Natural Selection and Communication Among Bark Beetles

Natural Selection and Communication among Bark Beetles Author(s): John Alcock Source: The Florida Entomologist, Vol.
65, No. 1 (Mar., 1982), pp. 17-32 Published by: Florida Entomological Society Stable URL: http://www.jstor.org/stable/3494143 . Accessed: 24/04/2013 08:43
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Insect Behavioral Ecology-'81 Alcock NATURAL SELECTION AND COMMUNICATION AMONG BARK BEETLES
JOHN ALCOCK*
17
It is populations, not individuals, of bark bettles that have created problems for the forest manager. Moreover, populations of these insects have generally proven to be remarkably resilient despite the best efforts of humans to control them. It is not surprising therefore that entomologists who have studied bark beetles have come to think of the population as the primary biological unit and have, perhaps grudgingly, grown to admire the seemingly adaptive properties of the populations they have studied. This view has led, however, to a tendency to interpret the behavior of individual beetles as adaptations that have evolved to promote the reproductive welfare of the group. By many entomological accounts, bark beetles are paragons of cooperation who work together to achieve "reproductive efficiency" for the population as a whole (e.g. Renwick and Vite 1969, Shorey 1973, Wagner et al. 1981) while at the same time preserving variant behaviors for future species-threatening contingencies (Atkins 1980). The following paragraph from a recent paper by Coulson (1979) is representative of this attitude: "Since high costs in the form of mortality to adults are undoubtedly associated with the search for relatively rare susceptible hosts, and as elaborate communicative mechanisms have evolved to enhance this search, it is reasonable to assume that behavioral mechanisms also exist that are directed to the efficient utilization of the basic habitat unit. Under-utilization would affect the chances of assembling a sufficiently large population to colonize new hosts in the next generation. On the other hand, over-utilization would result in mortality in the form of intraspecific competition between later life stages for food and perhaps habitat." Coulson seems to be saying that bark beetles cooperate in calling each other to rare food sources where they will space their nest burrows so as to use the host tree completely and yet regulate the number of progeny they produce so as to prevent over-population of the tree. This is done supposedly to maximize the number of recruits for the next generation, and thereby reduce the risk of extinction of the species. This paper will argue that the assumption of a population benefit as the evolutionary basis for cooperation is totally unjustified because it so completely violates what is currently known about population genetics and the evolutionary process. The goal of this paper will be to construct reasonable explanations for the behavior of bark beetles that are consistent with a modern understanding of genetics and natural selection. I shall employ the now almost universally accepted working hypothesis of evolutionary biologists that behavioral traits must in some way help individuals reproduce as successfully as possible in the face of competition from their fellow beetles and other utilizers of the food in certain trees. I hope to show how this approach is thoroughly different from the "good of the group" hypothesis (Alexander
of Zoology at Arizona State University. His research centers *John Alcock is a Professor behavior of solitary bees and wasps but he has also published on a variety on the reproductive An of other insects. His book, Animal Behavior, Evolutionary Approach (Sinauer, 1979 2nd of Zoology, Arizona State UniverEd.) is popular in its field. Current Address: Department sity, Tempe, AZ 85287.
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1975, Lloyd 1979) and I intend to reevaluate the pervasiveness of cooperation in these beetles.
THE DECLINE AND FALL OF GROUP SELECTION
It is entirely true that many species have become extinct and this naturally leads to the deduction that living species must have some properties that have enabled them to avoid this fate. The logic of this deduction sustained biologists for many years in the uncritical acceptance of the proposition that traits have evolved to further the interest (i.e. survival) of the species as a whole. The culmination of this philosophy was V. C. WynneEdwards's (1962) book that championed the argument that group selection,
the differential survival of populations (based on genetic differences among them), was a major mechanism for evolutionary change'. His basic theme was that species that failed to regulate their numbers were more likely to become extinct than populations that could sustain themselves at some optimum level (one that was not so high as to run the risk of exhausting key resources on which the species depended). Wynne-Edwards believed that if it were to a population's survival advantage for its members to reduce their reproductive output, then such self-sacrificing traits would be maintained by group selection because of their species-preserving function. But as many authors have shown since 1962, none better than G. C. Williams (1966), group selectionism a la Wynne-Edwards is plagued by a fatal flaw. Consider a population composed of individuals that fail to realize their reproductive potential so as not to exceed the population size most congenial for the long-term survival of the species. A population of this sort would be vulnerable to invasion by a mutant individual that practiced reproductive maximization. The genes of this individual and his descendants should become increasingly common over time by outreproducing the reproductive self-sacrificers. If this situation persists, natural selection would inexorably eliminate the genes that are "good for the group" even if in the long run their presence might prevent extinction of the species. It is the relative number of surviving offspring produced by different genotypes that determines the frequency of competing alleles in the next generation, not the value of an allele to the preservation of a species. It follows therefore that the working hypothesis for an evolutionary biologist must be based on individual selection, namely that an animal's traits should contribute to individual reproductive success and that any benefits to the group as a whole are purely incidental effects. This holds even in cases that superficially appear to promote group cooperation and "reproductive efficiency". An excellent example is the case of synchronous flashing by populations of male fireflies. Lloyd (1971, 1973a,b, 1977) has shown that group formation by males and synchrony in flashing can occur because asynchronous or isolated males are unattractive to females and so will fail to reproduce. Individuals engage in group behavior in order to compete more effectively for the opportunity to communicate with potential mates. Despite examples of this sort and despite 15 years in which Williams's critique of group selectionist thinking has been widely accepted, there persists the temptation to interpret animal behavior as designed (evolved) to prevent the extinction of species. This temptation is particularly strong in cases in which signaling individuals are found in groups. To counteract this
Insect Behavioral Ecology-'81 Alcock
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temptation let us consider the reproductive consequences for individuals that participate in a communication system (Otte 1974, Lloyd 1977).
WHAT IS COMMUNICATION?
The odors emanating from a bark beetle can be detected by others who may use the information in various ways. For example, one bark beetle may be drawn to the odor of another and establish a burrow near the sender. Through their association the two may gain an advantage in overcoming the toxic or entrapping defenses of the tree they have selected to colonize. Such a case of mutual reproductive benefit is very different from the interaction that occurs when the same bark bettle odors are perceived by predatory clerid beetles. Here the clue (bark beetle odor) has a negative reproductive effect on the sender (as it may result in its death) while enhancing the fitness of the predatory receiver. The reciprocal effect is also possible, with the producer of a cue gaining at the expense of the respondent. (An example are those predatory female fireflies that mimic the attraction signal of a female of another species in order to draw males of the prey species to them). Otte (1974) claims, and I agree, that in interactions in which either the signaler or receiver is harmed, exploitation rather than communication occurs. The exploiter can either detect a cue associated with its victim or provide a mimetic signal that resembles a communication message normally used beneficially by the receiver. Any definition of communication is of course a semantic issue but, however labelled, there is a real and significant distinction between cues (signals) that have a positive effect for both signaler and receiver as opposed to those with a benefit for just one interactant and a negative reproductive effect for the other (Table 1). Only when both those that release and those that respond to a cue gain from the interaction will individual selection favor the maintenance (and further elaboration) of the (communication) system. If signalers are consistently damaged by the release of their signal, selection will favor mutants that happen not to produce the reproductively disadvantageous "message" for their exploiters' benefit. Likewise, if the fitness of a receiver is on average reduced by reacting to a
TABLE
1. SOME MAJOR POSSIBLE EFFECTS ON THE REPRODUCTIVE SUCCESS OF AN INDIVIDUAL THAT PRODUCES A CUE AND AN INDIVIDUAL THAT RESPONDS TO THAT CUE.
Reproductive Effect Emitter +

