Alternative Mating Tactics and Evolutionarily Stable Strategies 1

Transcription

1 AMER. ZOOL., 24: (1984) Alternative Mating Tactics and Evolutionarily Stable Strategies 1 WALLACE J. DOMINEY Museum of Zoology and Division of Biological Sciences, University of Michigan, Ann Arbor, Michigan SYNOPSIS. Difficulties with applying Evolutionarily. Stable Strategy (ESS) methodology and terminology to alternative mating behaviors (in which some males in local populations adopt strikingly different, often non-competitive, behavioral patterns) are reviewed. Definitions for "tactic" (behavioral phenotype) and "strategy" (evolved set of rules for expressing tactics) are given. Inconsistent and incorrect applications of "mixed," "pure," and "conditional" ESSs are discussed. Cases of condition-dependent alternative mating tactics are reviewed. Because most alternative behaviors are condition dependent, neither their population-wide nor individual fitness contributions are expected to equal the fitness contributions of "primary" tactics. Individuals should, however, switch tactics at "equal fitness points." A particular conditional tactic will persist when its maintenance cost (genetic or physiological) is less than its fitness contribution. In only exceptional cases are the fitness contributions of tactics expected to be equal: 1) genetic polymorphisms, 2) stochastic "mixed" ESSs, 3) frequency-dependent choice and, 4) arbitrary assessment. Although alternative tactics may occur in cases of genetic polymorphism or genetic equipotence, most mating tactics probably occur when continuous heritable variation in underlying conditional strategy exists. Selection for genetically influenced "roles" (genetic background) may also uncover apparent heritability. INTRODUCTION In species in which the typical male mating pattern is highly competitive, individual males often adopt strikingly different, noncompetitive behavioral patterns, often termed alternative mating behaviors (reviewed in Alcock, 1979a; Cade, 1980; Rubenstein, 1980; Dunbar, 1982; Thornhill, 1981). For example, individual male fish may mimic the behavior of females rather than compete for nesting territories (Dominey, 1980). Similarly male crickets (Cade, 1980) or frogs (Emlen, 1976) may remain silent and attempt to mate with females attracted to territorial males. How this type of discontinuous variation in male mating behavior is maintained has received considerable theoretical attention. Unfortunately, the terminology and logic used have not always been consistent. Cade (1980) called for a consistent terminology, and he and Rubenstein (1980) followed Dawkins' (1980) lead in applying ESS (Evolutionarily Stable Strategy) terminology and methods to the analysis of alternative mating behaviors. In this paper, I argue that ESS meth- 1 From the Symposium on Alternative Reproductive Tactics presented at the Annual Meeting of the American Society of Zoologists, December 1982, at Louisville, Kentucky. odology is inappropriate for analyzing alternative mating behaviors in some cases, as when the fitness contributions of the alternative behaviors are not negatively frequency dependent. Other misapplications of ESS methodology are discussed, including incorrectly equating the coexistence of alternative behaviors with equality of their fitness contributions. Finally, I discuss the exceptional cases in which the fitness contributions of alternative behaviors are expected to be equal, and the probable genetic influence over alternative mating behaviors. To begin, I give brief definitions of terms that are commonly used when applying ESS methodology, as well as a definition of "tactic." The definitions are justified and discussed in the text. APPLICATION OF ESS THEORY TO MATING TACTICS Definitions STRATEGY: A set of rules stipulating which alternative behavioral pattern, of several stated options, will be adopted (or with what probability) in any situation throughout life. With respect to the stated options, each individual must have one and only one strategy, and different strategies must represent differences in genotype. TACTIC: One of several stated behavioral options (phenotypes). 385

2 386 WALLACE J. DOMINEY ESS (EVOLUTIONARILY STABLE STRATE- GY): A strategy such that if a critical proportion of the population adopt the ESS then no different strategy can produce, on average, a higher fitness. MIXED (STOCHASTIC) ESS: A strategy in which the tactics are stochastically assigned. Either individuals adopt several tactics probabilistically, e.g., "'guard' with probability p, 'sneak' with probability q," or individuals are randomly assigned permanently adopted tactics ("guard" or "sneak") with probabilities p and q. A strategy specifying a mixture of tactics is not automatically a "mixed strategy" (see "pure strategy" below). PURE STRATEGY: A strategy which contains no probabilistic statement. A pure strategy is not necessarily a strategy in which only one tactic is expressed. For example, "in situation A 'guard'; in situation B 'sneak'" is a pure strategy, not a stochastic "mixed" strategy. CONDITIONAL STRATEGY: A pure strategy specifying two or more conditiondependent tactics. Tactics or strategies'? The above definitions are consistent whenever possible with those of Dawkins (1980) and Maynard Smith (1982). The only significant deviation from typical ESS usage is the explicit splitting of "strategy" into