TREE vol. 1, no. 4, October 1986

Constraints The study of coevolution has ma- tured from a descriptive science con- cerned with demonstrating mutual counteradaptations in interacting species into an analytical science concerned with the patterns and pro- cesses of coevolutionary change. Studies of predators and prey, para- sites and hosts, and grazers and grazed have suggested that these interactions are subject to con- straints that affect both the rate and the direction of coevolutionary change.

Expectations as to how antagonis- tic interactions between species change over evolutionary time have varied in the past 20 years as our understanding of coevolutionary processes has improved. A once common view in parasitology, for example, was that interactions be- tween parasites and hosts tend to- ward commensalism, or at least re- duced virulence, over evolutionary time. But comparative studies of parasites have shown that virulence is often associated with transmis- sibility and that many coevolutionary outcomes are possible’-3. In ecol- ogy, older ideas on the balance of nature have given way to an under- standing that the evolutionary out- comes of antagonistic interactions can range from a continuing ‘arms race’4 to mutualism5, and that even these extremes are not mutually ex- clusive.

The ‘arms-race’ view, in which coevolution is seen as a series of progressive improvements in adaptations and counteradaptations in interacting specie@, has become especially prevalent in evolutionary ecology as a result of studies on defense and counterdefense in inter- actions between animals and plants7-g and the focus on the in- herent evolutionary selfishness of interactions?“. No single species is ahead in the race for long, since the other species are also continuing to evolve. Borrowing from Lewis Car- roll, Van Valen” called the extreme of this view the Red Queen hypoth- esis: ‘Now here, you see, it takes all the running you can do, to keep in the same place’. New adaptations in one species have detrimental effects on other species, which in turn select for evolutionary changes in those species. The pattern of coevolution- ary change in a world run on Red Queen conditions could range from continuous evolutionary change, ex- tinction and speciation among the

John Thompson is at the Departments of Botany and Zoology, Washington State Univer- sity, Pullman, WA 99164, USA.

interacting species, to steady states punctuated with evolutionary changes only in response to changes in the physical environment”. Such coevolutionary changes could in- clude escalation in levels of current defenses and counterdefenses or the appearance of novel defenses and counterdefenses through mutation.

Although the arms-race view of coevolution is a valuable heuristic tool, like any tool it has limitations. Arms races are probably seldom re- lentless bouts of defense and coun- terdefense. Instead, they appear to be subject to constraints that can affect both the rate and the long- term outcome of interactions.

Anything that hinders further progressive development of an arms race is a constraint. Constraints can prevent or slow down the escalation in current defenses or counter- defenses, or they can limit the de- ployment of new ones. There are obvious constraints, such as the availability of appropriate mutations and the inefficiency of natural selec- tion in small populations experienc- ing genetic drift. But there are also other constraints that derive partly from the way that selection acts on interactions.

Polymorphic equilibria Models of evolutionarily stable

strategies suggest that, in the ab- sence of new mutations, a stable equilibrium in current defenses and counterdefenses is possible if each species has only one kind of defense (or counterdefense) and that defense is subject to continuous environmen- tal variation13. With the addition of new defenses and counterdefenses, this initially stable equilibrium dis- appears. The populations may swing first in the direction of the new, mutant strategy and then back again as the mutant strategy becomes more common’4. Such frequency- dependent shifts in mutual counter- adaptations have been suggested for the evolution of resistance and viru- lence in parasite-host interac- tions15,16. The result would be the maintenance of multiple defenses and counterdefenses through frequency-dependent selection. Density-dependent selection or heterozygote superiority could also contribute to the maintenance of polymorphic mutual counter- adaptations “-“. As defenses and counterdefenses accumulate in the interacting populations, a pro-

commentary on Arms Races in

Coevolution John N. Thompson

gressive arms race could therefore give way, at least for a while, to a continual reshuffling of the alleles already present in the populations. In fact, what may appear as directional selection in a coevolutionary field study lasting several years or even decades may be just one part of a cycle of frequency-dependent or density-dependent selection on an interaction.