+
Definition of Interaction Communication: Both interactants gain Deceitful Exploitation: The signaler induces the receiver to do something that harms the receiver but benefits the signaler Eavesdropping Exploitation: The receiver takes advantage of a cue provided by the signaler and reduces the signaler's fitness in the process
Receiver
+ -
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signal, individual selection will favor others in the population that happen not to be responsive to the damaging cue. With this argument in mind we shall consider the effects of bark beetle "communication signals" on the fitness of individuals participating in the system. Instead of assuming that the function of a signal is to promote the welfare of the group, we shall approach the matter with skepticism and an alertness to the possibility of exploitation and competition rather than uniform cooperation2.
THE LIFE HISTORY OF Dendroctonus
pseudotsugae
In order to make our analysis more manageable, the discussion will focus primarily on one bark beetle species, D. pseudotsugae, whose behavior has been unusually well studied thanks to the work of Julius Rudinsky and his associates (Rudinsky 1969, Rudinsky and Michael 1974, Rudinsky and Ryker 1976, 1977, Rudinsky et al. 1976, Ryker in prep.). All of the major communication signals exhibited by this species have been found in other bark beetles (see Nijholt 1970, Wood 1973, Vite and Francke 1976) and so its behavior can be taken as reasonably typical of the group and used to illustrate some points about the evolution of communication in these insects. It is the females of D. pseudotsugae, not the males, that first colonize a host tree in the spring in the northwest. Often the tree selected is a recently dead or dying Douglas fir but the beetles have the capacity to attack living, healthy trees as well. When the female burrows into the bark of the tree to reach its nutritious phloem she innoculates the host with a fungus that invades the water transport system of Douglas fir. If sufficient colonists attack the tree it will die even if it was healthy originally. Large numbers of colonists do sometimes assault a host in a very short time (up to 15,000 settlers in one day). Mass attack occurs because as females form their galleries in the bark, the tree becomes far more attractive to flying beetles searching for a host. The incoming beetles detect a complex bouquet of odors from the exereta and debris in the burrows of the already established females. These frass chemicals include frontalin, methylcyclohexenol, and methylcyclohexone (MCH) as well as volatile monoterpenes "released" by the host tree. These combined substances attract both males and additional females when MCH is present in low concentration. The new females find unoccupied places to burrow into the tree; the arriving males search for females to court. When a male finds a burrow producing MCH in relatively low concentration he approaches the entrance, stops, and chirps by rubbing his abdomen against his elytra. This is the first stage in courtship that may lead to copulation and pair formation (the male may remain with his mate to guard her and to help remove the products of gallery formation from the burrow). During courtship both the female and the male release large quantities of MCH. At high concentrations, MCH no longer acts synergistically with the other attractants of the pheromone mixture but instead inhibits the arrival of new settlers. In a densely infested region of a tree with many pairs of mated beetles, the amount of MCH present becomes high with the result that this region is no longer attractive to incoming females or males. Thus MCH can be said to act (1) at low concentrations as an aggregation pheromone that attracts beetles of both sexes, and, at high concentrations, as both (2) an anti-aggregation pheromone that deters additional fe-
21
male settlers, and (3) a masking pheromone that blocks the response of males to the female pheromone. Let us look critically at each of these supposed communication functions to determine if they are compatible with what is presently known about genetics and selection. PHEROMONE THE AGGREGATION In the insect literature generally (e.g. Cross 1973, Joose and Koelman 1979) and the bark beetle literature in particular, chemicals released by one individual are said to be an aggregation or attractant pheromone if members of the same sex are attracted to the compounds. In bark beetles pheromones of this sort are known from at least 17 species representing 5 genera (Wood and Bedard 1976). The use of the term "pheromone" implies that the released chemicals serve an evolved communicatory function which in the case of bark beetles is generally thought to be the formation of a sufficiently large attacking force to overwhelm the defenses of the host tree (Birch 1978). Not all supporters of this view have employed a group selectionist perspective (although statements such as those by Coulson (1979) to the effect that the beetles are cooperating in order to produce as large a next generation as possible imply that a group benefit is the primary function of the trait). Those researchers that have operated within an individual selectionist framework have proposed that through pheromonal communication both the signaling residents and responding recruits benefit reproductively through their combined efforts to destroy the defenses of the tree. Rigorous tests of this proposition have, however, rarely been done (but see Raff a and Berryman, in prep.) and there is reason for caution in attributing a cooperative goal for aggregating individuals. There are many cases of supposed "aggregation signals" in which either the signaler or the receiver clearly does not benefit from the interaction. For example, males of many insects are attracted by the sexual signals produced by other males (Table 2) and in these cases it is highly probable that the joiner is attempting to take advantage of the signaler. A famous case inTABLE 2.
