1999/07/01 by Edmund D. Brodie · 6 citations
Environmental Science · Biochemistry, Genetics and Molecular Biology · Agricultural and Biological Sciences · #Animal Ecology and Behavior Studies #Genetic diversity and population structure #Insect and Pesticide Research #Predation #Predator #Biology #Zoology #Ecology #Fishery
paper · doi:10.2307/1313476
openalex publication_date 1999/07/01 · openalex created_date 2025/10/10 · openalex updated_date 2026/07/29
There is an intuitive appeal to viewing natural struggles among species as arms races between enemies. Consider the sit-and-wait predator in his shiny patrol car who sits behind freeway overpasses waiting to subdue speeding motorists. As drivers became more wary, law enforcement employed radar guns to identify their quarry. This development was easily combated with radar detectors, until police discovered X, K, and Ka bands. Radar detectors were gradually modified to handle each new frequency, but then some jurisdictions passed laws banning the use of radar detectors and police began using “VG-2 detector hunters” to identify motorists with illegal detectors. Stealth and cloaking options are now available that jam the police detector hunter units. Enter police Lidar detectors, which use laser technology to clock and register speed so quickly that drivers have little time to react and reduce their speed. The latest driver defenses not only detect Lidar, but jam the frequency to provide a few more seconds to slow down and avoid capture. Predator-prey interactions differ from other types of victim-exploiter systems in that selection on predators frequently may be weaker than on prey Natural enemies seem to behave in much the same way; improved abilities in one species demand compensatory improvements by its enemies if they are to continue to be successful. However, the use of the arms race analogy to describe an evolutionary phenomenon invokes specific criteria. In an evolutionary race, the players are lineages, not individuals. Steps are taken in evolutionary time (i.e., across generations). Finally, any beneficial step forward in the race by one player must cost the other and vice versa, so that evolutionary changes by one player increase selection on its opponent, causing a concomitant change. At the center of any arms race are the arms themselves. The interaction that drives any coevolutionary system occurs at a phenotypic interface that comprises the characters that determine the outcome of any confrontation between individuals. These are the traits that both cause and experience the selection of an evolutionary arms race; consequently, they are the features that become elaborated after generations of interaction. Reciprocity is the defining feature of coevolutionary interactions in general, and of arms races in particular. Not only must adaptation by one player favor change in its opponent, but the opponent's adaptation must likewise generate selection on and evolutionary response in the first player. The result is a race in which both players run neck and neck, with well-matched abilities; each step forward by one player necessitates a reciprocal step by the opponent, lest the opponent fall behind. As the metaphor suggests, arms races are interactions in which the players are antagonists that get caught in an escalation of ever-increasing abilities. Although many coevolutionary interactions can be described as arms races, not all of them fit this model. Mutualistic relationships among species, frequency-dependent cycling of traits in enemies, and a range of other dynamic processes all fit the criteria for coevolution but not the pattern of counter-escalation envisioned in an arms race. The simplicity of the arms race, and the sometimes all too personal familiarity with what it is like to be caught in one, has led biologists to apply this perspective to a wide array of evolutionary interactions between natural enemies. However, the degree of reciprocity and details of selection vary among antagonistic interactions. Predator-prey interactions, especially, may be characterized by asymmetrical selection that precludes arms races (selection on prey is thought to be stronger than on predators). In this article, we use a covariance approach to understanding selection to dissect those components of an interaction that contribute to the strength of selection by one species on another. After evaluating the evidence that selective inequalities exist and are unique to predator-prey systems, we suggest that interactions involving dangerous prey differ from other predator-prey systems and are likely to result in revolutionary arms races. In support of this view, we describe results from investigations of the roughskin newt (Taricha granulosa), which possesses the neurotoxin tetrodotoxin (TTX), and its resistant predator, the red-sided garter snake (Thamnophis sirtalis). Within-population variation in this system suggests the potential for evolution of resistance to TTX, and the matched exploitative and defensive abilities among populations fits the predicted pattern for arms races between predator and prey. Antagonistic interactions among natural enemies are to as This the many interactions one species from and predator-prey interactions. Although is some to all of interactions, the array of natural they that some may be by them The of victim-exploiter relationships interactions that differ in of and As a the of the races and not all victim-exploiter systems are likely to the for coevolutionary interaction. of coevolution have on and their and on and their The of in systems range from of of antagonistic and to of reciprocal selection and evolutionary change and in In many of systems, the phenotypic interface is not only from a phenotypic perspective but from a of have not only that the by have on species of but that among may the evolution of the of defensive traits and of have that and can be caught on a in which the in species in a frequency-dependent of the by the in in their frequency and their as the changes in the and the to escalation in arms races that are of adaptation have by traits in a and their and between predators and prey is Although the analogy has in systems, many of predator-prey arms races are defensive of prey as the by to predators and the and of that vary with types of predators These characters have in response to selection from but in is little evidence of by their to this pattern as the of in and