a set of rules or "strategy" and phenotypic expressions or "tactics." ESS theorists, though aware of the potential ambiguity (Brockmann et ai, 1979), have usually used "strategy" to indicate both the strategy (decision rules) and the tactics (phenotypic outcomes). As will be shown later, this ambiguity can lead to confusion. As one example, all alternative strategies are assumed to derive from different genotypes (Maynard Smith and Parker, 1976; Maynard Smith, 1982), but alternative tactics can be expressed by genetically identical individuals. "Tactic" was chosen to indicate an alternative behavioral phenotype because in common speech "tactic" implies a specific action, while "strategy" implies a long term objective (Dunbar, 1982). Also, alternative mating behaviors are frequently referred to as alternative mating "tactics" (Jackson, 1978; Wirtz, 1978; Waage, 1979; Dominey, 1980;Gwynne, 1980;Thornhill, 1981; Waltz, 1982). Other suggestions such as "actions" (Maynard Smith and Parker, 1976) or "outcomes" (Dawkins, 1980; see also Brockmann et al., 1979) are not commonly used in either the ESS literature, or in the alternative mating behavior literature. Alternative to what? In some sense all mutually exclusive behaviors are "alternative tactics" since the common goal of all behavior is increased inclusive fitness. Typically, however, when we speak of alternative tactics we refer to behaviors which are functionally equivalent, directed towards a specific goal like mating or foraging. Other restrictions are sometimes imposed, e.g., "genuine functional alternative" to indicate a tactic which is not situation dependent (Brockmann et al., 1979), and "adaptive alternative tactic" to indicate a tactic which makes an equal contribution to fitness (Rubenstein, 1980). More generally, however, alternative tactics are discontinuous, mutually exclusive behaviors that serve the same function. Because alternative tactics are defined only with respect to stated alternatives, a complete list of tactics must be made. In any relevant situation, then, we assume that one of the tactics is the optimal response, and require the strategy to designate which tactic is to be expressed. Alternative strategies are thus defined by changes in the specifications indicating when various tactics will be employed. As in the case of tactics, a complete list of alternative strategies must also be made. Strategies can only be evolutionarily stable with respect to stated alternatives (Dawkins, 1980). Pure or mixed strategy? For ESS theorists, "mixed" strategies are strategies specifying stochastic (probabilistic) expression of tactics (Dawkins, 1980; Maynard Smith, 1982), while "pure" strategies are those without stochastic elements, regardless of the number of alternative tactics specified. Unfortunately, "pure" and "mixed" have commonsense connotations which do not conform to their

3 ESS definitions. Pure strategies are sometimes taken to be strategies specifying single tactics, while mixed strategies are taken to specify multiple tactics without regard to conditional or probabilistic expression of tactics (e.g., Barash, 1981; Thornhill, 1979). In fact, there is a precedence for this usage since Trivers (1972) referred to a "mixed strategy" of aiding a primary mate in parental care duties while seeking extrapair copulations. The literature on extrapair copulations in avian species has many examples following Triver's lead (e.g., Beecher and Beecher, 1979; McKinney and Stolen, 1982). The inconsistent use of "mixed strategy" has in fact caused misunderstandings. Cade (1980) argued that Beecher and Beecher (1979) had prematurely claimed to document a mixed strategy sensu ESS models, while in fact, Beecher and Beecher were documenting a mixed strategy sensu Trivers. Likewise, Evans and O'Neill (1978), Clutton-Brock et al. (1979) and Kodric-Brown (1983) apparently consider any mixture of mating tactics in Hymenoptera, red deer, and pupfish, respectively to be a "mixed strategy" while citing Maynard Smith and Parker (1976). The difficulty becomes most acute when authors apply the conclusions derived from mixed ESS models to any strategy having a mixture of tactics. In particular, unlike most tactics, the stochastically expressed tactics of a mixed ESS are expected to produce equal fitnesses (see below, "When should fitness contributions balance?"). For clarity and consistency with usages already present in the literature, I agree with Dawkins' (1980) suggestion that "stochastic" is a better term than "mixed" when refering to strategies having stochastically expressed tactics. Perhaps "stochastic 'mixed' strategy" should be used when referring to a mixed ESS unless a full transition to "stochastic strategy" is made. Two classes of stochastic "mixed" strategies are possible. First, in all relevant circumstances, individuals may express with certain probabilities either alternative tactic. Second, permanently adopted alternative tactics are assigned probabilistically to individuals to be expressed in all relevant circumstances. This latter case has often been described as an ESS comprised MATING TACTICS AND ESSS 387 of multiple pure strategies (e.g., Maynard Smith, 1982). In the terminology adopted here, such a case would be an ESS comprised of multiple tactics, not multiple strategies. As used here, strategies cannot be stochastically assigned because they represent genotype