Is Coevolution Dead

Bernays and Graham pose two main alternative explanations for the commonness of host specialization in herbivorous insects: coevolution, and variability among plant species in the abundance of associated predators and parasitoids. Their suggestion that predator/parasite pressure deserves more consideration as a cause of specialization is laudable and should stimulate research in this underexplored area. However, their arguments against coevolution as a major cause of specialization raise several questions that need examination. There seem to be two ways by which the process of coevolution can favor specialization. The first is that coevolution inhibits broadening of the host range and thus keeps specialist species specialized. The argument here is presumably that by becoming more and more finely tuned to exploiting a single host plant, an insect may sacrifice the ability to broaden its host range in the future because it becomes less and less adapted to using other hosts. This loss of adaptation to one host in conjunction with increased adaptation to another implies the existence of trade-offs in adaptation to different hosts (Gould 1979, Rausher 1984, Via 1984, Futuyma and Philippi 1987). The second possibility is that coevolution actively narrows host range. Under this scenario, coevolution occurs between a somewhat generalized insect and one of the plants it uses. Selection imposed by the herbivore leads to the evolution of defenses in that plant, to which the insect can in turn respond in any of three ways: (1) by evolving counter-resistance; (2) by evolving avoidance of that plant; or (3) by doing neither (1) nor (2). Alternatives (1) and (3) involve no change in degree of behavioral specialization. Alternative (2), however, results in greater specialization. Bernays and Graham seem to argue that accumulating evidence indicates neither of these possibilities commonly occurs in nature. I believe that the three arguments they put forward are not entirely convincing. Their first argument is that coevolution has not commonly led to avoidance because many feeding deterrents have no harmful physiological effects when ingested. That a compound is a deterrent means that an insect has evolved behaviorally to interpret that cornpound as a signal that the plants(s) containing it are poor substrates for survival and reproduction. They may be poor substrates for several reasons: (1) the deterrent itself is toxic; (2) some other chemical in the plant is toxic or inhibits growth; (3) some other nonchemical character of the plant (e.g., toughness, trichomes) renders it a poor substrate; or (4) some aspect of the plant's microenvironment (microclimate, enemy load) is inimical to the herbivore. Situations 1-3 may all arise as a result of coevolution, i.e., as a result of the herbivore selecting for resistance factors. Even situations of type 4 could be caused by coevolution, as when selection for extrafloral nectaries increases the number of predators/parasites in the vicinity of a plant. Simply ruling out situation 1 does not, therefore, rule out coevolution as a major factor leading to reduction in the quality of a particular host and consequent evolution of avoidance of that plant by the herbivore (specialization). Bernays and Graham's second argument is that coevolution cannot commonly cause behavioral specialization, because insects seldom impose strong selection on plants and therefore co-evolution seldom occurs. It may be true, as they argue, that herbivorous insects are relatively rare. However, rarity may often be a result of the prior evolution of resistance mechanisms by plants. Remove those resistance mechanisms and herbivorous insects might become much more common, sufficiently so to generate the selection required for the evolution of resistance factors (Janzen 1979). Moroever, many studies have documented substantial reductions in plant growth rate, survivorship, and reproductive success caused by insects (Cantlon 1969, Morrow and Lamarche 1978, Rausher and Feeny 1980, Parker and Root 1981, Louda 1983, Marquis 1984). These studies do not demonstrate selection, since they do not demonstrate that plant genotypes that differ in susceptibility to herbivores also differ in fitness. However, they do indicate that the potential for intense selection by insects on plants is frequently present in nature. The only way to support or refute the contention that herbivores commonly exert important selection pressures on resistance traits is to measure selection and determine its causes directly. Such attempts are