EXAMPLES OF INSECTS IN WHICH MALES ARE KNOWN TO BE ATTRACTED BY THE SEXUAL SIGNALS PRODUCEDBY OTHER CONSPECIFIC MALES
Group Cicadas Katydid Trypetid fly Otitid fly Grasshopper Mole crickets Wasps Bee Beetles Pentatomid bug
Species Magicicada spp. Orchelium vulgare Dacus tryoni Physiphora demandata Syrbula fuscovittata Scapteriscus spp. Eucerceris spp. Euglossa imperialis Anthonomus grandis Tenebrio molitor Nezara viridula
Reference Alexander 1975 Morris 1971 Fletcher 1968 Alcock and Pyle 1979 Otte 1972 Ulagaraj and Walker 1973 Forrest 1979 Alcock 1975 Kimsey 1980 Hardee et al. 1969 Tschinkel et al. 1967 Harris and Todd 1980
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volves field crickets of the genus Gryllus in which some males are drawn to the vicinity of chirping conspecifics where they lie silently in wait to steal females attracted to the caller (Cade 1979, 1980). To label male singing an aggregation call simply because other males come to the singer would be misleading at best. The cricket's song has evolved to attract females to the singer. Both female receiver and male sender may benefit from the communication signal. But other males may exploit this system for their own advantage. By not singing a satellite male may avoid predators and parasites attracted by the call (another class of exploiters) while at the same time siphoning off receptive females that come to the singer. Thus the satellite gains (+ effect) but the signaler loses (-); the aggregative effect of the call on males is therefore an incidental by-product of what is functionally a sexual signal favored by individual selection because of its utility to the sender in male-female interactions. The attracted satellites impose a selective cost on the singing male that decreases the overall benefit of the calling behavior. Despite examples of this sort, the possibility that insects may be attracted to cues provided by others for the purposes of exploitation rather than cooperation has not been fully explored in the case of bark beetles. Let me assume the role of devil's advocate and suggest how the aggregation of females of D. pseudotsugae that results from the low level releases of MCH from resident females within a host could be rather more exploitative than cooperative. As noted at the outset, females of this and many other bark beetles usually attack dying trees. When this happens additional colonists do not help defuse the defenses of the host because the tree is already essentially helpless. The arrival of competitor females only reduces the food available for the brood of the established "signaler". Raffa and Berryman (in prep.) have shown that in D. ponderosae there is a strong negative correlation between density of attacks in cut (i.e. defenseless) logs and pupal production per female. Thus there is no gain for the supposed message sender but instead a loss3; the receiver benefits by taking advantage of olfactory cues associated with the colonist to locate a suitable host. This then is not cooperative communication in any meaningful sense of the word but exploitation of one individual by another. Why then do signalers produce an "aggregation pheromone" when in a "safe" tree? First, the costs of eliminating all volatile by-products of digestion may be so great (given that females must process large quantities of wood material through the gut and detoxify plant terpenes by creating new compounds-Renwick and Hughes 1975) that this disadvantage would outweigh any benefits gained by removing all cues as to the feeding females' location. Second, females do gain by attracting conspecific males. Low concentrations of MCH may be released for this purpose with female competitors exploiting the cue to locate a relatively safe food resource4. But what about those (relatively rare?) occasions in which some females colonize a healthy host with intact resin defenses. Under these circumstances it has been assumed, but only conclusively demonstrated for D. ponderosae (Raffa and Berryman, in prep.), that the risk of death from resin entrapment is reduced for the original settler (or her progeny) if she is joined by other females. If we accept this hypothesis as applicable to D. pseudotsugae as well, then an early colonizer will benefit if it draws additional females to
23
