levels of selection, altruism, and primate behavior

Levels of Selection, Altruism, and Primate BehaviorAuthor(s): Brenda J. BradleySource: The Quarterly Review of Biology, Vol. 74, No. 2 (Jun., 1999), pp. 171-194Published by: The University of Chicago PressStable URL: http://www.jstor.org/stable/2665094 .

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VOLUME 74, No. 2 THE QUARTERLY REVIEW OF BIOLOGY JUNE 1999

LEVELS OF SELECTION, ALTRUISM, AND PRIMATE BEHAVIOR

BRENDAJ. BRADLEY

Doctoral Program in Anthropological Sciences, State University of New York

Stony Brook, New York 11 794 USA

E-MAIL: [email protected]

ABSTRACT

Altruistic behaviors seem anomalous from a traditional view of Darwinian natural selection, and evolutionary explanations for them have generated much discussion. The debate centers around four major explanations: classic individual-level selection, reciprocity and game theory, kin selection, and trait-group selection. The historical context and defining criteria of each model must be reviewed before its validity can be assessed. Of these proposed mechanisms, group selection historically has been the most controversial. Although the extent to which empirical data support group selection hypotheses is uncertain, there is evidence for group-level selection among avirulent virus strains andforagingant queens. Researchers studyingmammalian behavior, particularly primatologists, have largely dismissed models ofgroup-level selection. Most discussion of altruism amongprimates has focused on differences in fitness among individuals within a single group, but students of altruistic behaviors exhibited by primates also need to investigate intergroup variation with respect to these behaviors. Various altruistic behaviors are likely to have evolved through different forms of selection, and each example of apparent altruism therefore needs to be evaluated separately.

INTRODUCTION

T HE PHENOMENON of altruism presents an interesting dilemma for the field

of behavioral ecology. Altruistic behavior is typically defined as actions that result in an increase in survival or reproduction of one or more other individuals, while causing a decrease in the survival or reproduction of the actor (Bourke and Franks 1995). In other words, altruism is individual self-sacrifice for the benefit of others. An altruistic behavior can vary greatly in the degree of benefit it provides to the recipient, as well as the amount of sacrifice it requires from the actor. In some altruistic acts, such as food sharing and grooming among primates, one individual benefits another directly, whereas other forms of altru-

ism, such as alarm calls and group defense, can have indirect effects on several individuals simultaneously.

Altruism is difficult to explain within traditional models of natural selection, which predict that individuals should exhibit behavioral traits adapted to promoting genetic self-interest. Any genic mutation that results in an altruistic behavior of the individual carrying it is likely to be decreased in frequency by selection. Despite this expectation, altruism has been observed in a vast number of taxa, ranging from avirulent viruses (Fenner 1965; Ewald 1994) and sterile working castes of social insects (see Bourke and Franks 1995 for review), to adoption of orphaned chimpan- zees (Goodall 1971) and human friendship (Tooby and Cosmides 1996).

The Quarterly Review of Biology, June 1999, Vol. 74, No. 2

Copyright ? 1999 by The University of Chicago. All rights reserved.

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172 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 74

Although the dilemma of altruism received very little attention in the century following Darwin's introduction of the concept of natural selection, it has recently become a frequent topic of controversy and debate (see Sober and Wilson 1998 for review). Historically, researchers have turned to levels of selection beyond the individual to provide explanations for this unexpected behavior. Many argue that in order for altruism to evolve, selection must operate at higher organizational levels than the individual, such as the kin group (Williams and Williams 1957), the population (Wynne- Edwards 1962), and the trait group (Wilson 1975; Wade 1978). Other theories suggest that what we term altruism may in fact be cooperation with delayed benefits (Trivers 1971; Axel- rod and Hamilton 1981) and thus a special model of individual selection.

The current debate over the evolution of altruism by natural selection centers around four major explanations: 1) classic individual- level selection; 2) reciprocity and game theory; 3) kin selection; and 4) trait-group selection. Although these four models have often been viewed in the past as alternative explanations, much of the conflict among their advo- cates can be resolved by clearly delineating the defining criteria and predictions of each explanation, based on a few characteristics. As a result, the models can be combined, and the ability of each to explain altruistic behavior can be tested.

Many researchers wishing to explain altruism have turned to models of group selection. Numerous studies from various fields of biology have been cited as evidence of group-level selection (see Wilson and Sober 1994 for review), but very few address the issue of altruism, and the corresponding empirical evidence is rather weak. However, three commonly cited examples of altruism selected at the group level are worthy of clearer thought and further investigation: the virulence of viruses (Shanahan 1990; Ewald 1994); female-biased sex ratios among social spiders (Colwell 1981; Aviles 1986; Frank 1987); and foraging specialization in cofounding ant queens (Rissing et al. 1989). These examples provide the best evidence to date of trait group-level adaptations.