their both of which that are for species These with the of that and and the have that are in the in the of matched features between prey and predator of and the abilities of their predators have in a Although this of evidence is of arms races, it not reciprocal selection and evolution between predators and prey. for the between prey and predator has by who that the of evolutionary interaction between predators and prey is not coevolution but The between escalation and coevolution is in the of selection that phenotypic In evolutionary change a pattern of species in response to their enemies predators than a reciprocal interaction between and predators and the is that evolutionary change in predators is by their predators not by their prey. in both predator and prey speed that are to an arms race result from both species to from their the of may have in response to and the of the predators of the may have a response to evolution by their not escalation is a of evolutionary the the with which the arms race analogy is to predator-prey predators and prey are likely than other natural enemies to be caught in coevolutionary arms races, what are the what features of the interaction between predators and prey not in interactions between other natural enemies, that coevolutionary races not and evidence suggests that predators may not be to in response to prey prey in response to and have to predator and prey may not be in an arms race; down to an of the strength and of reciprocal selection by prey on predators is to be much weaker than selection by predators on prey. understanding of the of selection is to predators and prey experience of selection if determine the of arms races between have the phenotypic of selection from the response that evolutionary change. this selection is the between and of traits are with than and selection can be as the covariance between traits and and The of this approach is that the strength of selection can be and using that increase the covariance between and generate stronger and that the covariance reduce the strength of The covariance approach is to the between and the same However, the same can be to the of other of the same species The covariance between an and the it the strength of selection from that the is species, as in potential coevolutionary interactions, the covariance of is between the of of one species and the of traits at the phenotypic interface in the other species This of selection by one species on that the between predator and prey is the same for all of predator In the is more predators with be to have relationships with the same prey. The covariance approach can be modified to this by the interaction of predator predator and prey but the is not we to the which a that it to the that the strength of selection in a interaction. covariance is as a The between as the of the and as the of the (i.e., as one is predicted by the In features can be as the of the interaction and the of the The between predator and prey The strength of selection as the from an interaction between species can be by in one species as a of the traits in the species it The that the and be the of an interaction and the of that The of the the increase in the of a predator that with a prey of a a any the the the of predator for a The is as the from the to the with little and with but with little but with and The results from in the of the interaction between predator and prey (i.e., the between and the to avoid selection is by in the of the with with Although we the covariance approach using the of predators as by interaction have a of relationships for predator-prey systems, prey can be as a of predator The of the interaction is the of an that with with a phenotypic is little between with the then the of the interaction is and the and prey from this is the of from predators of all predators are too slow to the then the of is for any of predator, but if predators are matched to prey the of differ between the and The of the is the that the be the degree to which the of one is predicted by the of another. may be the race is run a of other traits of predator prey for in the prey may be more the outcome of a interaction is only a of In other if the of an interaction is then the is but if the can be then is selection is weaker on predators than then must be in the of interactions the of There are some to both of as we some of are not unique to predator-prey systems, and they are to the of coevolution in predator-prey to be is in predators may be to avoid selection by prey. The the types of interactions likely to result in a coevolutionary arms systems in which predators with dangerous prey. The for predators may not to prey is the and The is a of the race between predators and prey that is to the selective between the a a one the other must the race the the and the its to from not the other if the the race it is caught by the and in The of this interaction is more for prey than for that selection is stronger on prey than on This in selection is to result in evolution of prey than predators in the evolutionary to with their prey. However, this the of phenotypic which is a of selection and The evolutionary change in a is predicted by the strength of selection and the the of variation in a that is by of and if the of and were to experience the same strength of speed more in the species with for the traits at the phenotypic selection is as with the then the of evolution may be if the of speed in the species the that variation are and and is little a to to be However, an of the of increase in is by the of to the that selection some to be for traits stronger selection and and if selection is stronger on prey than then prey defenses have variation than predator exploitative abilities. in selection to in that one in of phenotypic evolution for both predators and prey. at the of predators suggests that the is a of the strength of selection on predators have little to in a race with it is to the that from the of to the of from to The from races between to evolutionary races between populations must that if a predator races, it its The is more selection in a interaction is not only the of the race (i.e., but the abilities of the The of the interaction not on the of each species, but on its to that of its the players are then variation among predators have a on the predicted of a race the other if is in predator much of a to and the between the by predators be The predator