its living host. But will the respondents also gain? It could be that on average females gain by flying to sources of dilute MCH because on average the host tree discovered in this way will be dead or weakened. But when the tree is healthy and in the earliest phase of attack, the risk of death from resin flows will be relatively high. It is at least possible that under these conditions joining the signaler does not maximize the reproductive chances of a settler. Perhaps the initial colonists of a healthy tree exploit dispersing females to make the tree safer for them at the expense of those they attract to the host. In this context it may be significant that females of the mountain pine beetle, Dendroctonus ponderosae, produce more aggregation pheromone when burrowing in hosts that have relatively large amounts of protective resin (Vite and Pitman 1968, Raffa and Berryman, in prep.). In contrast, when a female finds a safe host she may gain if she can reduce the rate of colonization to some degree. This assumes that the first successful colonists can realize greater reproductive gains than latecomers as demonstrated for D. ponderosae (Raffa and Berryman, in prep.). The sooner a female produces her young, the larger they will be relative to the progeny of later arrivals, and the greater their competitive edge in the race to consume the limited supply of host phloem. Thus for a safe host, reduced amounts of "attractant" may be released. On the other hand, but for a dangerous one, residents with a tenuous foothold on the tree may gain by "amplifying" the cues that indicate the host is being utilized so as to lure additional females to the site. Joiner females should benefit if they can avoid exploitation and therefore are predicted to prefer safe hosts (if these are available and the females have the energy and time to find them). The fact that colonization rates are not a simple linear function of the number of resident beetles in a tree supports this prediction. Over the first few days of colonization of a host the number of new recruits is relatively low but once the population of residents reaches a certain level there is an explosive take-off in the number of beetles attracted to the tree (Gieszler et al. 1980). The number of new females of D. ponderosae settling on a living host per established female rises steeply until the attack density reaches about 40 females per square meter after which the attracted females to established female ratio collapses rapidly (Raffa and Berryman, in prep.). The 40 female figure is the density that insures the death of a living lodgepole pine; only females within dead wood succeed in rearing offspring. Thus mass attack, with relatively many females attracted per established colonist, occurs when the concentration and perhaps quality5 of the aggregation pheromone indicates to potential joiners that their chances of living and producing viable offspring are good given the number of already established beetles.
THE SIGNIFICANCE OF MASS ATTACK
Advocates of the "cooperative beetle" hypothesis have focused primarily on just one phase of the colonization of healthy trees (the mass attack) while ignoring interactions that take place in the very earliest stages of colonization, as well as the interactions that occur on trees that are dead or dying from causes other than the beetles. But even during mass colonization of a healthy tree the emphasis on cooperation may have been overdone. As the firefly example illustrates, synchrony of action does not automatically
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justify a conclusion of cooperation for group benefit. It is true that by joining in a mass attack newcomer females contribute to the speedy demise of a living tree. But this may not be their primary goal. Raffa and Berryman (in prep.) have shown that in colonizing a living tree there is a trade-off between getting in too early (and thereby risking death) and getting in too late (and thereby attempting to reproduce in a tree whose resources will be depleted before one's progeny can reach maturity). An early colonist who survives may do very well because of the competitive advantages of its offspring; a late arrival may have a low probability of dying from resin entrapment but also a low probability of finding a productive region of the tree. Mass attack may be the consequence of individuals racing to take advantage of a relatively safe and relatively productive resource before their fellows have exploited it.
THE ANTI-AGGREGATION PHEROMONE: FEMALE SIGNALERS AND FEMALE RECEIVERS
As the number of colonists increases on a healthy tree there will come a point (probably quite early in the attack) when any gains to the resident signaler from attracting more females are outweighed by the reduction in her production of surviving brood caused by increased competition for food. Thus although attractive signalers might benefit very early in the infestation, the effect of releasing the "aggregation pheromone" eventually must become negative for them (Table 3). Established females would seem to have everything to gain if they could prevent the arrival of additional colonists at the point when new settlers reduced their reproductive output. Females of D. pseudotsugae do release large quantities of MCH when contacted by a male and this substance does tend to inhibit settling by bark beetles. When many resident females are releasing MCH, incoming females are usually repelled and will land elsewhere on the host or nove to neighboring trees or continue dispersing farther still. The discoverer of this effect, Julius Rudinsky (1968, 1969), called the released MCH a "masking pheromone" implying that females altered their attractant pheromone to make it less readily detected by incoming females. This interpretation has been adopted by Matthews and Matthews (1978) in their recent text on insect behavior which states that by releasing MCH the resident female is "camouflaging the normally attractive odor she has produced in her frass". But if this were TABLE
3. POSSIBLE FITNESS EFFECTS FOR A RELEASER OF AN "AGGREGATION PHEROMONE" AND FOR AN INDIVIDUAL THAT RESPONDS POSITIVELY TO THE ODOR.
Fitness
Effects for
Stage of Infestation
of a
-Releaser of Odor
+ + + 0 or +
-Attracted Individual
+ or + ++ +
Tree with Intact Defenses

