with these details, covering a wealth of natural history, anatomy, life history and behaviour. What sets this book apart is the way in which this information is presented. Rather than merely catalogued, host-parasite interactions are used to illustrate broad ecological, evolutionary and philosophical discussions. After each chapter, one comes away both with a detailed knowledge of current parasitological research, but also with a deeper and broader grasp of fundamental conceptual issues in the biological sciences generally. Rather than restricting himself to the usual suspects-nematodes, flukes, trematodes and tapeworms-the reader is presented with an unprecedented breadth of examples. This book is the first parasitology text that considers mitochondria, mycorrhizae and mistletoes; cuckoos, cyanobacteria and chromosomes as worthy examplars of parasitism. Many biologists will be startled to find their study organisms included in a parasitological treatise, and Combes is to be credited for working from such a broad literature base. This breadth makes the emergent generalities and widely supported patterns all the more remarkable. A pertinent example is this passing comment: "this is why we know of no parasite (at least among the multicellular species) that has evolved to become free-living, even if such a passage appears to be theoretically possible", p 34; pointing out that the route to parasitism is necessarily a one-way street. In addition to novel examples, many case studies are well known-leaf cutting ants and their fungus gardens, Madagascan orchids and their moth pollinators, ungulates and their blood-borne trypanosomes. By incorporating recent findings and drawing comparisons with analogous systems, Combes presents many of these "text-book examples" in a new light, often revealing these interactions to be more convoluted than first thought. Hence, in the review of cuckoos and other nest parasites, we learn that cuckoos do not pick up ectoparasites from their adoptive parents-it is only when they mate in their second year that they acquire lice and mites from conspecifics. Hence, the very act of being a parasite confers a cuckoo immunity to parasitism until maturity. Even the footnotes are replete with parasitological gems: reminding us that the reason prized Woodcock are best consumed whole is to ensure the flavour of "millions of small tapeworms in the genus Amoebotaenia" residing in their intestines infuse the meat during cooking. A persistent theme throughout the book relates to the two filters or diaphragms defining the evolution of host-parasite systems: the encounter filter and the compatibility filter. Originally introduced in his 1995 book, this theme is well integrated and makes a significant contribution to the conceptual basis of understanding host-parasite interactions. There is a thoughtful clarification of the distinction between virulence and pathogenicity, an excellent précis of the Red Queen Hypothesis and a succinct summary of adaptationism, although he perpetuates the misuse of the term spandrel (c.f. pendentive, after Houston 1990). Closer to home, Combes discusses why humans play host to more parasites than any other species and, far from being merely a sampling artefact, elucidates the many facets of human history, behaviour, distribution and lifestyle that pre-dispose us to infection. This has dramatic consequences for human health and, more surprisingly, the health of our domestic animals. Taenia saginata and T. solium (the beef and pork tapeworms respectively) were both human parasites first, passed horizontally to these animals soon after domestication. The writing style is accessible, lucid and surprisingly engaging, using occasional anecdotes and asides to punctuate the text. Originally published in French, Daniel Simberloff translated the book into English, and his voice is almost imperceptible-the hallmark of a skilled translator (although I doubt Voltaire would have approved of his satire "Candide" being referred to as a pamphlet!). The French character of the book is still retained-the text is replete with idioms and analogies familiar to francophones. More importantly, Combes cites the French parasitological literature extensively, revealing a wealth of hitherto under-appreciated literature to monolingual researchers. While I was pleased at the inclusion of a glossary, it was all too brief (four pages) and many terms defined in the text were not included, including the subtle differences between endoparasites and mesoparasites, and the distinction between allomones and kairomones. The book is well illustrated with half-tone diagrams, flow-charts and graphs, all of a consistently high standard, and index is comprehensive. While the engaging style and uncluttered language make this book accessible to a general audience, this book is aimed squarely at non-parasitologist professional biologists, emphatically underscoring the relevance of parasitology to evolutionary biology and the life sciences generally. Combes demonstrates that there are few, if any clear-cut distinctions between predation, parasitism, commensalism, and mutualism. Rather, they are presented as a continuum, challenging current typological approaches to their study. Any biologist interested in interspecific interactions of any kind should read this book-it will change their view of what is (and isn't) a parasite, broaden their taxonomic horizons and remind them that there is a wealth of primary scientific literature written in other languages awaiting the adventurous explorer. DAVID M WATSON Institute for Land, Water and Society Charles Sturt University Albury NSW 2640, AUSTRALIA References cited Houston, A. 1990. Matching, Maximizing and Melioration as Alternative Descriptions of Behaviour. Pages 498-509 in Meyer JA, Wilson S, eds. From Animals to Animats. Cambridge, MA: MIT Press.

