The occurrence and mechanisms of innate immunity against parasites in fish

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Abstract

Parasitic infections in teleost fish are limited by constitutive innate defence mechanisms that render the host refractory or reduce the severity of infection. Controlled challenge trials using naive animals provide indirect evidence of innate immunity as well as identifying the host range or specificity of a parasite, often when specific details of defence mechanism(s) are lacking. Examples of parasites for which innate immunity may be inferred from cross-infectivity studies include Gyrodactylus spp., Lepeophtheirus salmonis, Cryptobia spp., Trypanosoma spp., Ceratomyxa shasta, Myxobolus cerebralis and Kudoa thyrsites. Recent studies however, have begun to clarify the relative roles of innate and acquired immunity against parasitic infection in teleosts by recognizing the presence and significance of specific innate effector mechanisms. The physico-chemical characeristics of skin mucus, the presence of bioactive substances including lysozyme, complement, C-reactive protein, haemolysins and lectins and the epidermal migration of inflammatory cells and their secretions may affect the establishment and proliferation of ectoparasitic copepods, ciliates or monogenea. Similarly in refractory species, haematozoic parasites are lysed via the alternative complement pathway and in susceptible and refractory hosts, protease inhibitors associated with the plasma neutralize proteolytic virulence factors. Detailed knowledge of innate resistance mechanisms against histiozoic parasites are lacking although non-specific cytotoxic lymphoid cells and macrophages probably play a role. The demonstration in certain disease models that innate resistance traits are under genetic control and may be inherited in a simple Mendelian fashion suggests opportunities for selective breeding for resistance against parasitic disease. Beyond a small number of well-described models however, research programs focussing on innate immunity against parasites in fish are lacking. Given the relative importance of innate immunity in fish, particularly as disease losses continue to have an economic impact in aquaculture, this area deserves considerable attention.

Introduction

Interest in defence mechanisms of fish stems from a need to develop health management tools to support a rapidly growing finfish aquaculture industry while at the same time addressing questions concerning the origins and evolution of immunity in vertebrates. Models of innate immunity against parasites in teleosts are particularly interesting because of the life-history, biochemical and genetic complexity of the eukaryotic parasite compared with viral or bacterial pathogens and because of the potential for greater diversity in anti-parasitic mechanisms. However, because of the comparative difficulty in adapting parasites to laboratory investigation, anti-parasite innate resistance in fish has received relatively little attention. Whether against parasitic or other infectious agents, innate or nonadaptive immunity plays a proportionally greater role in resistance in fish compared with that in homeothermic vertebrates [1], [2]. It is quite likely that the slow onset and limited repertoire of adaptive immune mechanisms manifested in poikilotherms have conferred a selective advantage on individuals or populations possessing natural mechanisms of disease resistance [3]. As the occurrence of innate resistance may reflect an historic association between a host population and its parasite fauna, a clearer understanding of the mechanisms of resistance may therefore provide a novel perspective of host–parasite coevolution. Similarly, while natural resistance in fish against virulent parasite challenges forms the basis of much of our knowledge in this field, the protracted survival of non-virulent parasites in the hostile host environment suggests that adaptation by the parasite is a distinct possibility. This chapter will explore natural or innate immunity associated with the parasites inhabiting discrete sites in the host: ectoparasitic (in or on the skin), haematozoic (in the blood) and histiozoic or coelozoic (associated with other tissues or body cavities). Where known, anti-parasitic defence mechanisms will be described and their role in protection discussed.

Host-specificity, a measure of the capacity of a parasite to survive in or on species other than the definitive host is commonly reported. Superficially therefore, it would seem appropriate that host-specificity is an indirect indicator of innate resistance. However, this should be viewed with caution were data are based on field observations on the occurrence of natural infections or where the history of the experimental animals has not been determined and the possibility of prior exposure is not known [4]. Host–parasite interactions, particularly those of heteroxenous species in which one or more intermediate hosts occur in the life-cycle, are complex and reflect behavioural, physiological and/or immunological differences among and between potential hosts [5]. Thus, for example, the absence of an infection with a heteroxenous parasite in an area enzootic for the parasite may reflect ecological factors including the local absence of a suitable intermediate host or the absence of an appropriate predator–prey relationship conducive to transmission. Although monoxenous host–parasite systems are relatively simple, inference of innate immunity based solely on natural occurrences must be supported by controlled studies. Parasite-specific factors may also affect the host range. Non-suitable hosts are rejected by the copepodite larvae of the parasitic copepod Lepeophtheirus salmonis for example, in their search for an attachment site [6]. Thus, where appropriate, inferences of innate immunity based on examples of host specificity will be drawn from well-controlled studies using naive animals.

Section snippets

Conclusion

The capacity of naive fish to minimize the impact of or, to resist entirely, parasite infection is a function of both innate and adaptive defence mechanisms. This review has focussed on examples of parasites of the skin, blood and other tissues to discuss respective site-associated evidence for innate immunity and its effector mechanisms. While the significance to innate anti-parasite immunity of the alternative complement pathway in several fish tissues is apparent, the relative contribution

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