Why Should Parasite Resistance Be Costly?
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116 Opinion TRENDS in Parasitology Vol.18 No.3 March 2002 and reviewing the logic leading to the assumption Why should parasite that fitness costs are associated with parasite resistance. First, they listed the categories of the molecular basis of resistance to xenobiotics (e.g. resistance be costly? pesticides and antibiotics). Second, they applied these categories to parasite resistance, emphasizing immunological forms of resistance. Coustau et al. [2] Mark C. Rigby, Ryan F.Hechinger and Lori Stevens pointed out that fitness costs of resistance are often, simply, extensions of the molecular mechanisms used to accomplish resistance Parasite resistance is sometimes associated with fitness costs. Costs of (e.g. through NEGATIVE PLEIOTROPY). They recognized resistance are fundamentally important in epidemiology, and in the ecology four specific mechanisms by which molecular and evolution of host–parasite interactions. The cost of resistance is often resistance could be achieved: envisioned as the cost of re-allocating limiting resources to resistance (1) increasing trait expression; machinery from other traits. This popular paradigm has resulted in a spate of (2) decreasing trait expression; research that assumes a fitness cost to resistance. We comment on this trend (3) qualitative trait modification; and and propose a working framework of various resistance means and (4) inducible trait expression. mechanisms. Within these means and mechanisms, we suggest that many are Clearly, increasing the expression of DEFENSE- not likely to incur significant fitness costs. related molecular traits could increase resistance. However, decreasing the expression of something that RESISTANCE (see Glossary) to parasites has important is necessary for parasites (e.g. molecules that implications for the agricultural, veterinary, medical, parasites use as cues to find their targets, such as the conservation, ecological and evolutionary sciences. Duffy receptors used by the malaria parasite With rapid advances in the understanding of the Plasmodium vivax to enter red blood cells [3]) molecular basis of resistance, there has been can also lead to resistance. Qualitative modifications increasing interest in the use of genetic engineering leading to immunological resistance are possible, to introduce parasite resistance alleles into food crops for example, through the alteration of defense and livestock. In addition, an understanding of products used to recognize (Box 1) or fight resistance is necessary when considering the efficacy parasites. Indeed, resistance to some parasites is and safety of using parasites in the bio-control of pest associated with specific variants of recognition species. A central issue in the study of resistance is molecules in plants and animals [4–6]. Resistance understanding the factors that determine the could also be achieved by employing resistance appearance, spread and distribution of resistance traits only when necessary, that is using inducible alleles within populations and across geographical defenses. As Coustau et al. [2] suggest, fitness landscapes. One factor of paramount importance to costs of resistance are most likely to be associated all of the above is the potential COST OF RESISTANCE. with the first mechanism, and fitness costs are Resistance is frequently conceptualized as a merely possible, but not necessary, with the other resource-driven, mystical ‘black box’ (i.e. resistance three mechanisms. is considered as a single trait that becomes more effective with increased resource input). Glossary Furthermore, resistance is often considered to reside Cost of resistance: Although the host could benefit from solely in the domain of the immune system. Some resistance by decreasing the effect of parasites or avoiding recent empirical work has shown that parasite parasites, the defenses used to achieve resistance could have an resistance sometimes comes with an associated associated fitness cost. When the cost of the defenses outweighs their benefit (e.g. defense in the absence of parasites), there could Mark C. Rigby* FITNESS cost. This cost is often envisioned as the cost of be a net fitness cost of resistance. Dept of Ecology, re-allocating limited resources to resistance Defense: Any trait an organism uses to prevent or reduce the Evolution and Marine effects of infection (i.e. a trait used for resistance). Biology, University of machinery from other fitness-related traits [1], and Fitness: The genetic contribution of an individual to the next California, Santa Barbara, recent work often implicitly assumes that resistance generation, relative to other members of the same population. CA 93106, USA. is costly [1]. Here, we revisit