Reaction norms Each new escalation in the level of

a current defense or the introduction of a novel defense need not necess- arily be countered directly by the other species in a gene-for-gene fashion. Since the phenotypic ex- pression of genes can vary among environments (the range of express- ion is called the reaction norm), the appearance of a new defense allele could sometimes simply induce a different but effective phenotypic re- sponse in the other species. In fact, selection could favor defense alleles that are especially variable in their phenotypic expression.

The immune system of verte- brates, which can respond to a wide variety of microbial invasions, may have resulted partly from this kind of selection. One of the problems with which the vertebrate immune sys- tem must contend is exemplified by cattle in Africa that become infected with Trypanosoma brucei, a flagel- lated protist parasite that lives in the bloodstream. Each parasite is cov- ered with a single glycoprotein, cal- led variable surface glyprotein (v.s.g.)*‘. As many as 1000 potential v.s.g. genes may occur in T. brucei, which allows a vast array of im- munologically distinct protein coats”. Hosts respond to the para- sites by producing antibodies appropriate to the particular v.s.g. coat. The parasites, however, can change their coats. Consequently, parasite numbers fluctuate within each host as antibodies are pro- duced to eliminate parasites with a particular v.s.g. coat, while parasites with other v.s.g. coats continue to appear and multiplyz2. If the cattle do not have different individual genes to counter each of the array of v.s.g. coats that individual parasites can produce, then selection would prob- ably favor phenotypic variability in these defenses.

Selective asymmetries Dawkins and Krebs4 have sug-

gested two ecological situations in 105

TREE vol. 7, no. 4, October 7986

ma brucei. The _:^^

which the strength of selective press- ures could be asymmetric on inter- acting species. In what they called the ‘rare-enemy effect’, one of the two species in an interaction is so rare that it has little selective effect on the other species. The interaction may be critical to the rare species and may exert very strong selective pressures on it, but may not be com- mon enough and selective enough in the other species to favor counter- adaptations. In the second scenario, which they termed the ‘life-dinner principle’, one of the two species has more to lose by failure in an inter- action. In their example, from a fable by Aesop, ‘the rabbit is running for his life while the fox is only running for his dinner’. Dawkins and Krebs argue that this asymmetry could pro- vide a built-in evolutionary advan- tage for the species that has more to lose in the interaction. The life- dinner principle probably would not prevent an arms race in the long term, but it could affect the rates of directional coevolutionary change.

Age-specific attack of hosts is not so much a constraint on an arms race as a potential evolutionary route that diminishes or eliminates the potential for further coevolution. Un- 0

A different kind of asymmetry has been proposed by Lenski and Levinz3 for the coevolution of bacteria and virulent phages. They suggested that arms races in these interactions are limited by mutational constraints on the phages and selective constraints on the bacteria. In both a mathemat- ical model incorporating mutation rates and in a chemostat experiment using Escherichia co/i B and virulent T-4 phage, Lenski and Levin found that E. co/i rapidly evolved resistance to the phage while no T-4 mutants

appeared to counter the resistant, during long runs of the model or experiment, indicating that the bac- terium may acquire resistance more easily than the phage can extend its host range to new host genotypes. Bacterial resistance could develop simply through single-base substitu- tions, insertions or deletions, where- as host-range extensions by the phage require more specific changes in the phage’s configuration or the mechanism triggering the injection of the genetic material. Lenski and Levin also suggested that selective constraints on the bacteria prevent the complete establishment of the resistant genotype. Under resource- limited conditions the resistant bac- teria may be under a selective dis- advantage in competition with sensi- tive bacteria, because the evolution of resistance may involve the loss or alteration of surface receptors that are important for the bacterium in exploiting its environment. This selective constraint is a form of density-dependent selection.

could be adjusted either by the tim- ing of contact with hosts or through a period of latency after penetrating a host. Parasites that preferentially attacked late- or post-reproductive hosts could in some cases have higher fitness than those attacking younger hosts. Since selection on post-reproductive individuals is ineffective2k27, late- or post- reproductive hosts may sometimes have reduced defenses as delet- erious genes or negative effects of genes become expressed late in life. Any new adaptation developed in the parasite to attack more effect- ively its post-reproductive host would not be met with counter- defenses in the host population. Although there are many parasties that usually attack hosts at late- reproductive ages, it is not clear if any of these cases is a result of selection in parasites for the specific attack of older individuals.

