Parasitology Is Dead. Long Live Parasitology!

Authors


Ecology and Evolution of Parasitism. Thomas, F., J.-F.Guégan, and F.Renaud , editors . 2009 . Oxford University Press , Oxford , U.K. 224 pp. $70 (paperback). ISBN 978-0-19-953533-0 .
Ticks. Biology, Disease and Control . Bowman, A. S., and P. A.Nuttall , editors . 2008 . Cambridge University Press , Cambridge , United Kingdom . 506 pp. $141.99 (hardcover). ISBN 978-0-521-86761-0 .
Primate Parasite Ecology. The Dynamics and Study of Host-Parasite Relationships . Huffman, M. A., and C. A.Chapman , editors . 2009 . Cambridge University Press , Cambridge , U.K. 531 pp. $131.99 (hardcover). ISBN 978-0-521-87246-1 .

Imagine taking a college class or becoming an undergraduate major in predatorology or primary producerology. Most of us would think this rather ludicrous because we generally do not consider the means by which organisms garner resources as sufficiently fundamental to define a subdiscipline of biology. But somehow parasites have been considered odd enough in their mode of foraging to justify singling them out for considerable special attention. Parasitology is one of the oldest distinct branches of biology, having evolved as an unusually interdisciplinary combination of autecology, physiology, developmental biology, functional morphology, systematics, ethology, and immunology. But as modern biology has restructured around levels of organization (cellular and molecular, organismal, and community and ecosystem), the appropriate place for parasitology has become unclear. Although we have no rigorous data to test our impression, it appears to us that college classes and majors in parasitology have waned dramatically in recent decades. Paradoxically, though, the demise of parasitology has been accompanied by increasing attention to the biology of parasites.

These three books represent three pathways by which modern parasitology is redefining itself. The first pathway results from intertwining the biology of parasites with central concepts of ecology and evolutionary biology. The Thomas et al. volume, which could be subtitled “Nothing in Biology Makes Sense Except in the Light of Parasitology” (to adapt a phrase from T. Dobzhansky), takes this approach. We learn that life-history traits of species, including age at first reproduction, reproductive rate, and longevity, should not be viewed as fixed, species-specific traits. Rather, they are highly flexible—especially in the face of parasitic infections. For instance, parasitized individuals often breed earlier and more often than unparasitized conspecifics. Parasite burdens and the underlying genetics of resistance are critical in sexual selection through both mate choice and intrasexual competition. For instance, attractiveness as a mate can be lessened if the potential mate is parasitized, and mate choice can be correlated with immunological compatibility with the chooser.

The behaviors of many (perhaps most) animals are profoundly affected by the need to avoid parasites or to reduce their virulence, yet once infected, host behavior is strongly affected by parasites to increase parasite fitness. Parasites can promote or accelerate speciation because hybrids between strains or subspecies of hosts are typically much more susceptible to parasites than are parental genotypes, which leads to reduced interbreeding and greater genetic differentiation. Parasites can regulate populations to the point of extirpation, which has a positive outcome when we seek to remove pests (e.g., through biocontrol), but a negative outcome when the population is of conservation concern. This book could revolutionize the thinking of some ecologists and evolutionary biologists who consider life-history evolution, sexual selection, behavior, and processes of population differentiation and regulation intrinsic to the focal species rather than influenced by parasites.

A second pathway to redefinition of parasitology is the use of rapidly developing molecular-genetic techniques to enrich our understanding of the more traditional aspects of parasitology (e.g., parasite physiology, immunobiology, endocrinology, and functional genomics). The Bowman and Nuttall book takes this approach with ticks as the focal parasites. This volume could be subtitled, “The More You Know about Ticks, the More Fascinating They Become.”

