Principles of coevolution
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1 Roctivo,.. v() 9s-' Principles of coevolution Principles of coevolution Much of coevolution occurs according to the broader principles of evolution in general. Selection on traits occurs when there is variation in reproductive success and when variation in the trait is correlated with reproductive success. A response to selection occurs when some of the variation in the trait is genetic. The types of variant that can be produced are constrained within lineages by developmental mechanisms specific to those lineages. The amount of mutational variation entering the population depends on its effective size, and the opportunity for mutations to affect a trait depends both on the number of genes coding for the trait and on the manner in which the trait is expressed. The capacity of a local population to adapt to local conditions depends upon the geographical structure of the meta-population in which the local population is embedded and the amount of gene flow it experiences. All that applies to the evolution of any trait, whether it is involved in a coevolutionary interaction or not. What is new in coevolution is interaction with an evolving partner. Among the new effects that this introduces are those listed below. KEY CONCEPT The intensity of a coevolutionary interaction depends on its frequency and its impact on the reproductive success of the partners. Reproductive success may now depend largely or in part on the reproductive success of the partner. The optimal values of interaction traits may now continue to shift from generation to generation as the partner changes, either in an endless, open-ended fashion, or towards some definite value in both partners. The geographical pattern of the interaction is determined by the overlap between the geographical occurrence of the focal species and the geographical occurrence of the partner. This overlap may be large or small, symmetric or asymmetric. Speciation may now result from speciation of the partner. A central issue in coevolution is whether the interaction will evolve towards specialization or not. Some of the interactions that evolve towards specialization from a generalized starting point are mutualisms and parasite host interactions. Predator prey interactions and competition evolve towards specialization less often, but some of those interactions do become specialized. The direction in which an interaction will evolve depends both upon the co-occurrence of several conditions and upon the opportunities for selection that they create. We now discuss those conditions. Frequency of interaction and impact on reproductive success Whether an interaction is, or will become, tight and specialized or diffuse and generalized depends upon the frequency with which the partners interact and
2 18 Coevolution on the impact the interaction has on their reproductive success.'in the discussio of levels of coevolution above, we began with intimate interactions betwee molecules within cells, moved through intracellular symbioses and interspec interactions, and ended with interactions between clades. Along that gradie the importance of other factors that could interfere with the coevolutiona process and prevent it from achieving a high degree of adaptation ranged fro low for molecules to great for clades. If the focal species can devote its attentio so to speak, exclusively to the coevolving partner, without being 'interrupted distractions,' then it is relatively easy for specialization to evolve. This wi happen for the following interactions under the conditions mentioned that favor specialization. Parasite host interactions: completion of the entire life cycle on a single host; feeding on the living host and having to deal with its induced responses; living within the host rather than on its surface. Plant herbivore and predator prey interactions: feeding on a species that is continuously available in edible form throughout the growing season of the consumer; the victim species is reliably available year after year; capturing, handling, or digesting the victim requires specialized adaptations that reduce the consumer's ability to eat other things; the victim is sessile, or moves slowly, and is easy to find (Thompson 1994). Mutualists: interactions either already are or during the evolution of the interaction become predominantly positive, with large, and fairly symmetrical, impacts on the reproductive success of both partners, this being facilitated by living in intimate contact for most or all of the life cycle. Some of the remarkable cases of specialization in vertebrates include giant pandas and red pandas, which eat only bamboo; sage grouse, which eat almo exclusively one species of sagebrush; and aardwolves, the most specialized the several mammal species that have converged on eating ants and termite Aardwolves eat only termites of one genus, Trinervitermes, a genus that protected from all other predators by the corrosive terpenes secreted by t soldier caste. Young aardwolves being weaned from a diet of bland milk corrosive termites have been observed having difficulty accepting the food th will become their diet for life (T.H. Clutton-Brock, personal communication In all three cases the consumer has to overcome significant defenses silicate bamboo leaves and defensive chemicals in sagebrush and termites. By being ab to overcome these defenses, they gain access to a food resource largely free fro exploitation by other consumers. W I Relative evolutionary potential Coevolutionary interactions can evolve towards stable coexistence; they can als evolve towards the extinction of one of the partners. There is no guarantee th