differences, nor can one strategy contain other strategies. Conditional or pure strategy? Although pure strategies need not specify single tactics, "pure strategy" has commonly been used to indicate one of several single tactic strategies occurring in a stable mixture: a genetic polymorphism. Here, different tactics represent different strategies. In such a case, no ESS exists since no one strategy is stable, although the population may be in an "evolutionarily stable state" containing individuals having different single tactic strategies yielding equal fitnesses (Dawkins, 1980; Maynard Smith, 1982). This situation is mathematically (but not biologically) similar to the stochastic "mixed" ESSs described above. When considering cases having only two alternative tactics, if a stochastic "mixed" strategy is stable, then so is the corresponding mixture of pure single tactic strategies. With more than two tactics, however, this conclusion no longer holds (Maynard Smith, 1982). In contrast to the above usage, a pure strategy may specify multiple tactics. For instance, "'guard' if large, 'sneak' if small" is a pure strategy (Maynard Smith, 1982). Such strategies have sometimes been referred to as "conditional strategies," usually in an attempt to emphasize that the strategy in question specified the conditions under which the tactics were to be expressed. By definition, all pure strategies meet this criterion, although the conditions specified by a pure single tactic strategy must be taken as "in all relevant circumstances." Some authors, however, incorrectly contrast pure with conditional strategies. "Pure" has been used as if it referred only to single tactic strategies specifying a genetically determined tactic while "conditional" has been used as if it referred only to strategies specifying multiple tactics practiced by genetically equipotential

4 388 WALLACE J. DOMINEY individuals. There are several difficulties with this usage. First, as seen above, pure strategies can specify either multiple or single tactics; all conditional strategies are pure strategies. Second, pure strategies specifying permanently adopted tactics do not necessarily indicate that individuals adopting different tactics differ in genotype. For instance, the same genetic substrate for the pure strategy "if large at sexual maturity 'guard' throughout life, if small 'sneak' throughout life" may be present in every individual. Third, conditional strategies do not always specify that individuals practice multiple tactics. The strategy given immediately above is both pure and conditional, and specifies that individuals practice only single tactics throughout life. Finally, the presence of a conditional strategy does not indicate that all individuals have the same strategy as suggested by Cade (1980). Strategies can differ not only by specifying different tactics, but also by requiring different conditions for the expression of the same tactics. Alternatives to the conditional strategy "'guard' at size x, 'sneak' at size x I" might be to switch from sneaking to guarding at size x + 1, or size x + 2, and so forth. MUST FITNESS CONTRIBUTIONS BALANCE? Gadgil (1972) was the first to suggest that males practicing different tactics might have equal fitnesses. He considered cases in which individuals practiced permanently adopted tactics including morphological as well as behavioral differences. Gadgil argued that escalating investment in costly male characteristics (such as horns) would continue until an equally fit alternative (e.g., hornless form) would be possible having lower average mating success but higher average survivorship (see also Charlesworth and Charlesworth, 1975; Gadgil and Taylor, 1975). "Fitness balancing," or the equalization of the average fitnesses of the two male types, occurred because the fitnesses of the two tactics were negatively frequency dependent. Thus, Gadgil assumed that males differing in tactics differed in genotype, males adopting different tactics had different underlying strategies. In general, at any equilibrium, alternative strategies must produce equal fitness contributions. Otherwise, we expect the strategy producing the greater fitness to replace the alternative. The failure of one strategy to replace an alternative can be due to negatively frequency-dependent fitnesses, or can result from heterozygote advantage, fluctuating selection, the effects of environmental heterogeneity, or any other mechanism for maintaining genetic variability. The extension of "fitness balancing" arguments from permanently adopted tactics representing differences in underlying strategy to tactics generally came with the advent of ESS models. In particular, the tactics specified by a stochastic "mixed" ESS were expected to contribute equally to fitness (Maynard Smith and Parker, 1976). Now, even tactics which were not permanently adopted and which did not represent differences in underlying strategy could be "equal fitness variants." In many subsequent papers (e.g., Alcock, 1979a;Brockmann^a/., 1979; Cade, 1980; Rubenstein, 1980; Warner and Hoffman, 1980; Barash, 1981; Perrill et al, 1982) a transition was made from the possibility that the fitnesses of alternative tactics could be equal to statements that the existence of alternative tactics required fitness balancing. Some authors qualified their statements; for example Brockmann etal. (1979) quickly