Very Early Early Middle Late Very Late
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true it raises two questions. First, why doesn't the signaling female simply cease to release the assembling scent instead of producing a specially altered signal. By not providing any signal at all a female would not have to manufacture and store MCH in quantities prior to its release and she would not provide a cue which could alert dispersing beetles to the location of a host. Second, why do female receivers fail to detect MCH or permit themselves to be repelled from a region of a tree by concentrated MCH? Let us deal with each question in turn. There are at least two problems with the no-pheromone option. First, as noted earlier, it is doubtful that a female could remove all volatile traces of her activity without incurring high metabolic expenses especially if the attractant cues are detoxification by-products. Second, because trees are colonized unevenly, heavily infested regions may be adjacent to sections that are lightly attacked. The interests of the beetles in the two areas may be in conflict. In the low density locale individuals might gain by attracting additional colonists. They would release aggregation pheromones that would draw other beetles to the tree, some of which might settle in the pheromoneless area, having no way to discriminate fully occupied from non-occupied sectors of the host. Therefore it is to the advantage of resident females, even after mating, to continue to provide an unequivocal signal of their presence, provided that this deters additional settlers. But why are additional settlers deterred? Rudinsky (1969) writing in an era when the difficulties with group selectionist thinking were not widely appreciated stated, "The survival value of the mask is clear. It tends to distribute evenly the available males, while both preventing overcrowding with resultant brood mortality and allowing the mass attack necessary to overcome host resistance." But if it were not to the reproductive advantage of signaler to provide the signal and advantageous for the receiver to respond by avoiding the MCH source, then the system would break down, whatever its group benefits. Perhaps the large release of MCH serves first to announce to the chirping male that the female is potentially receptive. Secondarily it provides a cue that other individuals might use to modify their own behavior for their own advantage. MCH concentration offers a measure of population density in the host which arriving females can use to assess their reproductive chances. By releasing additional MCH after contacting a male, a resident female (whose sexual peromone has done its job of attracting a mate) may be attempting to make her site appear more crowded than it actually is and so less attractive to would-be colonists. The fact that females automatically release quantities of MCH upon hearing a male at their gallery entrances, apparently without respect to population density in the host, suggests to me again that the primary function of MCH is sexual. Otherwise we would expect that population density, not the arrival of a male, would determine whether or not the female continued to produce the "aggregation bouquet". The deterrent effect that MCH has on arriving beetles may occur because it is generally in the reproductive interests of the dispersing beetles to avoid settling in trees with few remaining resources. The degree to which a joiner gains by landing on a host is largely a function of the current population density there which determines the food available for its progeny. The degree to which signaler and joiner probably gain varies depending on the
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stage of attack and need not be equal at any time (Table 3). Some individuals may join relatively crowded trees because they have in some way determined (unconsciously) that their chances of finding a superior host are slight-either because hosts are extremely rare, or the risks of dispersal are great, or their physiological condition makes prompt settling desirable. Therefore some individuals could gain reproductively by landing on a high density host, even though their reproductive success will be less than if they had found an ideal tree and even though their decision to colonize adversely affects the reproductive success of their neighbors (Table 3). In living lodgepole pine the density of attacking D. ponderosae regularly exceeds 60 females per m2 which is the point at which pupal production per female begins to decline sharply (Raffa and Berryman, in prep.). But if the reproductive chances of a female are nil if she were to land on a fully settled host or if her alternative options are profitable, then it becomes to her advantage to use information about colonist density provided by the MCH signal to avoid certain trees. When the reproductive interests of the signalers and receivers coincide, MCH does function as an antiaggregation pheromone, but it is important to recognize that the interests of the two classes of interactants will only be the same under rather special conditions.
THE ANTI-AGGREGATION PHEROMONE: AND MALE RECEIVERS MALE RELEASERS
The same argument applies to the release of MCH by males (after they reach a female's burrow) and to the response of conspecific males to the MCH stimulus. To the extent that this augments the female's MCH signal, the male's action can be seen as a contribution to the repulsion of additional female settlers whose presence would reduce the reproductive success of his mate and so reduce the number of his progeny. It can be argued that the male signal is also a "mask" directed at other males that counteracts the attractant fraction of the female's odor thereby reducing competition from rival males. This function has been ascribed to the release of a male pheromone in the case of the armyworm Pseudaletia unipuncta by Hirai et al. (1978). They perceived a group benefit of the behavior because the male that released the "inhibitory pheromone" was promoting "the increased reproductive efficiency (that) results when multiple males are prevented from competing for a single female." Both the group selectionist hypothesis of Hirai et al. (1978) and the hypothesis that individual males gain by hiding receptive females from other males have a logical flaw. If it were not to the reproductive advantage of a male receiver to be "inhibited" from approaching the source of male pheromone, then individual selection would favor those males that responded differently. Thus male MCH probably is not a masking pheromone but a clear signal to would-be competitors that the signaling male is near a receptive female. This repels approaching males because a female with a male guard is unlikely to be easily secured. In D. pseudotsugae males defend their mates vigorously and it is probable that the first male to enter a female burrow has a substantial advantage over later arrivals. Even so, fights do occur (Rudinsky and Michael 1974, Ryker, in prep.) indicating that males will sometime not avoid concentrated MCH if they can gain by ap-