the assumption of a cost Parasites could reduce the fitness of an individual by reducing *e-mail: rigby@ of resistance. Further, we expand on previous work survival, in addition to reproduction (i.e. number and quality of lifesci.ucsb.edu and propose a working conceptual framework offspring). Ryan F.Hechinger detailing how parasite resistance could be Knockout: To prevent the expression of a gene by blocking Dept of Ecology, transcription, translation or the action of the gene product(s). Evolution and Marine accomplished and conclude that there are many Over-expression: Increased gene transcription or translation, Biology, University of important forms of parasite resistance which are resulting in overproduction of the gene product(s) relative to the California, Santa Barbara, unlikely to have fitness costs, relative to more non-modified form. CA 93106, USA. Negative pleiotropy: When a gene has both positive and negative susceptible phenotypes. effects on different phenotypic traits. Lori Stevens Resistance: The ability of the host to avoid or diminish the effects Dept of Biology, Means and mechanisms of resistance of a particular parasite through the use or possession of defense University of Vermont, traits, relative to other members of the same population. Burlington, VT 05405, Coustau et al. [2] advanced our understanding by USA. looking inside the ‘black box’ of molecular resistance http://parasites.trends.com 1471-4922/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(01)02203-6 Opinion TRENDS in Parasitology Vol.18 No.3 March 2002 117 Box 1. The cost of recognition variation The first step in many successful inducible defenses variation in recognition alleles is likely to be cost-free is recognizing the attack. Defense activation requires and all the examples of recognition in Table 1 have no recognizing a cue from the parasite which reliably known costs, there could be exceptions if the signals that the host is, or will be, attacked. In the recognition allele is negatively pleiotropic or if the immune system of animals, receptors bind to allele is accompanied by increased expression of the parasites and activate host defenses [a]. Similarly, receptor. The outcome of this scenario is that hosts plants also use receptors (many are called R genes) to could exert selection on parasites to avoid recognize parasites (or pathogens) and activate their recognition. Parasites, in turn, exert selection on defenses [b]. hosts to recognize them despite their adaptations to Qualitative variation in the molecular receptors avoid detection. This is expected to cause frequency- that hosts use to recognize parasites could be some of dependent cyclical antagonistic co-evolution. This the best examples of cost-free means of achieving form is cyclical in that the frequency of recognition parasite resistance. There are so many different alleles in hosts and evasion alleles in parasites cycle parasite taxa, combined with diversifying selection over time, with neither side ever winning. This within taxa to avoid recognition by the host, that most scenario of cycling recognition alleles has been called hosts are unable to recognize all of the parasite trench warfare [c]. species or strains that attack them. In other words, References owing to a limited number of genes coding for a Roitt, I. et al. (1996) Immunology (4th edn), Mosby/Times recognition alleles, there are constraints on the Mirror International Publishers Ltd particular recognition alleles an individual can have. b Hulbert, S.H. et al. (2001) Resistance gene complexes: evolution and utilization. Annu. Rev. Phytopathol. 39, 285–312 The constraint entails fitness costs, but the cost is c Stahl, E.A. et al. (1999) Dynamics of disease resistance based on differential susceptibility to parasites and polymorphism at the Rpm1 locus of Arabidopsis. Nature 400, is not present in the absence of parasites. Although 667–671 Given the recent trend in implicitly assuming that use behavioral defense traits as well! (See Fig. 1.) there are fitness costs associated with parasite Life history (iv) changes could lead to resistance, for resistance, we would like to expand on the important example, by minimizing the duration of susceptible point by Coustau et al. that there could be cost-free life-history stages, changing the timing of forms of resistance [2]. We propose five categories for reproduction or producing offspring better suited to the general means of defense by which resistance resist parasites. Physical aspects of host morphology could occur or evolve. These are alterations in the: (or structure) (v) could also be used to deter, repel or (i) host immune system; remove parasites in what is termed structural (ii) host biochemistry; resistance. Altogether, there are several widely (iii) host behavior;