S36.Summary: Immunology and avian biology

1Laboratoire d'Ecologie, CNRS URA 258, Université Pierre et Marie Curie,Bât. A, 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France, fax 33 1 44 27 35 16, e-mail amoller@snv.jussieu.fr; ²Dipartimento di Biologia, Sezione Zoologia Scienze Naturali, Università di Milano, Via Celoria 26, I-20133 Milano, Italy

The ecological and evolutionary importance of parasites and diseases has been increasingly appreciated by biologists during the last decades (e.g. Price 1980; Loye and Zuk 1991; Toft et al. 1991; Grenfell and Dobson 1995; Clayton and Moore 1997). While ornithologists have played a central role in developing many fields of biology, the ecological and evolutionary implications of parasitism have been extremely under-exploited as a field of research, with the obvious exception of interactions between brood parasites and their hosts (Rothstein & Robinson 1998). The reason for this lack of interest among ornithologists in host-parasite interactions and how hosts defend themselves against parasite attacks remains obscure. However, one possibility is that this arose as a historical coincidence. When David Lack published extensively on population regulation, competition and life-history in the 1940's and 1950's, he severely under-emphasised the importance of parasites in all these contexts. For example in his influencial 1954 book, Lack wrote 'While further evidence is needed, it seems unlikely that disease is an important factor regulating the numbers of most wild birds' (Lack 1954, p. 169). Recently, things have changed and ornithologists are pursuing the study of the important host-parasite interactions as vigorously as biologists working on other taxa (e.g. Loye & Zuk 1991; Clayton & Moore 1997).

Given that parasites exploit their hosts for limiting resources and thereby reduce the survival prospects of parasitised hosts, there is strong selection on hosts to defend themselves against parasitism. Defence can be considered to have a number of different levels ranging from avoidance of infection as the first line of defence, to physiological and immunological mechanisms that allow expulsion of the parasite once infected, and to coping mechanisms that allow coexistence with minimum damage if complete recovery is impossible (Hochberg 1997).

The immune system of vertebrates provides one of two major defence systems that protect individuals from their surrounding biotic and abiotic environment (Klein 1990; Roitt et al. 1995; Wakelin 1996). The other defence line is the detoxification system which deals with reducing the danger of chemicals including biochemicals ingested in food (Gregus & Klaassen 1996). The immune system has a unique ability to distinguish between self and non-self and thereby prevent pathogens and parasites from exploiting hosts. Since the immune system interacts bidirectionally with the neuroendocrine system, the immune system has been likened to 'our sixth sense' (Blalock 1994). In this symposium we will briefly discuss a number of ways in which the immune system is important for an understanding of various aspects of avian biology.

The general features of the avian immune system are outlined in the paper by Anders Møller. The different components of the immune system and their role in anti-parasite defence are briefly reviewed. The mere magnitude of the avian immune system implies that immune function must be extremely costly. Hence we should expect that investment in one component detracts from investment in other activities such as maintenance, mating or reproduction. The evidence for such trade-offs between different components of the immune system, and between immune function and other activities, is briefly reviewed.

The first area of avian biology where immune function entered as a potentially functional explanation was sexual selection. Extravagant secondary sexual characters such as exaggerated plumes, colours, naked skin patches and spurs, but also costly display such as song and sexual display, have been hypothesised to signal the nutritional status or the quality of the signaller (Zahavi 1975). Hamilton & Zuk (1982) suggested that sexual displays might reliably reveal genetically based resistance to parasites, since only healthy individuals should be able to pay the cost of extravagant ornamentation. This and a number of other hypotheses implicating host immune function in sexual selection are reviewed by Marlene Zuk in the second paper.

Life-history theory deals with the evolution of breeding date, clutch size and similar traits (Roff 1992; Stearns 1992). Since resources are limiting, individuals are unable to breed early, lay large and many clutches and live indefinitely. Trade-offs between reproductive activities are central to life-history theory, although the physiological mechanisms ensuring such trade-offs remain obscure. Once reproduction has been initiated, offspring of many birds require parental investment in order to be viable. The level of investment in offspring relative to what the parents are willing to provide is the breeding ground for conflict (Trivers 1974). Parental investment theory attempts to investigate when and how much parents should invest in parental care (Clutton-Brock 1991). The reproductive value of offspring not only depends on the condition of the offspring, but also on their ability to defend themselves against virulent parasites. Young animals are not well-defended against parasitism, and the level of defence depends on the quantity and quality of food received. Nicola Saino reviews this literature in the fourth paper.