3 Principles of coevolution both species will be able to stay in the game. The factors that determine which of the partners may be able to gain the upper hand in the interaction include generation time, genetic system, and genetic variation for the interaction.traits. (1) All else being equal, the partner with the shorter generation time will evolve more rapidly. Most pathogens have much shorter generation times than their hosts; part of the vertebrate defense against pathogens is achieved by having an immune system whose response time is much closer to the generation time of pathogens than is the generation time of the organisms containing it. (2) All else being equal, sexual partners will be able to evolve more rapidly than asexual partners. Interactions with pathogens and parasites are one of the major reasons for the maintenance of sexual reproduction in hosts, and they have at times been countered with increased rates of recombination in parasites and pathogens (Chapter 8, pp. 192 f.). (3) And, all else being equal, the partner with more genetic variation for the interaction traits will evolve more rapidly. For bacterial pathogens living in vertebrate hosts, the chief threat is the vertebrate immune system. The immune system rapidly sorts through a huge array of molecules until it finds one that binds specifically to the surface of the bacterium. It is therefore in the interest of bacteria to frequently change the characteristics of the surface they present to their; hosts, and in fact the genes that code for surface proteins have the highest mutation rate and are the most rapidly evolving part of their genome (Moxon et al ). Unless it is in the interest of both partners that the interaction persist, and that interest is a top priority for both, one partner could win the arms, race and drive the other to extinction. If a predator, herbivore, or parasite can feed on several different prey species, the disappearance of one of them may make little difference to its reproductive success. If a competitor can be eliminated without serious consequences, there will be no reason for the focal species to alter its characteristics. The array of coevolutionary interactions that we observe thus probably consists of those in which this has not been the case, where the interaction stabilizes in a manner permitting coexistence, and of those in which extinction has not yet happened but is in the process of doing so. The Red Queen There is some paleontological evidence to support the idea that coevolutionary interactions have kept the extinction rate fairly constant over a long period of time. We label such dynamics Red Queen interactions after the character in Through The Looking Glass, by Lewis Carroll. The Red Queen told Alice, `Now here, you see, it takes all the running you can do, to keep in the same place.' To van Valen (1973), the Red Queen's message for evolution was that no matter how much one species adapted to what the other was doing, the other would change just as much in response, with the result that there would be no net long-term improvement in fitness. They would remain locked in an arms race with no exit. Red Queen: coevolutionary dynamics in which the participants struggle forever against each other with no longterm reduction in extinction probability.
4 41: 18 Coevolution Parasite allele cr Host allele Generation Figure 18.5 Cycling of parasite and host allele frequencies as a result of frequency-dependent selection (courtesy of Curt Lively). The dark rectangle indicates the portion of the cycle where the common host genotype is having serious problems with the parasite because the specialized parasite genotype is over 50%. The light rectangle indicates the portion of the cycle where the host is not having the problem because the specialized parasite genotype is at low frequency. (From Clay and '<over 1996.) In Chapter 8 (pp. 192 f.) we discussed such arms races in the context of host pathogen interactions for the maintenance of genetic variation in genes for virulence in the pathogen, for resistance in the host, and for sexual reproduction in both. We revisit that issue here because it is such a clear example of coevolution linking genetic changes in one species to genetic changes in another. Frequency-dependent selection makes life difficult for common virulence and resistance types and should maintain offset cycles of frequencies of virulence and resistance alleles in host and pathogen (Figure 18.5). Frequency-dependent selection does maintain very high levels of genetic diversity many alleles at each of many loci in the vertebrate immune system. Considerable genetic variation for genotype-specific virulence and resistance has also been found in crustacean and plant host pathogen pairs, including the water flea Daphnia (bacterial pathogen Pasteuria; Carius et al. 2001), the ragwort Senecio (powdery mildew pathogen Erysiphe), the soybean Glycine (rust pathogen Phakopsora), the flax Linum (rust pathogen Melampsora), and the cress Arabidopsis (mildew pathogen Perenospora; Clay and Kover 1996). There is thus suggestive genetic evidence for dynamic interactions well described as a coevolutionary arms race: each time the pathogen improves its attack the host changes in a way that improves its defense, which then causes a change in the pathogen that improves its attack. Whether those interactions are a sufficient explanation for the maintenance of sexual reproduction in host and pathogen remains a plausible hypothesis that has not yet been strongly confirmed (see Chapter. 8, pp. 192 ff.).