Although studies of viruses, spiders and ants may provide evidence of group selection, little

such evidence has been provided by studies of mammals. In particular, there is a need to evaluate the possible explanations for the evolution of altruism among highly gregarious primate species. Up until now, little attention has been paid to group-level explanations of altruism in the study of primate behavior and sociobiology. Traditionally, researchers have attributed primate altruism to simple kin selection and reciprocity (Silk 1982; Cheney and Seyfarth 1990). However, there is a growing need to reevaluate these assumptions in the field of primate behavior. Some of the more common forms of altruism observed among nonhuman primates are coalition formation (Pac4er 1977; Smuts 1985; Noe 1992) and alarm calls (Cheney and Wrangham 1986; Cheney and Seyfarth 1990). Primatologists need to reexamine the questions being addressed and the types of data being collected in order to better study altruism among primates.

The evolution of altruism continues to be a source of intense discussion in many subfields of biology. A historical review of the theories, along with an examination of observed altruistic behavior, will assist in putting the various theories into perspective. The major explanations for altruism can then be evaluated and taken into account in future studies of animal behavior.

HISTORY OF THEORIES AND MODELS

EARLY CONCEPTS OF GROUP-LEVEL SELECTION

The concept of natural selection, as it was introduced by Darwin (1859/1872) in On the Origin of Species by Means ofNatural Selection, em- phasized selection at the level of the individual. "Individual selection" refers to selection of those traits that positively contribute to the survival and reproductive success of the actor relative to its conspecifics. Darwin's descrip- tion of the necessary conditions for selection (heritable variation, competition for limited resources) is generally thought to refer to at- tributes of individuals rather than groups.

It is commonly, although incorrectly, per- ceived that Darwin found great difficulty in explaining altruism in sterile castes of social insects. For Darwin, the unique dilemma presented by social insects was not altruism, but the fact that sterile castes exhibit a great diver-



JUNE 1999 SELECTION, ALTRUISM, AND PRIMATE BEHAVIOR 173

sity of adaptations. Darwin found this puz- zling, since traits of workers, which do not reproduce, could not be acted upon by natural selection (Darwin 1859/1872; Cronin 1991).

The altruism associated with sterile insects posed only a minor problem for Darwin:

How the workers have been rendered sterile is a difficulty; but not much greater than that of any other striking modification of structure; ... if such insects had been social, and it had been profitable to the community that a number should have been annually born capable of work, but incapable of pro- creation, I can see no especial difficulty in this having been effected through natural selection (Darwin 1859/1872, p 204, italics added).

Although this passage suggests that Darwin attributed insect working castes to natural selection of groups (Ruse 1980), Darwin's solu- tion was probably much more similar to Ham- ilton's (1964) theory of kin selection (see further discussions of selection below). In an earlier passage pertaining to this topic, Dar- win states that "selection may be applied to the family, as well as to the individual" (Darwin 1859/1872, p 204).

Darwin does make reference to group level selection again in his later works, however (Ruse 1980; Cronin 1991). In The Descent of Man Darwin expressed difficulty in explaining human morality:

It must not be forgotten that although a high standard of morality gives but a slight or no advantage to each individual man and his children over the other men of the same tribe, yet that an advancement in the standard of morality and an increase in the number of well-endowed men will certainly give an immense advantage to one tribe over another (Darwin 1871, p 166).

Although this statement certainly implies that human morals may be explained as a result of group-level or tribe-level selection, Dar- win did not outline a formal theory of group selection, and his focus in The Descent of Man is on individual-level adaptations. Darwin may have been the first to suggest the possibility that group selection could explain the evolution of altruistic traits such as sterility and moral codes, but his attention focused on the

individual as the crucial unit of selection (Ruse 1980).

Although first introduced by Darwin (1871; 1859/1872), a systematic model of group selection was not discussed until Sewall Wright's development of the "shifting balance theory" (Wright 1931, 1945, 1980). Wright's "intergroup" selection differed greatly from later models of group selection because it was not developed to explain altruism. Under Wright's model, individuals maximize their personal fitness and no conflict exists between the wel- fare of the individual and that of the group (Cronin 1991). Although Wright was not con- cerned with the evolution of altruism, he was the first to establish a model in which one group could develop a selective advantage over another.

