SURVIVAL OF DISTASTEFUL INSECTS AFTER BEING ATTACKED BY NAIVE BIRDS: A REAPPRAISAL OF THE THEORY OF APOSEMATIC COLORATION EVOLVING THROUGH INDIVIDUAL SELECTION

Many unpalatable species of insects are brightly colored, i.e., aposematic, and this has been regarded as a signal to predators. Today there seems to be a general consensus that most predators learn to avoid aposematic prey only after sampling, and in the process killing, one or a few individuals (Eibl-Eibesfeldt, 1952; Brower, 1958a, 1958b, 1958c; Harvey and Greenwood, 1978). If this is correct rare aposematic forms will always be selected against, and it is hard to see how a gene for aposematic coloration could spread in any population. To resolve this problem it has been suggested that kin selection is necessary for the evolution of aposematic coloration (Fisher, 1930, 1958; Benson, 1971; Turner, 1971, 1977; Harvey and Greenwood, 1978). In fact, this view has been so persuasive that the very occurrence of aposematic animals is often referred to as evidence for the "existence" of kin selection in modern handbooks (e.g., Wilson, 1975 p. 124; Krebs and Davies, 1981 p. 21). However, when critically examining the literature it becomes evident that most recent papers deal with interactions between predators and variously colored artificial prey items (cf. Duncan and Sheppard, 1965; Morrell and Turner, 1970; Lea and Turner, 1972; Gittleman and Harvey, 1980; Gittleman et al., 1980; Schuler, 1980), or with experiments where predators are offered distasteful insects which have been killed prior to testing (cf. Brower, 1958a, 1958b, 1958c; Coppinger, 1969, 1970; Bowers, 1980). Therefore we conclude that the belief that kin selection is necessary for the evolution of aposematic coloration depends on the untested assumptioin that distasteful animals are killed during experimental tasting by predators. In fact there are several cases recorded in the literature where it is explicitly stated that aposematic prey are released unharmed after being tasted by amphibian (Butler, 1868, 1869; Belt, 1874 as quoted in Cott, 1940), reptile (Butler, 1869; Boyden, 1976; Johki and Hidaka, 1979), avian (Trimen, 1869; Swynnerton, 1926; Brandon et al., 1979; Jiirvi et al., 1981; SillenTullberg et al., 1982) and mammalian predators (Carpenter, 1921; Phillips, 1931; Brodie et al., 1979). However, in all of these cases the authors have made their observations on wild, or wildcaught, predators which may have learned to treat warningly colored animals with greater caution, thereby enhancing the probability that the distasteful prey will be released unharmed. To eliminate this possibility we handreared individuals of four different species of birds: great tits, Parus major, blue tits, Parus caeruleus, starlings, Sturnus vulgaris, and Japanese quails, Coturnix coturnix, and used them as predators on four different "life forms" of living aposematic insects: burnet moths, Zygaena filipendulae (Zygaenidae: Lepidoptera), larvae of the European swallowtail, Papilio machaon (Papilionidae: Lepidoptera) and the large white, Pieris brassicae (Pieridae: Lepidoptera), firebugs, Pyrrhocoris apterus (Pyrrhocoridae: Hemiptera), and ladybirds, Coccinella septempunctata (Coccinellidae: Coleoptera). In this paper we