and prey be selection than it is in in which abilities are The strength of selection on and change as the of each species this this has the coevolutionary and that the some that are and not the the the has more to if to the is then a of matched abilities is In are predators and prey to in an arms race. this dynamic is an of natural in that it traits can to selection the is for arms races, systems have for one feature are for use in and traits to one the is at at a but for of to This to adaptation suggests that selection is more with a in which the of a as it from its selection a that the can result in some of the (i.e., frequency-dependent cycling of the fit and the escalation of both species that is of an arms race and Although on the of the they an arms race a cycling if selective an arms race, they are unique to predator-prey The same of for the of and interactions, in the In interactions between predators and the is to experience weaker selection than the its in other types of victim-exploiter systems, the may have more to than the and reduce the of a to but of the the with some potential to if a from the is to to as its may be not their but they their they in This is a to the on a can sometimes result in that a can have and may on the other its at the of the which can and the in this in is little that coevolution occurs in this and other systems inequalities seem to the of coevolutionary interactions between predator and prey. of the among types of victim-exploiter systems is the of the degree to which each species the of the that defenses the may and the that is on the of that of are for both in an interaction. in the of the so player can avoid the of the as and which a for a an interaction their that are at the of interaction with a to players in victim-exploiter systems, which selection on their predators seem to be to avoid many of the of the interaction. that to detect a prey to a prey in a not with the prey. As a predators can avoid many of the selective that in a more interaction. specific defenses the prey from to be employed in the of the after capture. The of the interaction for the predator is to a and to and time are the Although the of a prey may be to an arms race, the of this for any predator is predator may the prey in which the of the first interaction is prey are the predator to a more and experience than if it the prey. The cost of any prey on as the its of its and a of other of the for the prey of the to much more than other to be Although are predators are and on a of prey As a result of their of predators have to to if one to capture. This to can selection by any prey species in the of is likely to be prey As a the covariance between predator and the of any one prey be (i.e., selection from any one prey is a predator can increase its by to prey. The to prey can the interactions with one prey in covariance of with the traits of that prey the to prey is a it can increase an and the cost of races with other prey. The between predator and the to prey be much than that between and the to any prey. The in selection on abilities suggests that predators prey selection by prey. This pattern of selection in the of that is of is to result from coevolutionary interactions predators and prey are caught in arms races, then the of between predators and prey is this pattern of selection may the are and not to prey The of and the of and in many are all of that increase the to a of prey types than one specific the same is of some defenses of as the of There in which prey and predator and in which the of with prey are and defenses can be to the of the in which they as and by a as and to after defenses in of are to generate selection on predators for the in the defenses the after predator and prey have the defenses that that the predator a interaction to the the degree of between and is and result from the prey are by the the of is to be for predators with prey is a The of can vary the of many defenses are to have a for the of and the of to the of but cause little to In selection on predators is the of the between and prey is the of the is the other some prey have and other features that can a predator and and that can and that and handle prey experience a with and selection is which predators with dangerous are likely to the for In the same that are selection from their predators are selection from dangerous prey. that variation for traits is this to an evolutionary response by at types of response are can be by of the prey improved exploitative to an arms of specific prey types is among predators and drives the evolution of systems and in prey. predators to avoid prey that have after an experience with the prey. The of prey can a predator to avoid prey in the The that to may be but they not have (i.e., prey are not The of predators to with the results in a pattern of of prey. However, not an evolutionary response of predators to prey each must the the to may of and has in and and but to detect of specific prey by natural predators have results This of evolutionary response is not the of prey. to this pattern is the of by predators and a that can potential The and pattern that their is by a wide of snake species that are not only Although it may seem that species are in a the species are by their to a species, it is to predators to avoid a prey that likely them a interaction. The of and the of which is likely to be this interaction has and and for the evidence that potential predators of have in response to this selection with and from potential predators of the of of with with with the and pattern of with other and in the same with the same in as than not the same response and were as potential prey. This is not a feature of as by the that species are to not avoid snake the of snake by predators is an evolutionary response to dangerous prey. The of by predators a selective to with of prey can and is one result of the and of with dangerous but it the of to prey defenses for coevolutionary arms races. an arms is but matched of both defensive of the prey and exploitative of the predator are the criteria of selection are in the range of the the selective may and with it the degree of of exploitative and defensive traits the abilities of both species matched in of and Finally, some perspective is to not traits in These of evidence in support of an arms race of coevolution in the predator-prey interaction between the newt and its garter snake predator in