Wright's shifting balance theory describes a situation in which, if all conditions are met, group selection could be theoretically possible. According to shifting balance, populations occupy a position on an "adaptive landscape" of all possible allele combinations. This landscape exists in n dimensions, where n is the number of traits or loci at which frequencies can vary. The average fitness in the population, w, reflects the altitude atwhich the population is positioned on the landscape. For any given landscape there can exist multiple peaks and valleys. Moving from peak to peak requires passing through a valley and, therefore, experiencing a temporary decrease in average fitness. Hence, natural selection can only move a population to the nearest local peak, which may not necessarily be the highest. However, if the population is small and relatively isolated, it could, because of genetic drift, move off the local peak into an adjacent valley. Ge- netic drift, coupled with natural selection, could then cause a population to move onto the slope of a different peak. Natural selection, if strong enough, will then push the population to this new peak. If the average fitness is now significantly greater than that of the peaks at which other populations are still located, the group at the higher peak will have a superior average group fitness. If this increased fitness results in increased population growth, the population located on the new peak will reproduce at a greater rate. Individu- als from this population could then migrate




and enter new populations. Within these new populations, individual selection would act to move the metapopulation to the new peak (Wright 1931, 1945, 1980).

Wright's theory raises several interesting questions (Barton and Rouhani 1993; Har- rison and Hastings 1996). First, it is difficult to determine how many generations would be required for a population to reach a new peak. Second, in order for shifting balance to occur, a population must be isolated enough for genetic drift to move it off its current peak and still allow individuals to disperse to new populations. Therefore, a critical balance between isolation and dispersal is required of natural populations if they are to undergo intergroup selection. Finally, the increased fitness of the new peak can only lead to increased group size if: 1) the change actually leads to an increase in environmental carrying capacity, or 2) the rate of fecundity increases as a result of the change in allele frequencies. How often this happens in natural populations is uncertain. Although not a universally accepted paradigm for how populations evolve, shifting balance theory provided the first model for the selection of traits at the level of the population rather than the individual. Shifting balance theory, as a model of group selection, influenced later biologists looking for an explanation for altruism.

The evolution of altruism in relation to group selection was not seriously examined until the publication in 1962 of Wynne-Edwards's book, Animal Dispersion in Relation to Social Behavior. The primary goal of this work was not to develop an elaborate theory of group selection, but rather to explain observed patterns of animal dispersal, territoriality and other relevant social behavior in animal populations. Wynne- Edwards believed that each habitat has an optimum population density, usually determined by available food resources. Populations must therefore put limits on their growth before resources are depleted. Selection will favor those groups that keep population densities close to optimal. Groups evolve a control system to reg- ulate group size and maintain "population homeostasis," analogous to an individual main- taining physiological homeostasis. This control system must be able to detect the current state of balance in the population, as well as restore

the balance if it is disturbed. He argued that the current state of balance is determined by "epideictic displays" like the choruses of birds or ritualized movements of insects. These behaviors give group members the necessary feedback that allows them to determine current population densities. If the population density is too high, groups exhibit decreased fecundity, infanticide and voluntary emigra- tions. Wynne-Edwards explained these altruistic behaviors of individuals within populations as a result of group selection. Individuals sacrifice their own reproductive success to maintain the homeostasis of the group. Hence, those groups that can maintain an optimum density are more likely to persist than other groups comprised of selfish individuals which are unable to control population size, and will therefore deplete their resources (Wynne- Edwards 1962, 1986).

The Wynne-Edwards model of group selection requires the following conditions: 1) As in Wright's model, populations must be physically isolated, with reproduction and mating taking place within each population, so that selfish individuals are not able to move into altruistic groups after they deplete their own resources; 2) There must be differential survival and extinction of populations; 3) Traits selected at the group level must result directly in increased probability of group survival. Sim- ilarly, groups lacking individuals with the needed restraints will be more likely to become extinct. In contrast to Wright's (1931, 1945, 1980) model, Wynne-Edwards (1962) focuses on limits to population growth rather than increased population size and immigra- tion (Wilson 1983). The work of Wynne- Edwards, although viewed today as naive (see below), was significant in that it brought the topic of group selection and the evolution of altruism to the forefront of biology.

RESPONSES TO EARLY GROUP SELECTION IDEAS

The argument presented by Wynne-Edwards (1962) was quickly eviscerated in the literature. In 1964, Maynard Smith questioned the theoretical plausibility of group selection. Al- though he demonstrated that group selection is possible in theory, his primary objective was to show that the conditions necessary for it to occur rarely exist in nature. Under Maynard



JUNE 1999 SELECTION, ALTRUISM, AND PRIMATE BEHA VIOR 175

Smith's model, group selection of altruistic traits requires that: 1) groups are either very small in size or frequently reestablished by single fertilized females; 2) the sacrifice made by the individual must be small, while the benefit gained by the group is large; and 3) gene flow must be minimal (Maynard Smith 1964).