5 Principles of coevolution 1 is n. :e ie ze!.11 is a re ly Evolution of niche width and location The niche width of competitors can also be seen as the host range of pathogens, parasites, and herbivores the number of different species they attack, and therefore the number of different species on which they could encounter competitors. How many different species should a consumer eat or infect? The answer is couched in terms of the balance of factors favoring specialization or generalization and the constraints on ability to evolve in one direction or the other. The classical view of the evolution of niche width in competitors is that interspecific competition will cause competitors to evolve to reduce the impact of that competition. They are thought to do so by diversifying to use different resources. As they evolve to reduce interspecific competition, they specialize on using different parts of the available food supply. In so doing, they are at least not decreasing, and perhaps increasing, the impact of intraspecific competition, for as they avoid the other species they will encounter more of their own species. Thus the rate of this process, and the degree to which it will result in narrower, more-specialized niches, depends on the balance of inter- and intraspecific effects. A pattern consistent with competition-driven niche shifts is called character displacement. Character displacement is seen by comparing closely related competitors in sympatry and allopatry. If they differ more in sympatry than in allopatry, then one explanation is that competition has caused the divergence. This explanation becomes more plausible if the traits that change are functionally related to competitive ability. As competitors specialize, another important effect comes into play. It is often, but not always, the case that a jack of all trades is a master of none, and a master of one trade is poor at the others. A superb specialist is often a poor generalist: when the reproductive success of a species increases as it becomes adapted to one resource, its reproductive success on other resources decreases. This effect is strongly confirmed by serial transfer experiments on the evolution of virulence: as a pathogen adapts to a new host it loses its ability to function on the old host. And it is clearly present in cases where the consumer has had to evolve specialized adaptations to overcome specialized defenses in the resource. There is then a tradeoff in performance on different resources. If the only effect determining niche width were a tradeoff in performance on different resources, one might expect all species to become specialized. There are at least four reasons why this does not happen: Intra-specific competition can limit the benefits of specialization. Organisms often have to eat different things at different stages of their development if only because they start smaller and end larger. Some resources are only intermittently present or exist in a geographical mosaic in which they do not overlap with the consumer everywhere; they must then be supplemented with alternatives if the consumer is to survive. Character displacement: Competing species differ in competition-related traits more in sympatry than they do in allopatry. Competition is then thought to have displaced the sympatric state from the allopatric state.
