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DIETL AND KELLEY—PREDATOR-PREY ARMS RACEScoevolution do not consider the process ofselection. “In order to make headway in the studyof coevolution and escalation, we need to studythe sources, frequencies, and cost-benefit effectsof selection. This entails careful observation ofencounters between species, together with anevaluation of the effects of such encounters onsurvival and reproduction” (Vermeij, 1994, p. 232;see also Herre, 1999, and below). It is importantto distinguish when selection occurs and whatagents are responsible (Vermeij, 1994). For aninterpretation of reciprocal adaptation to beappropriate, selection by the prey on its predatorhas to be stronger—with predictable consequences(Brodie and Brodie 1999)—than that caused byother enemies of the predator.Inequalities in interaction.—Slobodkin’s(1974) expectation that prey in an evolutionary racecan “keep ahead” led Dawkins and Krebs (1979)to point out that coevolution (reciprocal adaptation)between predator and prey gives the prey aninherent evolutionary advantage. Thus predator andprey are not equal partners from an economic pointof view in an arms race. They termed thisasymmetry in the evolutionary outcome betweenpredator and prey the “life-dinner principle.” It isa widely cited explanation for why predators maynot respond evolutionarily to prey adaptation(Vermeij, 1982b; Kelley, 1992; Brodie and Brodie,1999). If a predator fails, it only loses a meal (andsome energy and time), whereas failure for the preymeans death (or at least injury). The consequencesof the interaction clearly are more severe for theindividual prey, suggesting that selection by thepredator on the prey for improved defenses isstronger than selection by the prey on the predatorfor improved offensive capabilities. Asymmetry inselection is assumed to result in faster evolutionof prey than predators, leaving predators unable tokeep pace (in the evolutionary race) with their prey.Vermeij (1982b) reasoned that the prey’scontribution to selection for improved predatorcapability is further reduced if a predator preys onmore than one species; the short-term response ofthe predator might be to avoid the increasingly welldefendedprey. Vermeij (1982b) took this to implythat selection for predatory improvement is likelyto be far stronger from the predator’s own enemiesthan from its prey; thus interactions among multiplespecies decouple the coevolutionary responses of agiven pair of species. This was the major impetusfor the formulation of the escalation hypothesis andits view that prey play a minor role in directing theevolution of their predators.Dawkins (1982) proposed the “rare enemyeffect” as a means of balancing the asymmetryinherent in the life-dinner principle and allowingcoevolution to occur. Because rare predatorsrepresent a minor selection pressure on the prey,the predators are thought to “win” or “keep ahead”in the arms race (Dawkins, 1982). However, if apredator is rare, the risk of predation for anyindividual prey is low, and the prey would not beexpected to evolve costly morphological oravoidance defenses. If selection pressures on theprey are weak, coevolution of predator and prey isdifficult to envision (see also Abrams, 1986). Insuch a case, an opposite asymmetry may arise inwhich the prey do not respond to evolution of therare predator.Abrams (1986) has argued, on theoreticalgrounds, that the life-dinner principle does not takeinto account the fact that if a predator loses enoughraces, it will also lose its life. Predators that rarelycatch prey will suffer the same fate (death) as anunsuccessful prey individual. Furthermore, thefrequency or probability of attacks, as well as theiroutcome, has to be taken into account indetermining the net lifetime effect on survival,reproductive output, and fitness. The cost perunsuccessful attack is typically low for predators,but predators typically have a low success rate andmust make many unsuccessful attacks for everysuccessful one. In contrast, the cost to a prey ismuch higher, but the number of attacks experiencedper individual may be much lower over a lifetime.Thus, even though the consequences of oneindividual attack are highly asymmetrical betweenpredator and prey, the net outcome is not readilyobvious (J. A. Rice, pers. comm., 2002).In addition, Brodie and Brodie (1999) pointedout that the life-dinner principle, as formulated,361