To demonstrate his model, he describes two hypothetical mouse populations living in two different haystacks. Each local population is established by one fertilized female. If one group is fixed for the s (altruistic) allele while the other group is fixed for the S (selfish) allele, the frequency of the s allele in the total population can increase only if the following conditions are met: 1) there is reproductive isolation for several generations; 2) the group is founded by only a few individuals; and 3) there is no little or no gene flow between haystacks. It is necessary for the s allele to be fixed under this model, as ss individuals would quickly be eliminated in a mixed population. If SS individuals are allowed to encroach on ss populations, the s allele will be selected against.

Maynard Smith developed this model of group selection with the intent of demonstrat- ing the unlikelihood of Wynne-Edwards's ideas being applicable to natural populations:

It is concluded that if the admittedly severe conditions listed here are satisfied, then it is possible that behaviour patterns should evolve leading individuals not to reproduce at times and in circumstances in which other members of the species are reproduc- ing successfully. Whether this is regarded as an argument for or against the evolution of altruistic behaviour by group selection will depend on ajudgment of how often the necessary conditions are likely to be satisfied (Maynard Smith 1964, p 35).

Wynne-Edwards's version of group selection did not truly lose its attraction however, until the publication of G C Williams's Adapta- tion and Natural Selection in 1966. Williams argued that, although group selection may be possible in theory, it is simply unnecessary to explain the phenomena observed in nature. Adaptation, according to Williams, is never very effective at any level above the individual. He argued that it is necessary to distinguish between a population of adapted individuals and an adapted population. Therefore one

must observe natural populations and ask: Do inherited characteristics observed in a population reflect an effective design for maximizing the number of offspring produced by individuals, resulting in a greater contribution of those genes to the next generation (individual adaptations), ordo they reflect an effective design for maximizing the growth rate or numer- ical stability of the population as a whole (group level adaptations)? Williams labeled the former type of adaptation an organic adaptation, and the latter a biotic adaptation. If selection is happening at the level of the individual, organic adaptations will be observed. Conversely, if group selection is the significant force of evolution, one would expect biotic adaptations to be common.

Williams claimed that for natural populations there are no adaptations of obvious group benefit that cannot be explained on the basis of genic or individual selection alone. Many traits, like altruism, which were pre- viously thought to reflect group selection, could now be explained in terms of kin selection (Hamilton 1964). In other words, it was predicted that altruistic acts would be performed toward relatives, thereby making it possible for a gene producing an altruist phenotype to increase its frequency in the next generation. In addition, work by Lack (1954) suggested that many nesting birds that appeared to be limiting their individual reproductive potential (by producing fewer offspring than is physiologically possible) per clutch were actually maximizing reproductive success over the course of the entire breeding season. Later discussions of reciprocity (Triv- ers 1971) and game theory (Axelrod and Hamilton 1981; Axelrod 1984) demonstrated that what appears to be altruism may actually be a form of cooperation with delayed benefits. This lent additional validity to the argument that apparent altruism could be explained by individual selection alone.

Since the rate at which individuals replace themselves (the generation time) is much greater than the rate at which populations do (rate of group extinction), Williams (1966) concluded that genic (including individual and kin) selection is the most parsimonious explanation for the traits observed in natural populations. In addition, biotic adaptations




such as female biased sex ratios (discussed below), are seldom observed. Thus, he argued, group selection was unlikely to be a strong evolutionary force.

Lewontin (1970) elaborated on group selection theory and developed a hierarchical model of natural selection, in which selection occurs at multiple organizational levels of life. Although Lewontin agreed with Williams that the primary force of selection is the individual, he argued that selection also acts on numerous other nested levels, ranging from the mol- ecule and organelle to the species and community. Lewontin outlined three necessary principles, modeled after Darwin (1859/1872), in order for a population to evolve by natural selection (Lewontin 1970, p 1):

1) Different individuals in a population have different morphologies, physiolo- gies, and behaviors (phenotypic variation).

2) Different phenotypes have different rates of survival and reproduction in different environments (differential fitness).

3) There is a correlation between parents and offspring in the contribution of each to future generations (fitness is heritable).

Lewontin argues that any level of organization at which these conditions are met will undergo evolutionary change by natural selection. In Lewontin's model these conditions are both necessary and sufficient for natural selection to occur. Therefore, the "levels-of- selection" theory of Lewontin implied that selection could act simultaneously on several different levels. There may be conflicting in- terests among levels, however. For example, behaviors that maximize the probability of group survival may not maximize fitness for individual members within the group. As a result, a compromise is reached between the force of selection at each level (Lloyd 1992; Bourke and Franks 1995).