added that tactics resulting from conditional strategies need not produce equal fitnesses. Most others explicitly considered cases in which alternative tactics need not balance, and hence some of the confusion has undoubtedly resulted from the use of "strategy" to refer to both strategies and tactics. Although strategies must generally produce equal fitnesses, tactics do not share this restriction. As Dawkins (1980) pointed out, most alternative mating tactics are likely to be condition dependent, resulting from conditional strategies. With conditional strategies, "there is no reason to expect (the tactics) to be equally successful" (Dawkins, 1980). Alternative tactics should be expressed as the optimal response to particular situations, and depending on the distribution of these situations some tactics may contribute little to total fitness. In view of this, there has been an overemphasis of

5 MATING TACTICS AND ESSS 389 the importance of fitness balancing in the alternative mating literature. A notable exception to this trend is the review by Thornhill (1981) in which he details his work on scorpionflies (Panorpa). Male scorpionflies use three alternative mating tactics. Males either compete for dead arthropods, secrete saliva, or attempt forced copulation. The dead arthropods and saliva secretions are used as nuptial gifts which if accepted by females facilitate copulation. Thornhill showed that males prefer controlling dead arthropods over the other two tactics. In the absence of dead arthropods, however, or if prevented access to them by male-male competition, males would switch to secreting saliva or forced copulation. The reverse, switching from less preferred to more preferred tactics also occurs as Thornhill showed by removing males which controlled resources (dead arthropods or saliva). Additionally, males did not secrete saliva unless they had recently eaten. Given the condition-dependent expression of these alternative mating tactics, it is likely that their fitness contributions would not balance; this is exactly what Thornhill found. Males controlling dead arthropods had not only the highest mating success, but also the lowest probability of being eaten by spiders. Males attempting forced copulations had the lowest net fitness gain, and those secreting saliva were intermediate. In the section that follows, I present many additional examples of condition-dependent alternative mating tactics in which neither the fitness contributions to individuals, nor the population-wide fitness contributions of the tactics are expected to balance. CONDITION-DEPENDENT TACTICS Perhaps the largest class of conditiondependent tactics can be traced to malemale competition. The scarcity of alternative tactics at low population densities in many organisms (Brown and Pierce, 1967; Alcock et al., 1977; de Boer, 1978; Cade, 1980; Warner and Hoffman, 1980; Sullivan, 1982; Kodric-Brown, 1983) is usually attributed to reduced competition for mates. More directly, low dominance status (Constanz, 1975; Cox and Le Boeuf, 1977; Foster, 1977), past losses in aggressive encounters (Fellers, 1979; Hamilton, 1979; Gwynne, 1980; Thornhill, 1981), or aggressive vocal exchanges (Perrill et al., 1982) can lead to the adoption of alternative tactics. In many anurans (Brown and Pierce, 1967; Perrill et al., 1978, 1982; Fellers, 1979; Sullivan, 1982) and insects (Cade, 1980) removal of dominant calling males causes parasitic non-calling males to switch tactics. Similar changes from one mating tactic to another follow the removal of dominants in fish (Barlow, 1967; Constanz, 1975). In addition to responding to male-male competition, males may switch mating tactics due to the presence or absence of necessary resources. In the absence of dead arthropods, scorpionflies switch to secreting saliva or to forced copulation (Thornhill, 1981). Also, males must have recently eaten to secrete saliva. Horse botflies prefer to intercept females at equine hosts, but if horses are absent upon emergence, males await females at hilltops (Catts, 1979). Similarly, some male syrphid flies search for females at oviposition sites, others at feeding sites (Maier and Waldbauer, 1979). Male damselflies have been shown to change from non-territorial to territorial tactics as new oviposition sites are provided (Waage, 1973). The reverse, that is, changing from territorial to non-territorial tactics when territories are lost, is probably equally as common. If the presence of suitable females can be considered a resource, then forced copulation in ducks is "resource-dependent" (McKinney and Stolen, 1982) as are "guarding" or "searching" tactics in bull elephants (Barnes, 1982). A related group of opportunistic switches in courtship tactics occur in male fish (Farr, 1980) and newts (Verrell, 1982) in response to the receptivity behavior of females. Similarly, male damselflies (Waage, 1973) and spiders (Jackson, 1978) employ different tactics depending on whether females are located on or off the male's territory. Some tactics are not adopted opportunistically, but are differentially expressed according to age. The typical pattern is for younger males to adopt "sneak" or submissive tactics while older males are territorial or dominant. Usually the exact ages