27
proaching the source (that is, if they can determine that their opponent is relatively weak or small and if the option to continue the search for an unsecured female is not likely to be productive). Often, however, potential male joiners gain by moving on when they receive the MCH signal and thus the release of the compound and the "typical" response to it have positive fitness effects on both sender and receiver of the message.
CONCLUSIONS
Since individual beetles are the product of natural selection and therefore attempt to reproduce as much as possible, our view of bark beetle communication must take on a distinctive character. If nothing else I have tried to suggest that the interactions between resident beetles and attracted joiners could be much more complex (and more interesting) than one would conclude from the "cooperative beetle" hypothesis. There is little doubt that bark beetles do sometimes communicate with pheromones and do sometimes achieve mutualistic goals as a result (Raffa and Berryman, in prep.). But the perspective presented here argues that they do so only when certain conditions enable them to use and respond to signals in ways that further their individual reproductive interests. Beetles that gratuitously raise the reproductive success of others while damaging their own reproductive chances are not likely to be long represented in the gene pool of the species. I am confident that future research on bark beetle communication will confirm that reproductive competition is at the heart of the interactions among individual beetles and that the animals possess the ability to adjust or vary their signals and responses in subtle but adaptive ways. Those interested in controlling populations of bark beetles can take comfort in the recognition that they are not opposed by a monolithic cooperative pest all of whose members are working and sacrificing for the common goal of population growth. Instead the enemy is composed of reproductively selfish individuals that may attempt (unconsciously of course) to exploit their fellow beetles. Ideally it would be possible to control bark beetles by using their evolved abilities against them. Thus the tactic of releasing large amounts of synthetic MCH over trees vulnerable to D. pseudotsugae appears promising because it exploits the adaptive (reproductively selfish) tendency of receivers to avoid crowded areas with low reproductive potential (Ryker, in prep.). At the same time, this and any other system of control based on manipulation of the animal's communication network must contend with some problems. First, not all individuals can be expected to respond identically in releasing pheromones or responding to a given concentration of aggregation or anti-aggregation pheromone. An intriguing and plausible possibility raised by Raffa and Berryman (in press) is that the genetic make-up of individuals in some bark beetle populations may undergo cyclical changes in response to fluctuations in overall population size. In populations that have reached epidemic proportions, selection may favor females that have a low threshold for settling in living trees. The odds are good that some females from the very large pool of dispersing individuals will also settle in the tree and help render it defenseless. The progeny of these colonists will profit from the thick phloem of the once vigorous tree. But during the low population phase of the "cycle", selection would favor highly discriminating females that were
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reluctant to settle in all but the "safest" of trees as the probability of acquiring the additional recruits to defeat a healthy tree are slim at these times. Thus host discrimination responses may not be static at all but instead could be a dynamic reflection of fluctuating selection pressures. In addition, any one beetle may be able to adjust its signal release or signal reaction depending upon the conditions it encounters or has experienced. Only one-fifth of the females of the southern pine beetle that land on apparently suitable hosts actually burrow into the tree during the mass attack phase (Burt et al. 1980). This may be due to genetic differences or environmental and experiential differences among the females. Likewise as many as one-half of the western pine beetles that establish galleries in trees may subsequently emerge again (presumably after reproducing to some extent) to disperse to other trees. This suggests that the beetles may be able to alter their tactics even after seeming to commit themselves to one course of action (Wood and Bedard 1976). I have little doubt that the same kind of intra-specific variation in behavior occurs with respect to the anti-aggregation pheromone. Control programs that are based on the typological thinking that there is one standard response by all members of a target species to a particular situation or signal are therefore unlikely to succeed. Variation among individuals and the behavioral flexibility of specific beetles create a kind of "resistance" that could thwart even sophisticated biological control measures just as thoroughly as insecticide-resistant mutations have sabotaged chemical control efforts in some cases. For this reason it is unfortunate that the attempt to document the degree of behavioral variation within a species and the range of options open to individuals has barely begun in bark beetle research (but see Raffa and Berryman, in prep.). As these features of bark beetle communication are discovered it will be important to explore the adaptive basis for the variation. Do individuals of different age, size, potential fecundity, and past dispersal experience react differently to aggregation and anti-aggregation cues in ways that promote their reproductive success? Do individuals react to living, damaged and dead hosts in different ways? Does the abundance and pattern of distribution of potential hosts correlate well with differences in signal and response behavior? If the beetles are as adaptively flexible and variable in their behavior as I suspect, then they will in many respects be a more formidable foe than one composed of individuals all of whom follow a single route of sacrifice for group success. In the long run an awareness of how individual beetles achieve reproductive success in a variable and socially competitive environment should contribute to the development of measures that will have a better chance of truly controlling bark beetle populations.