After Lewontin developed this hierarchical theory of selection, several biologists accepted and expanded his model (Alexander and Borgia 1978; Wimsatt 1980; Wilson and Sober 1989, 1994). Although it is generally ac-

cepted that evolution is defined by changes in gene frequency, when a population is structured into multiple, complex levels, the forces that change gene frequency are thought to act at all levels, often in opposition to each other. Lewontin's theory rejected the idea that group selection, kin selection and individual selection are mutually exclusive theories, and developed instead a paradigm by which natural selection is envisioned as acting simultaneously on the individual and the group, as well as at numerous other levels. Lewontin's levels- of-selection theory has greatly influenced modern models of group selection.

MODERN GROUP SELECTION MODELS

The early ideas of group selection, especially those of Wynne-Edwards, are rarely en- dorsed any longer, but modern theories of group selection are now the subject of much discussion (Wilson and Sober 1994; Rose and Lauder 1996; Sober and Wilson 1998). Wilson (1975, 1980, 1983) is the primary proponent of the importance of group selection. Unlike earlier models that viewed the "group" as an entire deme or population, Wilson's unit of focus is mainly the "trait group." He defines a deme as a population in which mating occurs-homogeneous with respect to genetic mixing, but heterogeneous with respect to ecological interactions. Mating occurs within the deme, but not all members of the deme share a common fate with respect to environmental interaction. Often these demes are structured into numerous, distinct trait groups. A trait group is a smaller subset of the deme, within which all individuals have a common fate with respect to a given trait. Examples of trait groups include schools of fish and flocks of migratory birds, which typically experience the same environmental conditions but often mate with members of other trait groups.

Each trait, therefore, has a "sphere of influence" (Wilson 1980) within which the phenotype of each individual affects and is affected by that of every other individual. This "sphere of influence" need not be a physically isolated group, nor does it need to be the same "sphere" for each trait. For example, Wilson (1980) states that traits manifested among young nesting birds will result in a trait group




comprised of just the birds within the same nest, whereas traits manifested during the adulthood of the birds will result in much larger trait groups. Wilson's model thus requires that populations be structured into these isolated trait groups. Although trait group isolation need not be physical (as long as there is preferential interaction between individuals), it often results from spatial hetero- geneity.

Wilson's model states that while classic individual selection acts within each trait group, there is differential selection among trait groups within the deme. For this reason it is often referred to as intrademic group selection or IGS (Wade 1978) to differentiate it from early interdemic group selection models such as those of Wynne-Edwards and Maynard Smith. It should be noted, however, that between group selection or BGS may be a less ambiguous acronym for representing intrademic group selection.

The basic IGS or BGS model is as follows (Figure 1): A deme or "global population" is structured into numerous trait groups, each containing a frequency, (x, of altruistic individuals, A. The frequency of nonaltruists (B = nonaltruistic individuals) is (1 - o) or P3. The frequencies of A and B individuals can also be calculated for the global population or entire deme. These are symbolized by & and 3 re- spectively. The frequencies of ot and 1 must vary between groups (a "group" in this model refers to the "sphere of influence of a trait"). Within each group, A individuals are selected against, and therefore cx decreases while 13 increases. This is classic individual-level selection. However, if the A-trait causes the groups with the most A individuals to have either greater productivity or reduced mortality relative to other trait groups, the global frequency of A individuals, &, could actually increase relative to 3. This increase in & would be a result of selection at the level of the trait group.

This balance can be modeled mathematically (see also Price 1970, 1972 for more complex mathematical modeling). Fitness values can be calculated for each trait (altruist = WA, and nonaltruist = WB) given a specified value for c (cost to the altruist) and b (benefit to the recipient). A trait group fitness index (GFI) can then be calculated as well.

WA= 1- c+ b(Na -1) / (N-1)

WB = 1 + bNot / (N- 1)

GFI = (WANoa) + (WB(1 - No))

where N = the size of the trait group; a = the frequency of altruists in the group; c = the cost to the altruist; b = the benefit to the recipient. A baseline fitness of 1 is given to each phenotype.

The (N - 1) implies that each individual receives the benefit except the one that provides it. This scenario is exemplified by the altruistic behavior of alarm calling. However, if a behavior provides a benefit to the actor as well, N would replace (N - 1) in the above equations. Many altruistic behaviors in nature (e.g., active group defense or mobbing) are of this type.