6 390 WALLACE J. DOMINEY of the individuals are not known. Examples of age-specific tactics have been reported in fish (Warner et al., 1975; Dominey, 1980), mammals (Le Boeuf, 1974; Cox and LeBoeuf, 1977;Clutton-Brock^a/., 1979), amphibians (Howard, 1978), and birds (Lill, 1974; Wiley, 1974). As with age-dependent expression, sizedependent expression of mating tactics is common. The typical pattern is for small males to practice submissive or "sneak" tactics while larger males are dominant or territorial. Examples are found in fishes (Constanz, 1975; Warner et al., 1975; Kodric-Brown, 1977; Wirtz, 1978; Dominey, 1980; Warner and Hoffman, 1980; Kodric-Brown, 1981); amphibians (Emlen, 1976; Howard, 1978); reptiles (Trivers, 1976); insects (Alcock et al, 1977; Borgia, 1980; Eberhard, 1980, 1982; Thornhill, 1981; Severinghaus et al., 1981), and spiders (Christenson and Goist, 1979). In some cases the effects of age and size can be separated (e.g., Lill, 1974; Dominey, 1980) but in others, especially in organisms with indeterminate growth (e.g., bullfrogs, Emlen, 1976; Howard, 1978) size and age can be expected to act together. Size differs from most other conditions influencing the expression of alternative mating tactics in that size differences at sexual maturity may commonly lead to the permanent adoption of single tactics. In such cases, although the alternative tactics are not at present conditionally expressed, the choice of permanently adopted tactic could have been condition dependent at some time during ontogeny. Environmental conditions during ontogeny might "lock" individuals into one or another developmental pathway. This type of ontogenetic switch based on size may be common in insects in which adult size is fixed, perhaps determined by larval food abundance as suggested for Centris bees (Alcock, 19796) and beetles (Eberhard, 1982). WHEN SHOULD FITNESS CONTRIBUTIONS BALANCE? Most alternative mating tactics are condition dependent. As such, neither their fitness contributions population-wide, nor to individuals, are expected to be equal. Consider two hypothetical age-dependent tactics. Males "sneak" the first year they attempt reproduction, and "guard" thereafter. Obviously, both tactics can persist even though "sneaking" might contribute relatively little to individual or populationwide fitness. Similarly, alternative tactics which are expressed only in relatively rare situations, such as opportunistic forced copulation, may persist while contributing little to total fitness. Some conditiondependent tactics will be "best of bad job" tactics (Dawkins, 1980) in which individuals permanently disadvantaged in competition adopt alternative tactics, while others are simply situation-dependent, occurring whenever the appropriate situation arises. Indeed, apparent unequal fitness contributions of alternative tactics have been reported (e.g., Boness and James, 1979; Christenson and Goist, 1979; Gwynne, 1980; Thornhill, 1981; Kodric- Brown, 1983). However, the fitness gains attributable to alternative tactics are difficult to determine. Both the relative lifetime mating contribution and the relative lifetime cost of expression should be measured. Contrary to most condition-dependent tactics, four classes of alternative tactics are expected to produce equal fitness gains: tactics resulting from 1) genetic polymorphisms, 2) stochastic "mixed" ESSs, 3) frequency-dependent choice, or 4) arbitrary assessment. I argue below that each of these will be rare. Genetic polymorphisms The first case in which the fitness contributions of tactics are expected to balance is when individuals practice different, genetically distinct tactics throughout life, such as proposed by Gadgil (1972). Because such tactics represent differences in underlying strategy, the balancing of the fitness contributions of these tactics occurs as a balancing of strategies. Permanently adopted tactics, genetically mediated or otherwise, are rare. The best examples occur in ruffs (Hogan-Warburg, 1966; van Rhijn, 1973), sunfish (Dominey, 1980), horned beetles (Eberhard, 1980), and fig wasps (Hamilton, 1979). Notably all these mating tactics include morphological differentiation which implies a cost

7 MATING TACTICS AND ESSS 391 to switching tactics. Purely behavioral tactics are unlikely to be permanently adopted because opportunistic switching should, at least occasionally, be beneficial and the cost of retaining flexibility in behavioral response should not be large. In general, condition-dependent switches should be favored over condition-blind genetic control (West-Eberhard, 1979; Eberhard, 1982). The only exceptions will be cases in which no useful assessment of the appropriateness of switching tactics can be made. No permanently adopted tactic is known to represent a difference in genotype (strategy), although Hamilton (1979) showed that fig wasp morphs were equally fit which may indicate a genetic polymorphism. The horned beetles are believed to be condition dependent (Eberhard, 1980, 1982), and preliminary data (F,s) indicate that the sunfish mating types are not due to genetic differences. Genetic mediation is required before fitnesses are expected to balance. Stochastic "mixed" ESSs The second case when the fitnesses of tactics are expected to balance is when tactics are strictly stochastically expressed and their fitnesses are negatively frequency dependent. Such tactics are expected to reach equality of fitness contributions as shown by stochastic "mixed" ESS models (Maynard Smith and Parker, 