The Problems

There are obvious benefits to bearing warning colors in a population of warning-colored prey. As noted by early naturalists like A. R. Wallace and later E. B. Poulton, experienced predators avoid warningly colored prey, and presumably the number of prey killed during the predators' education is lower than in the absence of signaling. These benefits are clear at the group level but are not so clear at the individual level, because the first warningly colored individuals in a population of cryptic (and noxious) prey suffer strongly increased predation. Indeed, novel warningly colored prey not only suffer increased detection by prospective predators, but also elicit no avoidance in the predators. Consequently, there is strong positive frequency dependence, putting novel rare warning signals at a disproportionate disadvantage against an established strategy (crypsis, or another already established warning signal).

How could warning signals evolve at all if the first mutants using this strategy are killed? Laboratory experiments using the "novel world" design (Fig. 2) show rather unequivocally that aposematic patterns cannot evolve gradually in unpalatable prey. Indeed, small increases in visibility in cryptic prey increased attack rates without enhancing learning. Similarly, deviant phenotypes in established warning patterns suffered stronger predation. Finally, rare conspicuous prey suffered disproportionate predation, even when presented in groups. Therefore, a gradual increase in conspicuousness towards aposematism seems unlikely. This means that the evolving population must undergo a sudden jump, both in phenotype (to get a pattern that predators categorize as a different item) and in numbers beyond a threshold frequency (to allow the local predators to learn about the new pattern). Once the new pattern has achieved the minimum frequency and phenotypic thresholds, positive frequency dependence helps the new mutant to spread in the population. Peak shift or other processes can then occur, increasing the conspicuousness or adding other components to the signal. How can these evolutionary leaps be achieved— or circumvented—by an incipient aposematic prey?

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