Within the trait group, fitness of altruists (WA) will always be less than fitness for nonaltruists ( WB), but the group fitness of groups containing more altruists will be higher. It will often be roughly proportional to the number of altruists within that group, although group fitness need not always increase with the addition of each altruist. The level of group fitness associated with behaviors such as alarm calling does not necessarily increase with each additional caller. Classic individual selection acts against A individuals within the group, whereas IGS selects for A individuals (and groups containing them) across the global population. The term altruism therefore only applies to interactions within the trait group under the IGS model. Although the absolute fitness of the altruist may be high, its fitness relative to selfish individuals in the same trait group is low. This is what Wilson (1980) calls selection for "weak altruism."

There are several necessary conditions for this IGS model to be valid. Not only must populations be structured into several distinct trait groups, as described above, but variation must exist among those trait groups. The strength of the IGS model depends on the degree of genetic variation among these groups. The greater the difference in concentration of altruists in groups, the greater is the dis- crepancy in fitness among groups. The most common cause of a nonrandom (or nonbinomial) distribution of gene frequencies is simply the fact that many trait groups are also kin




N=20 N=20 B B A A A B I. A structure deme subdivided into

6 B B A B\ ( A B A \ two trait groups, each containing B A

B B A A A altruists (A) and nonaltruists (B).

B B A B A A A A B The frequency of altruists (a) differs i A BA A B A A A for each group. The global

a = 0.5 A frequency of altruists (a) is 0.5. The

A global frequency of nonaltruists (p)

a =0.25 p =0.75 P= 0.5 a =0.75 p =0.25 is also 0.5.

N=5 N= II. Individual selection causes a to

/ B \ / A A AX decrease within each trait group. The

BAB A A AL \group with the highest frequency of A A altruists has a decreased mortality

B B B rate, however. The global frequency a= A05 of altruists increases.

a =0.20 p = 0.80 p= 0.45 a =0.66 p =0.33

A A B A A B B

B B A B A B m. Mating occurs across the global

B A B A A B A B population; it is not restricted to the A A B A B trait group. Each individual has one

V A y B A B A A BJ jB offspring.

N=20 N=20

A IV. Population settles back into trait r

A A A A B A groups. Both trait groups experience A an increase in a due to a high global

A AA A A B frequency of altruists. ~~A A A

a = 0.25 p0.75 0 = 0.45 a =0.25 p =0.75

FIGURE 1. DIAGRAM OF INTRADEMIC GROUP SELECTION, IGS (MODELED AFTER WILSON 1975).

groups. However, it would also be possible to get a nonbinomial distribution through what Wilson (1980, p 35) terms "differential mixing." This occurs when differential genetic interactions with the environment translate into spatial patterns. In other words, the gene that results in altruism may also influence spatial preference resulting in altruists being grouped together more often than would be expected at random.

In addition to deme structure and trait- group variation, the relevance of the IGS model also depends on the values for b, c, and cx in the equations above. Simpson (1994) calculated values for WA, WB, and GFI from the above equations for various values of each variable (Table 1). All calculations were based on groups of 10 individuals (N = 10). He found that in order for altruism to evolve under

group selection, costs to the altruist must be low, benefits to the group must be high, and a large portion of the group must be altruists. An initially high frequency of A would probably be very rare in natural populations under this model, since trait groups are not isolated with respect to reproduction, and therefore are unlikely to undergo genetic drift.

Wilson's model is formally plausible, but to what extent does it apply to natural populations? In order to answer this, one must determine how often the conditions required by this model are met. IGS requires structured demes, variance among groups, and a combination of small individual cost (c), large group benefit (b) and large portion of altruists in the group (oc). In addition, the trait must result in either a high group-fecundity rate or a low




TABLE 1 Fitness of altruists (WA), nonaltruists (WB), and groups (Group Fitness Index: GFI) when costs (c), benefits (b),

and proportion of altruists in a group (a) vary. Equations from Wilson and Sober, 1994. Table from Simpson, 1994, with permission of Cambridge University Press.

Parameter values Fitness indexes

costs benfits altruists in WA WB GFI (c) (b) group (CX)

