Claude Combes - The Art of Being a Parasite

The University of Chicago Press, Chicago 60637

The University of Chicago Press, Ltd., London

2005 by The University of Chicago

All rights reserved. Published 2005

Printed in the United States of America

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ISBN: 0-226-11429-5 (cloth)

ISBN: 0-226-11438-4 (paper)

ISBN-13: 978-0-226-11429-3 (cloth)

ISBN-13: 978-0-226-11438-5 (paper)

ISBN-13: 978-0-226-77872-3 (ebook)

Also published in French as Les associations du vivant: Lart dtre parasite, Flammarion, Paris, 2001.

Library of Congress Cataloging-in-Publication Data

Combes, Claude. [Associations du vivant. English]

The art of being a parasite /Claude Combes; translated by Daniel Simberloff.

p. cm.

Includes bibliographical references and index.

ISBN 0-226-11429-5 (cloth: alk. paper)ISBN 0-226-11438-4 (pbk. : alk. paper)

1. Parasites. 2. Parasitism. I. Title.

QL757.C614513 2005

577.857dc22

2005000674

The paper used in this publication meets the minimum requirements of the American National Standard for Information SciencesPermanence of Paper for Printed Library Materials, ANSI Z39.48-1992.

THE ART OF BEING A PARASITE

CLAUDE COMBES

Translated by Daniel Simberloff

The University of Chicago Press

Chicago and London

Parasites form a large proportion of life on the earth.

PETER W. PRICE (1980)

We are living and surrounded by life.

Listen to Prvert: Then all the animals, the trees and plants, begin to sing, to sing, to sing at the tops of their voices, the true living song, the song of summer, and everyone drinks, everyone raises a glass.

Everyone...

Prvert was able to say everyone. So many different living beings, those that are visible and those that are unseen. And some of these unite to form symbioses, or living associations. Because one of the fundamental characteristics of life is that it is present on our planet in discrete forms. But the discreteness can sometimes be erased. We can imagine that life arose on our planet just once and that it remained in the form of a single species, evolving or not throughout the geological ages. Possibly the first of these propositions (that life arose just once) is correct. The second is obviously false.

Far from remaining monotonous, life has exploded into a multitude of distinct species. These species are separated from one another by the criterion of reproductive isolation: the horse and the cow do not hybridize; thus, they belong to separate species. The horse and the donkey mate, but their hybrids are sterile; therefore they also belong to separate species. We believe that several million species (of which only 1.5 million are known) constitute the current biosphere and that possibly 2 billion species have existed at one time or another since the origin of life about 4 billion years ago.

In the context of biological evolution, this splitting of life into a multitude of species can be represented as an enormous tree whose shape we try to reconstruct by various means. Each node or branch point of the tree corresponds to an act of speciation, the separation of a parent species into two daughter species. This tree can be interpreted in terms of information.

Each living being, from the most primitive in terms of complexity to the most highly evolved (which is usually considered to be humans), is constructed on the basis of information encoded by the nucleic acids of the genotype. Because they are structured as a succession of nucleotides, nucleic acids can encode blueprints of a nearly infinite number of proteins. Starting with these proteins, cascades of interactions lead to the synthesis of many other molecules and finally to the construction of an entire organism, whose physical manifestation is known as the phenotype. For example, the construction of a human being requires some three billion nucleotides (although only a fraction of them actually engage in making proteins).

When speciation occursthat is, when an ancestral species gives rise to two daughter species that cease to interbreedthe information associated with each daughter species is definitively isolated from that of the other species, just as branches of a tree do not rejoin once they have separated.

Associations, however, can form between species that have followed separate evolutionary trajectories (often for a very long time). Let me return to the metaphor of evolution as an immense tree: it is almost as if two branches come together and from then on are associated. Such associations are termed symbioses (fig. 1). In the great majority of cases, one of the two species uses the other not only as habitat but also as food. The species inhabiting the other is the parasite, and the species it inhabits is the host. As we shall see, symbioses are generally strongly asymmetric.

Of course there exist many more nuanced sorts of symbioses; the most important variant is when the exploitation is not always in the sense I have just described. In some cases (the number is increasing as study of the phenomenon becomes more intensive) it is not the inhabitant species that is exploiting the habitat species, but the inverse. To speak in deliberately provocative terms, I can say that it is not the parasite that exploits the host, but the host that exploits the parasite. Because this inversion cannot occur unless there is at least some reciprocity in the exchange of benefits between species, such symbioses are called mutualisms rather than parasitisms. I return to this apparent paradox at the end of this chapter.

In a symbiosis, whether a parasitism or a mutualism, the genetic information of each species can interact with that of the other in two ways. First, each species may contribute to some degree in the production of the phenotype of the other species, thus extending its genetic expression into the phenotype of its partner. This is a hybridization of information. Second, these species can extend the interaction still further by exchanging DNA sequences. This is an exchange of information.

Fig. 1. Hypothetical schema showing how two repositories of genetic information, separated for millions of years, can find themselves associated in a symbiosis.

We will see throughout this work that symbioses, whether parasitic or mutualistic, have played a key role at several points in evolutionary history.

By hybridization of information I mean what Richard Dawkins (1982) has called, in a striking metaphor, the extended phenotype. What do I mean? In response to this question, let us consider, with Dawkins, galls that certain parasitic insects induce in their host plants.

When, for example, a wasp in the family Cynipidae lays an egg on the leaf of an oak or a rose bush, cells of the leaf multiply to form a mass around the developing parasite. This excrescence is the gall. Its apparent function is twofold: on the one hand it protects the parasite from various enemies by enclosing it in a thick wall; on the other hand it provides nourishment, because the insect larva consumes the gall from within it. Moreover, the insect actually controls the growth of the gall in that the structure of this excrescence arises gradually, apace with the needs of the larva.