1976). Stochastic "mixed" ESSs are commonly of the form "'guard' with probability p, 'sneak' with probability q." Whatever the starting frequencies, p and q, if one tactic currently contributes more to fitness, an alternative strategy specifying an increased probability of expression of that tactic should invade. However, as the frequency of occurrence of the more successful tactic increases, its average fitness contribution decreases due to negative frequency dependence. Eventually, its frequency will be held at the evolutionarily stable frequency when it contributes equally to fitness. The evolutionary stability of such a stochastic "mixed" ESS is only against stated alternative strategies (Dawkins, 1980), namely those specifying different proportions of the same stochastically expressed tactics. In most cases, however, the "strategy set" should include conditional strategies in which some relevant condition is assessed. Any novel alternative strategy stipulating condition-dependent expression which increased total fitness should be selected, and should invade a population in which individuals expressed tactics probabilistically (see also, Eberhard, 1982). Because of the likelihood of condition-dependent mating tactics, Dawkins (1980) has suggested that a stochastic "mixed" mating strategy should be a hypothesis of last resort. Cade (1980) has argued that as additional research on the conditional expression of mating tactics is completed, deletion of the stochastic "mixed" strategy concept with respect to mating tactics may become desirable. Generally, stochastic tactics are only expected when the costs of assessing relative fitness gains are high, or when assessment cannot accurately predict relative fitness gains. Such cases may occur in n-person games or cases of "playing the field" (Maynard Smith, 1982). Frequency-dependent choice The third case in which fitness balancing is expected is when the fitnesses of the tactics are negatively frequency dependent, and a conditional strategy specifies tactics according to their relative frequencies in the population (Brockmann and Dawkins, 1979). For instance, individuals might assess the relative number of males "guarding" or "sneaking" (perhaps by encounter rates) and then "guard" or "sneak" according to which tactic would produce the highest fitness gain. Since many alternative mating tactics intuitively have a frequency-dependent component to fitness, some switching according to the local frequencies of various tactics may be commonplace. Noncalling toads switching to calling when calling males are removed (Sullivan, 1982) may be such an example. However, any asymmetries in individuals or in conditions favorable to the expression of one tactic or another, as argued above, would act against the complete equalization of the fitnesses of the two tactics. It would be interesting to consider the interaction between frequency-dependent choice, tending to bal-

8 392 WALLACE J. DOMINEY ance the fitness gains of tactics, and internal and external asymmetries tending to favor different fitness gains for different tactics. Arbitrary assessment Finally, tactics are expected to produce equal fitnesses in cases in which their condition dependence bears no relation to the likelihood of success in a particular tactic (Brockmann, personal communication). Maynard Smith (1982) gives such a case for age-specific tactics in which age is not used as an indicator of asymmetric potential for success, but as an arbitrary, randomizing device. Tn such a case, and given negative frequency dependence of the fitnesses of the tactics, natural selection should adjust the switch point (age) so that the average individual fitness contributions of the tactics are equal. The evolution of such a randomizing device seems unlikely. Assessments based upon internal or external conditions which do provide some prediction of success should replace arbitrary randomizing devices. There may, however, be a continuum of effectiveness of various assessments ranging from near perfect prediction of success to very little correlation between assessment conditions and the success of the tactic. If the correlation was, in fact, zero then the conditionally expressed tactic would resemble in some respects a stochastically expressed tactic. At zero correlation, probabilistic expression yielding equal fitnesses should invade by drift or due to the cost of assessing the relevant conditions. GENETIC CONTROL OF MATING TACTICS Individuals which practice different mating tactics do not necessarily differ in underlying strategy (genotype). Even individuals practicing different permanently adopted tactics may be genetically equipotential, perhaps having been locked into one or another fixed alternative pathway early in ontogeny. In cases in which individuals were in fact genetically equipotential, measuring the apparent contribution to "fitness" of alternative tactics gives little insight into the maintenance of the alternatives. Regardless of the relative contributions of the tactics to the fitnesses of individuals, the next generation would again contain genetically equipotential individuals. The strongest contrast to genetic equipotence would be a one-to-one correspondence between permanently adopted alternative tactics and differences in genotype: a genetic polymorphism. In this case, the fitness contributions of the alternatives are critical