Trends in Ecology & Evolution
Volume 15, Issue 9, 1 September 2000, Pages 378-383
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Perspectives
Resistance to xenobiotics and parasites: can we count the cost?

https://doi.org/10.1016/S0169-5347(00)01929-7Get rights and content

Abstract

The nature and cost of single genes of major effect is one of the longest running controversies in biology. Resistance, whether to xenobiotics or to parasites, is often paraded as an obvious example of a single gene effect that must carry an associated fitness ‘cost’. However, a review of the xenobiotic resistance literature shows that empirical evidence for this hypothesis is, in fact, scarce. We postulate that such fitness costs can only be fully interpreted in the light of the molecular mutations that might underlie them. We also derive a theoretical framework both to encompass our current understanding of xenobiotic resistance and to begin to dissect the probable cost of parasite resistance.

Section snippets

Predictions from xenobiotic resistance

For resistance to xenobiotics, expectations relative to costs derive from a model of adaptation developed by Fisher8. In this model, independent selection pressures shape the present (almost) optimal phenotypes through complex gene coevolution. This inferred gene interdependence makes any mutation with a large phenotypic effect likely to induce severe deleterious effects. Therefore, the key point determining the likelihood of a counterselection of resistance gene(s) is the shift in distribution

A diversity of molecular mechanisms

Recently, the molecular basis of xenobiotic resistance has been extensively reviewed elsewhere2, 12, 13. Four classes of mechanisms are observed: (1) constitutive overproduction; (2) constitutive underproduction of one gene product; (3) alteration of a target or receptor; and (4) an inducible change in gene regulation. Therefore, the expected ‘cost’ varies for each mechanism. The first class includes mechanisms that lead to a constitutive overproduction of drug-inactivating enzymes,

What do we mean by parasite resistance?

In reference to parasites, the term ‘resistance’ is often used in a broad context, referring to all mechanisms contributing to a decrease in the detrimental effect of the parasite33, 34, 35. These mechanisms include acquisition of avoidance behaviour, expression of inducible defences and modification of life history traits. A more specific meaning of resistance refers to the biochemical and physiological changes preventing proper parasite establishment, survival and/or development – here, we

Can we predict the probable cost of parasite resistance?

Theory on the evolution of host resistance to parasites and its potential associated cost has been derived from models based on host–parasite genetic interactions, rather than on models of adaptation to new environments. Two types of interaction have been investigated in particular (for details and comments see 47, 48). Matching-allele models correspond to symmetric frequency-dependence models, where the outcome of parasite infection is determined by the correspondence of one allele at a host

Prospects

Although there has been considerable recent progress in our understanding of both the theoretical, ecological and molecular basis of parasite resistance, our level of understanding still lags behind that of xenobiotic resistance. However, based on our knowledge of xenobiotic resistance, we can begin to make some predictions as to when fitness costs are likely to occur (Table 1). In this framework, costs associated with changes in resource allocation are restricted to one specific set of

Acknowledgements

We thank C. Berticat, T. de Meeus, M. Raymond, F. Rousset, J. Jokela and L. Hurst for fruitful discussions and comments on this article, and L. Hurst for the computer virus analogy. R.ff-C. was supported by a grant from the BBSRC. This is contribution 2000-44 of the Institut des Sciences de l’Evolution.

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