Although ticks are themselves obligate, blood-feeding parasites of vertebrates, they are also hosts and vectors of many microscopic parasites—viruses, bacteria, and protists-–that infect vertebrates of various kinds, including humans. From this book we learn that bacterial parasites can affect their vectors. For example Borrelia burgdorferi (causative agent of Lyme disease) causes its vector, the blacklegged tick (Ixodes scapularis), to increase expression of a salivary-gland protein more than 10-fold over baseline and then coats itself in this protein, which is a potent T-cell immunosuppressant in mammalian hosts. The result is that the bacteria co-opt tick physiology to evade the immune system of hosts. In fact, no fewer than five of 21 chapters are devoted largely to describing various aspects of the seemingly arcane world of tick spit, which contains a rich pharmacopeia of vasodilatory compounds, antiplatelet factors, anticoagulants, antihistamines, other antiinflammatory compounds, and analgesics. Vaccines against tick-borne diseases that are based on some of these antigenically active compounds are now under development for humans and domestic animals. Both ticks and the microparasites they transmit have evolved to persist in radically changing environments—ticks alternate between persistent free-living stages, contending in many cases with harsh environmental conditions, and short bouts of attachment to and blood-feeding on mammals, birds, and squamates. Their associated microbes alternate between tick and vertebrate hosts. Chapters in the Bowman and Nuttall volume describe the exquisite adaptations of ticks and their microbial hitchhikers to these varying environments. But they do so with little attention to underlying conceptual issues in ecology and evolutionary biology that dominate the Thomas et al. volume.

The third pathway is to “discover” parasites as critical to the biology of a focal taxonomic group of hosts. The Huffman and Chapman volume takes this approach to the ecology of primates, which for most of its history has largely ignored parasites. From this volume we learn that the dominant paradigm that primate social organization is shaped by competition for resources and mates is being shaken by a new view that social organization is shaped at least as strongly by avoidance of infectious disease. For instance, the chapter by Walsh et al. argues that mortality of gorillas from Ebola (approximately 96% in some sites in Congo and Gabon) was higher than that of chimpanzees (<86%) because gorilla social groups have greater rates of interindividual contact and thus virus transmission. They suggest that the territorial and fission–fusion structure of chimpanzee social groups evolved to lessen the impacts of virulent infectious diseases such as Ebola. More generally, primatologists are discovering that primates are in some ways an ideal group for use in addressing questions about the ecology and evolution of host–parasite interactions. They are often studied through long-term monitoring of groups of identifiable individuals in the field, and thus the social and genealogical context of individuals is often known, selection of food items is observed directly, and researchers can assign feces to individuals because they defecate conspicuously. This latter characteristic is important for examining the causes and consequences of variable loads of gastrointestinal parasites. Primate parasitology is all the more compelling because of the sheer number of parasites nonhuman primates share with humans and because so many primates are of conservation concern.

The Thomas et al. volume is an English translation (by the authors themselves) of a text that was published originally in French in 2007. All chapter authors except two (a Canadian and a New Zealander) are French, and all are francophone scientists. Small translational glitches exist throughout, but they are not distracting, and the quality of prose is consistently high. Each chapter ends with bulleted lists of “Important Points” and “Questions for Discussion.” The book is intended as a text for university students and it certainly would be a leading candidate for undergraduate and graduate courses in parasitology. It would also make an excellent companion text for general courses in ecology and evolutionary biology. The Bowman and Nuttall volume is a revision of an eponymous 2004 supplement to the journal Parasitology. All but 3 of the original 24 papers are present in the newer volume. Most chapters contain modest changes from the original; only a few have been more substantially revised and updated. This book is a must read for acarologists and highly recommended for medical entomologists. For parasitologists and for conservation biologists, the volume seems less compelling. The Huffman and Chapman volume is a hybrid between a practical manual on how to collect and identify parasites of primates and study their effects and a general text on the biology of primate–parasite interactions. It also combines a few excellent, conceptually structured overview articles with a series of empirical studies of much narrower scope. Primatologists are likely to find the combined practical, empirical, and synthetic chapters essential reading as they embrace parasites as profoundly important to the animals they study and to themselves.

More and more, knowledge of the biology of parasites is recognized as essential to the theory and practice of conservation biology. Parasites are frequently transported long distances by people, can jump hosts, and increasingly are causing the demise of host species. For these reasons, conservation biologists will often need to manage parasites to achieve their goals. On the other hand, parasites are a critical component of biological diversity, can themselves become imperiled as their hosts decline, can contribute strongly to drug and vaccine development, and can indirectly protect critical areas by discouraging human use. The rebirth of parasitology, represented well by these three books, will provide essential knowledge for conservation biologists.

Ancillary