Host-parasite interactions in birds have received increasing attention in recent years, with a large number of studies demonstrating negative, but highly variable effects of parasites on host reproductive success and survival (Møller 1997). The damage inflicted by parasites on their hosts as measured by host mortality is termed virulence. The evolution of virulence has been studied intensively during the last two decades for purely scientific, but also practical reasons. Given that parasites differ in their fitness impact on hosts, this should affect the level of host investment in anti-parasite defence. Santiago Merino reviews the literature on the relationship between parasite virulence and host defence in the final paper.

A number of other aspects of avian biology are potentially closely associated with immune function. Since parasite faunas and strains vary geographically, and since hosts may adapt to local parasites under certain conditions (Gandon et al. 1996), host immune defence should link directly to the evolution of dispersal and migration. There is some evidence for host immune function being related to migration as discussed by Santiago Merino.

It is obvious that five symposium presentations cannot fairly represent an entire field. Hence, a number of subjects that are potentially very important have not been dealt with at all. Anders Møller directs readers to some of these subjects in his paper.

Blalock, J.E. 1994. The immune system: Our sixth sense. Immunologist 2(1): 8-15.

Clayton, D.H. & Moore, J. (eds). 1997. Host-parasite evolution: General principles and avian models. Oxford; Oxford University Press: 473 pp.

Clutton-Brock, T.H. 1991. The evolution of parental care. Princeton; Princeton University Press: 352 pp.

Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y. & Olivieri, I. 1996. Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London B 263: 1003-1009.

Gregus, Z. & Klaassen, C.D. 1996. Mechanisms of toxicity. In: Klaassen, C.D. (ed) Casarett and Doull's toxicology: The basic science of poisons. 5th edn. New York; McGraw-Hill: 35-74.

Grenfell, B. & Dobson, A.P. (eds). 1995. Ecology of infectious diseases in natural populations. Cambridge; Cambridge University Press: pp.

Hamilton, W.D. & Zuk, M. 1982. Heritable true fitness and bright birds: A role for parasites? Science 218: 384-387.

Hochberg, M.E. 1997. Hide or fight? The competitive evolution of concealment and encapsulation in host-parasitoid assocations. Oikos 80: 342-352.

Klein, J. 1990. Immunology. Oxford; Oxford University Press.

Lack, D. 1954. The natural regulation of animal numbers. Oxford; Clarendon Press: 343 pp.

Loye, J.E. & Zuk, M. (eds). 1991. Bird-parasite interactions: Ecology, evolution and behaviour. Oxford; Oxford University Press: 406 pp.

Møller, A.P. 1997. Parasitism and the evolution of host life history. In: Clayton, D.H. & Moore, J. (eds) Host-parasite evolution: General principles and avian models. Oxford; Oxford University Press: 105-127.

Price, P.V. 1980. Evolutionary biology of parasites. Princeton; Princeton University Press: 237 pp.

Roff, D.A. 1992. The evolution of life histories. New York; Chapman and Hall: 535 pp.

Roitt, I., Brostoff, J. & Male, D. 1996. Immunology. 4th edition. London; Mosby: 28 chapters. [NO CONTINUOUS PAGE NUMBERS]

Rothstein, S.I. & Robinson, S.K. (eds). 1998. The ecology and evolution of brood parasitism. New York: Oxford University Press: in press.

Stearns, S.C. 1992. The evolution of life histories. Oxford; OxfordUniversity Press: 249 pp.

Toft, C.A., Aeschlimann, A. & Bolis, L. (eds). 1991. Parasite-host associations: Coexistence or conflict? Oxford; Oxford University Press: pp.

Trivers, R.L. 1974. Parent-offspring conflict. American Zoologist 14: 249-264.

Wakelin, D. 1996. Immunology to parasites. 2nd edn. Cambridge; Cambridge University Press: 204 pp.

Zahavi, A. 1975. Mate selection - a selection for a handicap. Journal of theoretical Biology 53: 205-214.