because unless some mechanism for maintaining genetically distinct forms is present, the more successful tactic is expected to replace the less successful. Thus far, I have considered two contrasting cases, genetic equipotence and genetic polymorphism, Intermediate cases, however, can exist in which males may simply be more likely to exhibit one or another tactic, given the same circumstances (Alcock, 1979a). This third situation is probably representative of the vast majority of alternative mating tactics. Conditional expression of alternative mating tactics has often incorrectly been equated with genetic equipotence. This assumption has focused attention away from the type of genetic differences (strategies) which are likely to influence the adoption of most alternative mating tactics. Even individuals expressing the same condition-dependent tactics may differ genetically as to the precise conditions which will elicit particular tactics. For instance, genetic variants might use or emphasize different cues in switching from one tactic to another, or might switch at different points along a gradient of a single cue. To the extent that there is genetic variation in these "switch points," multiple conditional strategies exist. As with so many other ecological and behavioral characteristics, I expect heritable differences in switch points, and thus, nearly continuous variation in underlying strategy, even when the phenotypes are discontinuous. Given continuous variation in underlying strategy, it is not surprising that selection experiments would uncover heritability when alternative mating tactics are used as the selected phenotypes. In an important study, Cade (1981) demonstrated that "calling" and "non-calling" behaviors were highly heritable in field crickets (Gryllus integer). Though he suggested that calling

9 MATING TACTICS AND ESSS 393 and non-calling behaviors were probably "separate genetic strategies," it seems more likely that there was continuous variation in underlying strategy. This is particularly the case since calling behavior is condition dependent (Cade, 1980). The presence of continuous variation in underlying strategy points to the inadequacy of describing such a situation as a conditional ESS (or any ESS). As argued above, the presence of many conditional strategies is likely, and is equally as stable as a single conditional strategy (ESS). Similarly, any combination of pure and stochastic "mixed" strategies that achieves the stable mix of tactics is also an "evolutionarily stable state" (Brockmann and Dawkins, 1979). Calling such a case an ESS is misleading, although ESS methodology can be applied to some types of continuous variation in underlying strategy. An example would be cases in which strategies are taken to correspond to some continuous variable, like "staying time" at a resource (Maynard Smith and Parker, 1976). Aside from heritability due to variation in underlying strategy, selection experiments may also indicate apparent heritability of tactics due to selection on genetic background. In the terminology of ESS theorists this is equivalent to selection on those "roles" which are influenced by genes. Roles are defined as internal or external conditions which affect the adoption of alternative tactics. Examples of roles include "territory owner" vs. "interloper," and "large size" vs. "small size" (Maynard Smith and Parker, 1976). Any genes influencing roles must be independent of the genes influencing strategy (Maynard Smith and Parker, 1976), otherwise the role would be part of the strategy. This is equivalent to assuming that there is no pleiotropy or linkage disequilibrium between the genes for the strategy, and the genes, if any, for the roles (Maynard Smith, 1982). Returning to field crickets, imagine genetic variation in cricket body size which is independent from a conditional strategy stipulating the adoption of "non-calling" at some small size, x. Selection experiments using non-calling as the selected phenotype would unknowingly select for small body size, even though the genes influencing body size were independent from those determining the switch point, x. In this situation, although the strategy per se was not heritable, selection on genetic background (size) would produce an apparent heritability. The now small crickets would call less frequently. In practice distinguishing the genetic variation underlying roles from that underlying strategies will be difficult, but potentially important given that we seek to understand how animals choose behavioral options when faced with certain intrinsic and extrinsic conditions. AN ALTERNATIVE VIEW OF ALTERNATIVE TACTICS Most alternative mating tactics are condition dependent. Different tactics are adopted when appropriate intrinsic and extrinsic conditions are encountered. The maintenance in the population of any particular tactic will depend on whether the fitness costs to individuals of maintaining the tactic (genetic, physiological, and neurological costs) are less than the increase in fitness actually produced by the tactic. This relationship will determine whether the tactic will persist, not the total fitness contribution of one tactic vs. that of any alternative tactic. The special circumstances which require the fitness contributions of tactics to be equal are likely to be rare. Although the fitness contributions of tactics are usually not expected to balance, the conditions at which individuals switch from one tactic to another should be adjusted by natural selection such that at the switch point (from one tactic to the other), the fitnesses of the two tactics should be equal (West-Eberhard, 1979). Imagine a continuum of sizes. Smaller males gain more by "sneaking," larger males by "guarding." Given a continuous effect of male size, at some intermediate size (x), males will do equally well to "guard" or to "sneak." The switch from "sneaking" to "guarding" should be made at x, although in some cases the exact condition x may not exist, as when considering discontinuous conditions like being winged or wingless, or the presence or absence of a resource. Note that the fitness gains of the