6 18 Coevolution Another consequence of spatial heterogeneity is that it provides the contras ing selection pressures in different places that maintain both niche width an genetic variation within the focal species. Niche width usually, but n always, evolves to match the amount of variation present in the environmen with homogeneous environments containing specialists and heterogeneo environments containing generalists (Kassen 2002). For all these reasons, we should expect specialization to evolve often, but no always. Both extreme specialists and extreme generalists are interesting cases, for they represent evolutionary histories with unusual combinations of effects. Evolutionary transitions among parasitism, mutualism, and commensalisms Vertical transmission: Transmission of parasites or pathogens from host parent to host offspring, often during host reproduction. Horizontal transmission: Transmission of parasites or pathogens to other organisms at times and places not necessarily associated with host reproduction or relationship. The nature of a coevolutionary interaction is not written in stone. The impact of the partners on each other can evolve, even to the extent of changing sign, at least from to 0. Such evolution of the interaction is particularly well understood in the case of hosts and pathogens (see next chapter, pp. 488 ff.). If the pathogen is vertically transmitted from host parent to host offspring, then the reproductive success of the pathogen depends upon the survival and reproduction of its host. The expected result is that the virulence of the pathogen will evolve downwards, eventually to zero. In the process a host pathogen interaction will have been converted into a commensalism, from + into +0. Such complete attenuation of virulence is only expected with strict vertical transmission. Where there is horizontal transmission of the pathogen from host to unrelated host, independent of host reproduction, then virulence is expected to stabilize at an intermediate level that balances reproductive success within one host with transmission probability between hosts. It does not pay a pathogen to kill a host so quickly that transmission is unlikely. These effects were seen clearly when a flea-transmitted viral disease, myxomatosis, was introduced from Europe to Australia to control the exploding population of introduced rabbits (Fenner and Ratcliffe 1965). Samples of the virus were frozen for later reference when it was introduced. At the beginning the disease was extremely virulent, but as it spread its virulence decreased because the strains that were most virulent killed their hosts before they could be transmitted. Comparison of the frozen with the evolved strains demonstrated that the reduction in virulence was due both to a decrease in the virulence of the virus when tested on a standard host and to an increase in the resistance of the rabbits. Virulence did not evolve to zero; it stabilized at an intermediate level. There is another way for coevolution to convert a parasite host relation into a commensal relation. A commensal +0 relation can evolve from a + parasite host interaction when genes in the host for resistance compete with genes for tolerance. A gene for resistance cannot take over the population completely because as it becomes more frequent, the incidence of infection declines, which
7 Striking outcomes of coevolution and its absence 'duces the advantage of resistance. If there is any cost to resistance, resistance cries cannot be fixed, and resistance genes alone cannot eliminate diseases. In _ ontrast, if a host gene for disease tolerance sweeps through a population, it increases the number of hosts that can serve as habitat for the disease, the incidence of the disease increases, and that in turn creates positive frequencydependent feedback on the frequency of the tolerance gene, which rapidly goes to fixation. As predicted by this hypothesis, resistance traits tend to be polymorphic and tolerance traits tend to be fixed in field studies of interactions between diverse plant species and rust fungi (Roy and Kirchner 2000). The evolution of mutualisms has attracted a great deal of attention because the principles involved also explain the evolution of cooperation between unrelated individuals. The principle theoretical tool used in these investigations has been game theory. In this kind of theory one imagines that both partners can exist in two versions, cooperators and defectors, and that there are certain payoffs for cooperating and for defecting. The payoffs are delivered in the form of changes in reproductive success. The analysis then asks, under what conditions will a rare cooperator mutant be able to spread into a population composed mostly of defectors? If it can spread, then cooperation will increase, and if it can take over the population and go to fixation, which is a separate question, then a cooperation will have evolved uniformly throughout the population. There are two conditions that greatly facilitate the evolution of cooperation (Doebeli and Knowlton 1998): increased investments in the partner must yield increased returns, and the partners must be close to each other in space. Cooperation spreads more easily when contacts between cooperating partners are more frequent than random, and spatial contiguity is one effective way to achieve this. Under these conditions, it is surprisingly easy for mutualism to evolve. Thus the barrier to the evolution of mutualisms may be not the evolution of the interaction but the initial penetration of host defenses. Once the two partners are reliably associated closely in space and exchanging some resource with even a very small initial mutual benefit, the intensity of the interaction will be selected to increase to the benefit of both. Such a process could take an interaction that was very close to 00 and convert it rapidly into one that was strikingly + +. Striking outcomes of coevolution and its absence Volumes have been written on the outcomes of coevolution, and it is not easy to make an illustrative selection from the abundance of striking examples. We have chosen four classic interactions: mimicry in butterflies, the specialized active pollinators of yuccas and figs, leaf-cutter ants and their domesticated fungi, and the introduction of foreign pathogens and predators to naïve ecosystems. In KEY CONCEPT Coevolution has produced striking examples of complicated adaptations embedded in ancient clades.
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