.25 1.00 .75 1.47 1.83 15.62

.25 1.00 .50 1.19 1.56 13.75

.25 1.00 .25 .92 1.28 11.88

.25 .75 .75 1.29 1.63 13.75

.25 .75 .50 1.08 1.42 12.50

.25 .75 .25 .88 1.21 11.25

.25 .50 .75 1.11 1.42 11.88

.25 .50 .50 .97 1.28 11.25

.25 .50 .25 .83 1.14 10.63

.50 1.00 .75 1.22 1.83 13.75

.50 1.00 .50 .94 1.56 12.50

.50 1.00 .25 .67 1.28 11.25

.50 .75 .75 1.04 1.63 11.88

.50 .75 .50 .83 1.42 11.25

.50 .75 .25 .63 1.21 10.63

.50 .50 .75 .86 1.42 10.00

.50 .50 .50 .72 1.28 10.00

.50 .50 .25 .58 1.14 10.00

.75 1.00 .75 .97 1.83 11.88

.75 1.00 .50 .69 1.56 11.25

.75 1.00 .25 .42 1.28 10.63

.75 .75 .75 .79 1.63 10.00

.75 .75 .50 .58 1.42 10.00

.75 .75 .25 .38 1.21 10.00

.75 .50 .75 .61 1.42 8.13

.75 .50 .50 .47 1.28 8.75

.75 .50 .25 .33 1.14 9.38

N = 10 individuals per group. WA = 1 - c + b (Not - 1) / (N - 1)

WB = 1 + bNot / (N- 1)

GFI= (WANot) + (WB(1 - NOt))

mortality rate relative to those of other trait groups.

The first condition, that demes must be subdivided into trait groups, is surely met by many natural populations. Wilson (1980) cites several examples, such as schools of fish that co- alesce in order to shoal. A high frequency of altruists within a trait group is unlikely, however, unless the trait group is composed of kin, in which case the evolution of the trait could be attributed, at least partly, to kin selection.

Many have argued that since kinship is the most plausible cause of group selection, IGS is simply another way of viewing kin selection,

and hence it should not be called group selection at all (Maynard Smith 1976; Grafen 1984; Nunney 1985). However, it is possible to have group selection without kin selection, as long as the variance among groups is not the result of identity by descent.

EVALUATION OF THE

GROUP SELECTION CONTROVERSY

No longer does the dilemma presented by conflicting views of altruism need to seek an explanation. Instead, the challenge is to differentiate among several proposed explanations, all of which are theoretically possible.




The major competing explanations for altruistic acts are: 1) classic individual selection; 2) reciprocity; 3) kin selection; and 4) (nonkin) intrademic group selection, or IGS. Since different altruistic behaviors may require different explanations; it is necessary to note the criteria for evaluating each one. This will allow researchers, when observing altruism among animals, to determine the most likely explanation for how such a behavior may have evolved.

Before these four major explanations can be compared and reconciled, however, it is necessary to review the importance of Dawkins's (1976, 1982) replicator concept. Dawkins stated that the fundamental unit in natural selection is the gene, or replicator. Replicators are enti- ties that make exact copies of themselves, re- taining their integrity with each generation (Dawkins 1982). The individual is simply a vehicle or "survival machine" by which a replicator can transmit copies of itself into the next generation. Evolution by natural selection is defined by the increase and decrease of certain replicators over time, rather than the increase and decrease of individuals (vehicles). Individuals and genotypes cannot evolve. They are not replicators, they are vehicles or interactors (Hull 1980). Vehicles, such as sexual organisms, do not leave copies of themselves in the next generation, as they are simply mechanisms by which replicators increase in frequency through time. Like individuals, groups can also be viewed as vehicles for gene replication.

It is necessary to distinguish between replicators and vehicles before the relative importance of competing explanations of altruism can be evaluated. By definition, an altruistic replicator could never be selected for. A replicator that increases the fitness of another replicator at the expense of its own reproduction will not increase in frequency in the next generation. However, a vehicle that exhibits an altruistic trait could be selected for, as long as it did increase the frequency of its replicators in the next generation. Therefore, the ques- tion of altruism concerns the differential fitness and selection of vehicles, not replicators. Individual selection, kin selection, and group selection all refer to selection of vehicles, and each gene can simultaneously influence several nested vehicles. The reproduction of one

vehicle (such as the individual) can be sup- pressed or compromised in favor of maximizing the reproduction of another vehicle (such as the group).

The problem of selection units arises when several replicators rely on the same vehicle, and the actions of the vehicle may benefit replicators differentially. Within a vehicle, selection will tend to minimize conflicts among replicators. Within a given organism this conflict is minimized because competition among replicators is mainly for representation in the next generation. Alleles at different loci within an individual rarely compete with one another as long as they have a shared fate. All cells within the individual share the same replicators, and each allele at a given locus has the same probability (0.5) of being represented in each ga- mete. This results in a minimization of conflict within an individual organism (Bourke and Franks 1995).

Likewise, if the degree of genetic similarity at a given locus within a group is high and all individuals within the group have a shared interest or common fate, the conflict among individuals will be minimized. In other words, selection among groups of individuals could be significantly stronger than selection among individual members within the same level- the situation represented by Wilson's intrademic group selection (Wilson and Sober 1989).