species of garter are with one more of the but only has to that is the only predator that is resistant to the of the in but more has that resistance among populations of and of as a prey may not have for it on the range of the and are a of traits that in so of one prey result in of The phenotypic interface of the interaction between and the TTX, of the is one of the of the to in and The of of the results from of in the and this is to a wide range of potential predators of the TTX, but is many more than its to Although is in a of at in is the only with a resistant predator and The selective of a prey are and that sometimes the newt The garter snake is the to this but it is not after a of the first of is the of and and some that a newt and may be for to this of can a an that is to may and if caught in a for too to As with other the of for any other species, for that the predator has the prey. fits the of a dangerous prey that a and for predators response of garter the evolutionary potential and of a some of the of variation among and we a to resistance on the of on and are with a of TTX, and their speed is The in their is of their resistance to by at of their may at than of their speed. This is a and one of its first is to The is in that it in and is of the of in prey and from of to and have that is not in the system of this we have to the of a in response to prey The of resistance in is a that is the only species of garter snake that is resistant to at an (i.e., to it on with a of resistance that of any other of the However, the in the and its to be a resistance to than is in other in that may be some to resistance the variation for selection to on and potential for evolutionary change. resistance has from to on of in resistant populations to and of this variation is likely by one a few of and on resistance and to increase resistance to have results that resistance is a that has the potential to to The of of is with the for those at the phenotypic interface of coevolutionary interactions and and As for resistance to in with a this In populations resistant and so we have evidence of a between speed and resistance at both the phenotypic and and and that have the resistance to to have the speed. The of this may in the of Although the is resistance likely results from the of are by a and have for have in many and than and the of resistance in garter the evolution of the between and resistance from the of the of the its may be an in the evolution of resistance the coevolutionary predicted by some and arms race between predator and dangerous The evolutionary response of predators to dangerous prey is of only one of an arms race, and we are only to the to reciprocal coevolution is between garter and we have some that suggest an arms race in of of and are matched on a and of populations a pattern of variation in resistance and resistance not only among species of garter but among populations of the in speed after an of a of TTX, we have the of among populations of and populations of that exist the range of are not resistant to and populations are not with the selective of we not them to have is is that among the populations that are with and are to on resistance an range and resistance was in populations from that are as resistant as populations other However, populations from and the of that are to on are more resistant than the populations as their of resistance is than the At the other are from the of the garter that are more resistant than any other This is on of their of have other natural populations with of resistance and of tetrodotoxin resistance in the garter snake resistant and The range of the newt is as the in resistance of the garter snake to tetrodotoxin The resistance of each is as a of of The for the populations to the on the in on was as the of an speed after an of a of is on a in as the of to of in by the of from a populations of and are more resistant to than populations by the of populations and are with populations that The resistant populations and an range of resistance and are with newt populations to the pattern of resistance among populations is so then the the evolution of resistance must differ (i.e., is a of The is the selective Although it has that are their range and that the of is the species, suggest that both are The of in was in the using from the of and the both with populations using from and of in as to from the populations to and This result suggests that from have little TTX, which is from the that can on have a of the variation in among populations of their we have to in among and for some of the for which of snake resistance are that populations vary in the of in as as in the of and populations from garter are have the of have much of TTX, and one in of some populations have at in tetrodotoxin of from in and were for of using The of has of TTX, as as of and to the are the are in from The of variation in that of snake In the of a covariance of the in to in the strength of TTX, predators experience a a of on and and is to predators to In the cost of resistance in may be selection exploitative abilities in the the evolution of resistance an arms race is at this The criteria of reciprocity and have not and we have little variation and selection on in are all of However, the evolution of prey in response to predator is The unique feature of the garter system is that it dangerous prey can selection on the evolution of exploitative Although predators and prey are to in an arms both evidence and suggest that predator-prey interactions not arms race Predator-prey interactions differ from other types of victim-exploiter systems in that selection on predators may frequently be weaker than on prey. The of this is that prey more than predators to the covariance approach to selection as a it that of interactions and the of the the strength of selection by one species interactions with another. of in predator-prey systems suggests that the in selection is not by the but by the of the an predator to a prey. However, interactions to the of the are more At this prey as that can a In predators are to experience selection and to of dangerous the of they exploitative traits that interaction with the dangerous prey. The is by the interaction between and their resistant garter snake and of resistance and all that garter are in response to prey and that an arms race between predators and prey is This has by the and for of some of the and improved the of the