Population structure If interacting populations of para-

sites and hosts differ greatly in gen- eration times, as in some parasites of vertebrates and pathogens of peren- nial plants, then the interaction could tend toward a decreasin arms race over evolutionary tim3*24. Short- lived parasites that attack long-lived hosts could potentially choose among host ages at which attack would be most beneficial to the para- site fitness. Age-dependent attack

less extended parental care IS important in the host population, attack of late- or post-reproductive hosts by parasites may be essentially commensalistic with respect to host fitness.

The antagonism/mutualism interface Mutualisms are as much based

upon manipulation of another spe- cies as are antagonistic interactions, and many mutualisms appear to be simply fortuitous evolutionary shifts in interactions that were previously mostly antagonistic5. In antagonistic interactions the focus of selection in victims is to reduce both the prob- ability of interaction and the negative effects of the interaction on the vic- tim’s fitness; selection on the exploi- ter is to increase both the probability of interaction and the positive effect of each interaction on its fitness. By comparison, the focus of selection on a host in mutualistic interactions is to maximize the probability of in- teraction and the positive effects on its fitness while minimizing what it must give up to attract its mutualist; selection on the visitor or symbiont is essentially the same as in antag- onistic interactions.

In both antagonism and mutual- ism there is always the potential for the continuing evolution of defenses and counterdefenses as selection favors individuals that obtain more or lose less from the interaction. The major consequence of the evolution of mutualism from antagonistic interactions is that it places some constraints on the kinds of defenses

TREE vol. 1, no. 4, October 1986

and counterdefenses that can be de- ployed, since selection on hosts is no longer to prevent or minimize the probability of interaction.

The balance between antagonism and mutualism can also shift back and forth over evolutionary time de- pending upon the availability of re- sources and the abundance and fre- quency of other species in the com- munity. As resource levels and the frequency and abundance of sur- rounding species change, selection on hosts to increase the probability of interaction could be juxtaposed with bouts of selection to decrease the probability of interaction. Some mutualisms, for example, involve at least three species, one species being used as a means of defense either directly5 or indirectly28 against another species, e.g. some Acacia species defend themselves against herbivores and encroaching

!? lants

by harboring aggressive ants’ . The importance of the mutualism to a plant depends upon the abundance of herbivores and competing plants, which can vary over time. Conse- quently, the morphology, life history and behavior of the mutualists can reflect the past history of variable selection on the interaction, and some hosts could appear to be either overdefended or underdefended against their mutualists.

In yet other interactions, species could be mutualistic in some aspects of their life history while being antagonistic in others. Templeton and Gilbet?’ have found a clear ex- ample in Heliconius butterflies. Heli- conius adults are brightly colored and distasteful to avian predators, and in Central and South America the color patterns converge among sympatric species to form Mullerian mimicry complexes (groups of dis- tasteful species that adopt similar warning displays). Avian predators learn to avoid individuals with these color patterns, and individuals of all the Heliconius species in the mimicry complex benefit from having the avoided color pattern. The same Heliconius species, however, com- pete for nectar and pollen of two

genera of cucurbit vine, Anguria and Gurania, that are critical for adult survival and reproduction. Here the antagonism is competition rather than exploitation between trophic levels, but similar kinds of inter- actions that are simultaneously antagonistic and mutualistic un- doubtedly exist between trophic levels.

A plethora of outcomes Overall, the past decade of theor-

etical and empirical studies on the coevolution of antagonists has sug- gested that arms races between spe- cies are seldom likely to proceed as relentless and progressive bouts of defense and counterdefense. Escala- tion and the introduction of novel mutual counteradaptations are likely to be erratic and constrained, as some interactions evolve toward commensalism. others cycle through frequency-dependent or density- dependent selection, and still others cope with varying selection for mutualism and antagonism. The problem now is to understand the ecological conditions that make some outcomes more probable than others. This will re interaction I.4

uire the study of norms , that is, the

variation in outcomes of interactions across environments and under different ecological conditions as genotypes (or distributions of genotypes) are held constant.

Acknowiedgements I thank R.N. Mack and L.D. Mueller for

comments on the manuscript. This work was supported in part by USDA grant 84CRCR-1-1395.

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