ACKNOWLEGEMENTS
Participation in this symposium was funded in part by a U.S. Department of Agriculture-sponsored program entitled "The Integrated Pest Management R & D Program for Bark Beetles of Southern Pines", Forest Service Southern Station Cooperative Agreement 1981-8 with the University of Florida. Dr. Randy Thornhill sent me a pre-publication copy of his manuscript (written with L. Kirkendall) that assesses "aggregation signals" in a similarly skeptical fashion. Dr. Kenneth F. Raffa provided a copy of Raff a
29
and Berryman (in prep.), a paper I found extremely valuable. Dr. Lee C. Ryker and Dr. James Lloyd provided help with the literature search and constructively reviewed the manuscript as did Dr. Ron L. Rutowski. I especially thank Dr. Lloyd for inviting me to the symposium and Dr. Ryker for his generous and knowledgeable assistance with matters pertaining to bark beetle behavior.
APPENDIX
'In order for group selection to occur within a species, three conditions must be met. (1) Certain groups within the species must survive and others must become completely extinct. (2) There must be genetic differences between the two categories of groups. (3) These genetic differences must contribute to the differences in the probability of survival of a unit. Under these restrictive conditions it is theoretically possible for the differential survival of groups to lead to changes in the frequency of competing alleles within a population. Most workers feel however that these requirements for group selection are not often met. More importantly still, selection at the individual level should almost always successfully counteract group selection when group selection happens to favor genetically self-sacrificing behavior. In other words, an allele favored by group selection can be eliminated by individual selection (see the text), leading to the conclusion that individual selection is the more potent force for evolutionary change. 2Communication is a special form of cooperation. Cooperative behavior of all sorts can evolve through individual selection but only if the participants generally gain more reproductively than they lose by assisting the other individuals with whom they are interacting. Special circumstances are required if a helpful action is to lead to mutual benefit and therefore any hypothesis that a behavior is truly cooperative deserves special scrutiny. 3In some species of bark beetles additional colonists may help the signaler even if they cannot reduce the danger from the tree's defenses. The gain could come from overwhelming the consumption capacity of the local predators, thereby reducing the risk of attack for any one resident. But little evidence exists on whether established residents experience great mortality from their enemies. Another possible benefit for the resident that attracts additional colonists of its species occurs when there is interspecific competition for the tree's resources. When two rival species occupy the same host in equal numbers, larval survival for both may be severely reduced (Birch 1978). This could favor individuals that can attract sufficient numbers of conspecifics to make the tree unattractive to members of other species (but only if conspecific juveniles are less damaging than those of other species). Interspecific interactions based on chemical signals are common among bark beetles (e.g. Birch 1978; Birch et al. 1980). 4The work of Brand et al. (1976) showing that an aggregation pheromone component (verbenone) is produced by a fungus in D. frontalis raises the possibility that bark beetle pheromones are produced by the insect's gut flora and fauna for the benefit of these fellow travelers (Birch 1978). It is not unlikely that the survival and reproduction of the fungus is facilitated in trees that experience mass attack by the beetles. It would be ironic if the fungal symbionts manufactured verbenone to exploit or manipulate their bark beetle hosts for their own reproductive purposes. 5Raffa and Berryman (in prep.) suggest that the interaction between a living host tree and its beetle colonists will affect the mix of volatile chemicals emanating from an attacked tree and this in turn could provide cues that incoming beetles might use to judge the acceptability of the host. In particular, the ratio of a detoxification product (e.g. trans-verbenol in D.
30
March, 1982
ponderosae) to its resinous precursor (e.g. alpha-pinene) could be correlated with the stage of attack. If the resinous precursor dominated the odor bouquet about a tree, the tree would probably be healthy, and in the process of releasing quantities of defensive resins to repel its attackers. Such a tree would often not be a good bet for a dispersing beetle. But if beetle density were higher (or if the defenses of the tree were intrinsically weaker), resin flows would be less, and the established beetles could convert a large proportion of this material into its detoxification by-product. This in turn would be correlated with a tree that was succumbing to attack. Selection would favor colonists programmed to find such a combination of odors particularly attractive because of the improved likelihood of surviving and reproducing successfully within such a tree. LITERATURE CITED ALCOCK, J. 1975. Male mating strategies of some philanthine wasps (Hymenoptera: Sphecidae). J. Kansas Ent. Soc. 48: 532-45. , AND D. W. PYLE. 1979. The complex courtship behavior of Physiphora demandata (F.) (Diptera: Otitidae). Z. Tierpsychol. 49: 352-62. ALEXANDER,R. D. 1975. Natural selection and specialized chorusing behavior. Pages 37-77 in D. Pimentel, ed. Insects, science and society.