10 394 WALLACE J. DOMINEY tactics need not be frequency dependent, nor is there any reason to expect the total fitness contributions to individuals, or population-wide, to be equal. In general, fitness is maximized not by balancing the fitness contributions of the various tactics, but by maximizing the total. Total fitness is maximized by expressing the various alternatives when such expression makes the largest net increase to fitness. Real (1980) has provided a model utilizing the "law of diminishing returns" to show how animals might switch tactics as the return on continued expression of a tactic is diminished. Waltz (1982) has used the same law to model the conditions for expression of alternative mating tactics. Although cases of "equal fitness variants" are likely to be rare and quite interesting, in general discussions of mating tactics, emphasis should be given to conditionally expressed alternatives. ACKNOWLEDGMENTS I thank W. H. Cade, R. Dawkins, J. Maynard Smith, and E. C. Waltz for useful criticism of the manuscript, and H. J. Brockmann, W. D. Hamilton, and J. Seger for useful discussion and criticism of the manuscript. I also thank C. Smith for providing me with a copy of her unpublished review of alternative mating tactics. REFERENCES Alcock, J. 1979a. The evolution of intraspecific diversity in male reproductive strategies in some bees and wasps. In M. S. Blum and N. A. Blum (eds.), Sexual selection and reproductive competition in insects, pp Academic Press, New York. Alcock, J. 1979fc. The behavioural consequences of size variation among males of the territorial wasp, Hemipepsis ustulata (Hymenoptera: Pompilidae). Behaviour 71: Alcock, J., C. E.Jones, and S. L. Buchmann Male mating strategies in the bee Centris pallida Fox (Anthophoridae: Hymenoptera). Am. Nat. 111: Barash, D. P Mate guarding and gallivanting by male hoary marmots (Marmota caligata). Behav. Ecol. Sociobiol. 9: Barlow, G. W Social behavior of a South American leaf fish, Pohcentrus schomburghi, with an account of recurring pseudofemale behavior. Amer. Midi. Nat. 78: Barnes, R. F. W Mate searching behaviour of elephant bulls in a semi-arid environment. Anim. Behav. 30: Beecher, M D and I. M. Beecher Sociobiology of bank swallows: Reproductive strategy of the male. Science 205: Boer, B. A. de Influence of population density on the territorial, courting and spawning behaviour of male Chromis cyanea (Pomacentridae). Behaviour 77: Boness, D. J. and H. James Reproductive behaviour of the grey seal (Halichoerus grypus) on Sable Island, Nova Scotia. J. Zool. London 188: Borgia, G Sexual competition in Scatophaga stercoraria: Size- and density-related changes in male ability to capture females. Behaviour 75: Brockmann, H. J. and R. Dawkins Joint nesting in a digger wasp as an evolutionarily stable preadaptation to social life. Behaviour 71: Brockmann, H. J., A. Grafen, and R. Dawkins Evolutionarily stable nesting strategy in a digger wasp.j. Theor. Biol. 77: Brown, L. E. andj. R. Pierce Male-male interactions and chorusing intensities of the Great Plains toad Bufo cognatus. Copeia 1967: Cade, W Alternative male reproductive behaviors. Fla. Entomol. 63: Cade, W Alternative male strategies: Genetic differences in crickets. Science 212: Catts, E. P Hilltop aggregation and mating behavior by Gaslerophilus intestinahs (Diptera: Gasterophilidae). J. Med. Entomol. 16: Charlesworth, D. and B. Charlesworth Sexual selection and polymorphism. Am. Nat. 109: Christenson, T. E. and K. C. Goist, Jr Costs and benefits of male-male competition in the orb weaving spider, Nephila clavipes. Behav. Ecol. Sociobiol. 5: Clutton-Brock, T. H., S. D. Albon, R. M. Gibson, and F. E. Guinness The logical stag: Adaptive aspects of fighting in red deer (Cervus elaphus L.). Anim. Behav. 27: Constanz, G. D Behavioral ecology of mating in the male Gila topminnow, Poeciliopsis occidentalis (Cyprinodontiformes: Poeciliidae). Ecology 56: Cox, C. R. and B. J. Le Boeuf Female incitation of male competition: A mechanism in sexual selection. Am. Nat. 111: Dawkins, R Good strategy or evolutionarily stable strategy? In G. W. Barlow and J. Silverberg (eds.), Sociobiology: Beyond nature /nurture?, pp Westview Press, Boulder, Colorado. Dominey, W. J Female mimicry in male bluegill sunfish A genetic polymorphism? Nature 284: Dunbar, R. I. M Intraspecific variations in mating strategy. In P. P. G. Bateson and P. H. Klopfer (eds.), Perspectives in ethology, Vol. V, pp Plenum, New York. Eberhard, W. G Horned beetles. Sci. Am. 242: Eberhard, W. G Beetle horn dimorphism: Making the best of a bad lot. Am. Nat. 119:

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