The little (and some not so little) buggers are everywhere!:
The term "parasite" usually evokes the image of some little critter feasting off some "host" unable to reject it or cast it away. Claude Combes wishes us to revise that simplistic description in favour of a more realistic view. "Parasitism" needs better definition. He prefers a more descriptive term, "mutualism" which covers more biological territory. In this wonderfully conceived and beautifully written account of what science has learned about parasites, he explains how species interact, sometimes to mutual benefit. The "art" of being a parasite resides in their evolutionary history. Some creatures, once free-living, have managed to occupy others at various surface contact areas or internally. The mitochondria in our cells, the "energy engines" were clearly once free-living bacteria. Invading cells, they paid a "rent" of genes donated to the main genome in the nucleus. The arrangement is apparently incomplete, as mitochondria still make bids for independence. In some cases, the intruder merely occupies the host, generally on its way to another species to enter its reproductive phase. Other invaders proved to interact so well with their hosts that they have become entirely dependent on each other for survival. Combes lays all these situations out for us, describing the process as part of the "evolutionary arms race". That arms race has other applications such as predator-prey interaction, but the result in that scenario has no mutual benefit - the predator wins, eating the prey, or loses and goes hungry. The key to parasite-host relations lies in two filters. The invader must pass an encounter filter, which might reflect little more than availability. If a potential host is not close to the parasite, there's nothing to attach itself to. If the parasite is species specific - as is the case with the wasp-fig associations, the potential parasite will expire. The host may have mechanisms in place to resist the intrusion. If the parasite gains entry, a "compatibility" filter situation arises. The host may have immunity elements that cast off the intruder. Both these filter systems are the basis of the evolutionary arms race between parasite and host. That situation has been credited with being the foundation for all evolution. The erection of the filters by the host and changes to circumvent them by the parasite may have brought about selection changes. This is the basis for much of what's called "coevolution" - an ongoing process over time in which each species changes in response to changes in the other. While "parasitism" is generally considered to be one species utilising another's resources - even if the parasite is using the host as a way-station to another host - there are many cases in which the arrangement is more mutual. The wasp-fig liaison is fairly well known now with the wasps acting as pollinators between the fig plants. Except that the wasp lives in galls formed in the fig's branches, it resembles the action of bees with flowers. A less known mutual arrangement is the inhabiting of molluscs by bacteria. The mussel provides a sheltered environment, but feeds on the bacteria. Yet enough are permitted to survive to allow them to reproduce and infest other mussels. As Combes notes, "Who is exploiting whom?" It's a big question, since "parasites" make up more than half the planet's biomass and human beings are subject to more parasites than any other species. Not all parasites are microscopic nor even small. One of the more recognised "parasites" are the cuckoos of Europe and cowbirds of North America. Both lay eggs in the nests of other species. These, in turn, have sometimes learned to recognise the intruder's eggs and cast them from the nest, or the nest is abandoned with the mating pair relocating to a new site. Less commonly known is a tapeworm inhabiting whale intestines. Combes declares it to be the longest creature living - at 40 metres! All these elements are presented in a beautifully written (thank you, David Simberloff for an excellent translation) and effectively illustrated book covering a topic many would avoid. They shouldn't. Given that parasites are so complex and prevalent they are creatures and lifestyles we need to know more about. (stephen a. haines - Ottawa, Canada)