Academic Press, New York. ATKINS, M. D. 1980. Introduction to insect behavior. Macmillan, New York. BIRCH, M. C. 1978. Chemical communication in pine bark beetles. American Sci. 66: 409-419. BIRCH, M. C., P. SVIHRA, T. D. PAINE, AND J. C. MILLER. 1980. Influence of chemically mediated behavior on host tree colonization by four cohabiting species of bark beetles. J. Chem. Ecol. 6: 395-414. AND S. J. BRAND, J. M., J. W. BRACKE, L. N. BRITTON, A. J. MARKOVETZ, BARRAS. 1976. Bark beetle pheromones: Production of verbenone by a myeangial fungus of Dendroctonus frontalis. J. Chem. Ecol. 2: 195-99. AND P. C. JOHNSON. 1980. Behavior of the southBURT, W. D., J. E. COSTER, ern pine beetle on the bark of host trees during mass attack. Ann. Ent. Soc. America 73: 647-652. W. 1979. The evolution of alternative male reproductive strategies in CADE, field crickets. Pages 343-79 In M. S. Blum and N. A. Blum, eds. Sexual selection and reproductive competition in insects. Academic Press, New York. CADE, W. 1980. Alternative male reproductive behaviors. Florida Ent. 63: 30-44. COULSON,R. N. 1979. Population dynamics of bark beetles. Annu. Rev. Ent.
24: 417-47. CROSS,W. H. 1973. Biology, control and eradication of the boll weevil. Annu. Rev. Ent. 18: 17-46. FLETCHER, B. S. 1968. Storage and release of a sex pheromone by the Queenland fruit fly, Dacus tryoni (Diptera: Trypetidae). Nature 219: 631-32. FORREST,T. G. 1979. Phonotaxis in crickets: Its reproductive significance. Florida Ent. 63: 45-52. AND R. I. GARA. 1980. Modeling the dyGEISZLER,D. R., V. F. GALLUCCI, namics of mountain pine beetle aggregation in a lodgepole pine stand. Oecologia 46: 244-53. HARDEE,D. D., W. H. CROSS, AND E. B. MITCHELL. 1969. Male boll weevils are more attractive than cotton plants to boll weevils. J. Econ. Ent. 62: 165-9.
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HARRIS, V. E., AND J. W. TODD.1980. Male-mediated aggregation of male, female and 5th-instar southern green stink bugs and concomitant attraction of a tachinid parasite, Trichopoda pennipes. Ent. Exp. Appl. 27. 117-26. HIRAI, K., H. H. SHOREY, AND L. K. GASTON.1978. Competition among courting male moths: Male-to-male inhibitory pheromone. Science 202: 644-5. E. N. G., ANDT. A. C. M. KOELMAN. JOOSE, 1979. Evidence for the presence of aggregation pheromones in Onychirus armatus, a pest insect in sugar beet. Ent. Exp. Appl. 26: 197-201. KIMSEY, L. S. 1980. The behaviour of male orchid bees (Apidae, Hymenoptera, Insecta) and the question of leks. Anim. Behav. 28: 996-1004. J. E. 1971. Bioluminescent communication in insects. Annu. Rev. LLOYD, Ent. 16: 97-122. . 1973a. Fireflies of Melanesia: bioluminescence, mating behavior and synchronous flashing. Environ. Ent. 2: 991-1008. . 1973b. Model for the mating protocol of synchronously flashing fireflies. Nature 245: 268-70. . 1977. Bioluminescence and communication. Pages 164-83 in T. A. Sebeok, ed. How animals communicate. Indiana Univ. Press, Bloomington. 1979. Mating behavior and natural selection. Florida Ent. 62: 17-34. K. Z. 1963. On aggression. Bantam Books, New York. LORENZ, R. W., ANDJ. R. MATTHEWS. 1979. Insect behavior. John Wiley MATTHEWS,
& Sons, New York.
MORRIS,G. K. 1971. Aggression in male conocephaline grasshoppers (Tettigoniidae). Anim. Behav. 19: 132-7.
NIJHOLT, W. V. 1970. The effect of mating and the presence of the male
ambrosia beetle, Trypodendron lineatum, on "secondary attraction". Canadian Ent. 102: 894-7. OTTE, D. 1972. Simple versus elaborate behavior in grasshoppers: An analysis of communication in the genus Syrbula. Behaviour 42: 291322. . 1974. Effects and functions in the evolution of signaling systems. Annu. Rev. Eco. Syst. 5: 385-417. RAFFA,K. F., ANDA. A. BERRYMAN. In prep.. The role of host resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). J. A. A., ANDP. R. HUGHES.1975. Oxidation of unsaturated cyclic RENWICK, hydrocarbons by Dendroctonus frontalis. Insect Biochem. 5: 459-63. 2 AND J. P. VITE. 1969. Systems of chemical communication in Dendroctonus. Contrib. Boyce Thompson Inst. 24: 283-93. RUDINSKY, J. A. 1969. Masking of the aggregation pheromone in Dendroctonus pseudotsugae Hopk. Science 166: 884-5. 1974. Sound production in Scolytidae: 'Rivalry' , ANDR. R. MICHAEL. behaviour of male Dendroctonus beetles. J. Insect Physiol. 20: 1219-30. , AND L. C. RYKER. 1976. Sound production in Scolytidae: Rivalry and premating stridulation of male Douglas-fir beetle. J. Insect. Physiol. 22: 997-1003. , AND L. C. RYKER. 1977. Olfactory and auditory signals mediating behavioral patterns of bark beetles. Pages 195-209 in Comportement des insectes et milieu trophique, C.N.R.S. Paris, France. , L. C. RYKER, R. R. MICHAEL,L. M. LIBBEY,AND M. E. MORGAN. 1976. Sound production in Scolytidae: Female sonic stimulus of male pheromone release in two Dendroctonus beetles. J. Insect Physiol. 22:
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RYKER, L. C. In prep. The world of the Douglas-fir beetle. SHOREY,A. H. 1973. Behavioral response to insect pheromones. Annu. Rev. Ent. 18: 349-80. TSCHINKEL, W. R., C. D. WILSON, AND H. A. BERN. 1967. Sex pheromone of
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ULAGARAJ,S. M., AND T. J. WALKER. 1973. Phonotaxis of crickets in flight:
Attraction of male and female crickets to male calling songs. Science 182: 1279-79. VITE, J. P., AND W. FRANCKE. 1976. The aggregation pheromones of bark beetles: Progress and problems. Naturwissenschaften 63: 550-5. , AND G. B. PITMAN. 1968. Bark beetle aggregation: Effects of feeding on the release of pheromones in Dendroctonus and Ips. Nature 218: 169-70. WAGNER, T. L., R. M. FELDMAN, J. A. GAGNE, J. D. COVER,R. N. COULSON, AND R. M. SCHOOLFIELD. 1981. Factors affecting gallery construction, oviposition and reemergence of Dendroctonus frontalis in the laboratory. Ann. Ent. Soc. America 74: 255-73. WILLIAMS, G. C. 1966. Adaptation and natural selection. Princeton Univ. Press, Princeton.
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beetles. Symp. Roy. Ent. Soc. London 6: 101-17. , AND W. D. BEDARD. 1976. The role of pheromones in the popu-
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Natural Selection and Communication among Bark Beetles Author(s): John Alcock Source: The Florida Entomologist, Vol.

Florida Entomologist 65(1)

Insect Behavioral Ecology-'81 Alcock

Reproductive Effect Emitter +

Florida Entomologist 65(1)

Insect Behavioral Ecology-'81 Alcock

Florida Entomologist 65(1)

Insect Behavioral Ecology-'81 Alcock

Florida Entomologist 65 (1)

Tree with Intact Defenses

Insect Behavioral Ecology-'81 Alcock

Florida Entomologist 65 (1)

Insect Behavioral Ecology-'81 Alcock

Florida Entomologist 65 (1)

Insect Behavioral Ecology-'81 Alcock

Florida Entomologist 65 (1)

Insect Behavioral Ecology-'81 Alcock

Florida Entomologist 65(1)

the mealworm beetle, Tenebrio molitor. J. Exp. Biol. 164: 81-5.

D. L. 1973. Selection and colonization of ponderosa pine by bark WOOD,

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