View - Kowalewski, M. - Virginia Tech

PALEONTOLOGICAL SOCIETY PAPERS, V. 8, 2002it is reasonably predicted that coevolution mayresult in inducible defenses as opposed toconstitutive adaptations.If trends in predation-related traits involveinducible, rather than constitutive, defenses, ourinterpretation of such trends is complicated.Although evolutionary trends in both constitutiveand inducible defenses result from predation, themechanism differs. In cases of consistently highpredation pressure, natural selection will actdirectly to favor constitutive defenses (Tollrian andHarvell, 1999). However, if predation has a variableor unpredictable impact, inducible defenses willbe favored; in that case, selection acts indirectlyby affecting the norm of reaction (Travis, 1994).As the degree and variability of predation changes,defenses may alternate between constitutive andinducible or perhaps be lost entirely, depending onconstraints. This may affect what direction andwhat rate an evolutionary trend might take.Most studies have focused on plasticity fromthe prey’s point of view, as a defense against itspredators. However, adaptive plasticity not onlyprovides a mechanism through which prey mayavoid predation, but, in turn, may give predators theopportunity to respond reciprocally to overcome theprey defense. Thus, inducible defenses may havethe potential to alter both the short-term dynamicsand long-term evolution of predator-prey systems(Adler and Grunbaum, 1999; Harvell, 1990).However, it is unclear if in the long run predatorswould still exact primary “top-down” control indirecting the prey’s evolution as predicted by theescalation hypothesis (see also Vermeij, 2002).Communities that are dominated by generalizedpredators that are capable of switching amongdiverse prey, such as the crab Callinectes sapidusin marine soft-bottom habitats, often control thedistribution and abundance of a number of cooccurringspecies (Virnstein, 1977; Peterson, 1979;Hines et al., 1990).It is important here to distinguish reciprocalselection or within-generation change in phenotypedistribution from evolutionary reciprocal adaptation,which is a change in phenotype distribution acrossgenerations (Fisher, 1930). The conditions underwhich selection for induced prey defenses andpredator offenses operates in nature remain unclear.Is an inducible “dialogue” between predator andprey played out in ecological as well as evolutionarytime? If selection targets the norm of reaction ofboth predator and prey, coevolution may occur overthe long run (Smith and Palmer, 1994). There isexperimental evidence that partners in an interactioncontinually respond in a reciprocal fashion overecological time (Agrawal, 2001). Reciprocal changein ecological time may thus have resulted from longtermevolution in which the environment (the speciesinteraction) has been variable.FINAL REMARKSThere are two major underlying themes of thispaper. Our first goal was to clarify the conceptualdifferences between coevolution and escalation.The major difference between the two processesis in the nature of selection (Vermeij, 1994).Escalation is enemy-driven evolution. In this view,the role of prey (with the exception of dangerousprey) is downplayed in arms races betweenpredator and prey. In coevolution, prey are linkedtightly to their predator and are thought to drivethe predator’s evolution. Janzen (1980) posed thequestion: “When is it coevolution?” to drawattention to the ways in which the process wasmisunderstood. Similarly, we ask: “When is itcoevolution and not escalation?” The answer to thisquestion depends on the predator-prey system ofinterest. The naticid gastropod predator-prey systemwas initially envisioned as a coevolutionary system(Kitchell et al., 1981), but fossil evidence supportsan interpretation of escalation (Kelley, 1992). Insystems in which prey are dangerous to the predator,coevolution is the appropriate model (e.g.,confamilial naticid predation; Dietl and Alexander,2000; Busycon whelk predation on bivalve prey suchas Mercenaria; Dietl, in review). However, even inthese coevolving systems, the role other enemiesplay in reinforcing the selection pressure exactedby prey should not be overlooked—evolution doesnot take place in an “ecological vacuum” (sensuBoucot, 1983) even when considering a coupled368