This distinction between replicators and vehicles is important in evaluating competing explanations for altruism. It must be recognized that individuals are vehicles of selection that exist within other vehicles, such as kin groups and trait groups. Once it is understood that natural selection is defined only in terms of changes in replicator frequencies, and that differential selection of vehicles at several levels can cause these changes, the various explanations for altruism can be reconciled and evaluated (see Table 2).

1. Individual Selection

Classic individual selection, in which the organism is the only vehicle, parallels genic level selection for the reasons outlined above. Un- der this explanation, an individual will always maximize its own reproduction, and it will do so at the expense of relatives and other group



JUNE 1999 SELECTION, ALTRUISM, AND PRIMA TE BEHA VIOR 181

TABLE 2 Comparison offour explanations for the evolution of altruism

Individual Selection Reciprocity Kin Selection Intrademic Group Selection (IGS)

Vehicle Individual organism only Individual organism only Kin group Compromise between trait group and individual

Nature of No real sacrifice; not No real long-term Individual sacrifice Individual self-sacrifice Altruistic truly altruistic sacrifice; altruism only following Hamilton's relative to other trait- Act in short term rule: b> c/r group members, but

not relative to overall population

Necessary * Act must provide imme- * Frequent interactions * Genetic similarity * Population Condition diate benefit to actor between individuals; among interactors structured into nu-

groups not ephemeral due to identity by merous trait groups descent

* Nonaltruists recognized * No need for future * Frequency of altruists and excluded repayment or fre- in trait groups must

quent interaction vary * All interactors demon- * Behavior typically * Trait groups with

strate similar frequency directed at relatives higher portion of al- of altruistic behaviors; or groups contain a truists exhibit higher interactions limited to large portion of kin fecundity rate and/or fellow altruists although lower mortality rate they need not be kin compared to other

groups

* Strength of IGS dependent on cost to actor, benefit to group, group size, and frequency of altruists in group

members. Altruism, in the strict sense, cannot evolve by individual-level selection. An act that may appear altruistic could, upon closer in- spection, be a result of the individual's at- tempt to maximize its own genetic success. What may appear as self-sacrifice to an ob- server might actually be an evolutionary strategy for the individual. Altruistic behaviors may provide benefits to the actor, even though they go unnoticed by ethologists. The first pu- tative explanation for altruism, then, is that it simply is not altruism at all, but rather that the individual is actually maximizing its own genetic success.

It should also be noted that some self-sacri- ficing behaviors are a result of the beneficiary manipulating or deceiving the altruist by using false signals. Although behaviors of this kind

have been largely overlooked in discussions on altruism, manipulation is likely to play a role in determining the extent to which organisms donate resources to others. Deception explains numerous types of altruistic behaviors, including pets "manipulating" human responses of care-giving through neotenous morphologies and behaviors (Archer 1997), and inquiline beetles that penetrate and live in an ant colonies by producing imitation pheromones (Wilson 1975). Although manip- ulated individuals experience a loss of resources, they may still be maximizing long term fitness within their environments. The benefits of an altruistic response to a given sig- nal (e.g., neotenous morphologies or specific pheromones) are probably greater than the cost of occasionally misallocating resources or




energy to manipulators. Altruistic individuals may occasionally experience a loss of resources due to manipulation, but if the altruistic behavior is usually in response to true, rather than false, signals, it can still maximize long-term fitness. Those who wish to explain specific altruistic behaviors must consider the possibility that some altruistic acts are a result of manipulation and deceit by the beneficiary, and therefore are indeed costly for the altruist.

2. Reciprocity A second and frequently employed expla-

nation for altruism is mutual reciprocity, or reciprocal altruism (Trivers 1971; Axelrod and Hamilton 1981; Axelrod 1984; Nowak and Sigmund 1998). Reciprocity predicts that an individual will make a sacrifice with the expectation of prompt or future repayment by the beneficiary. This explanation of altruism has been influenced by game-theory models such as TIT FOR TAT and the "prisoner's dilemma" (Axelrod and Hamilton 1981). Reci- procity, however, can only be considered to be altruism when the long-term fitness benefits are ignored. Since, on average, each act of self- sacrifice should sooner or later be repaid, it is more appropriate to view reciprocal altruism as cooperation with possibly delayed benefits, rather than as true altruism. Not only is reciprocity selected for at the level of the individual, but the vehicle upon which selection acts is also the individual. If apparent altruism is a result of reciprocity, one would predict that altruistic acts will occur only among individuals that interact frequently, and "cheaters" would be recognized and excluded (Packer 1977). Although genetic similarity is not required, an "altruist" must sacrifice to benefit only fellow "altruists" under this model to en- sure repayment at some future time. Inter- actors would thus not need to share the same alleles at the same loci for reciprocity, but they would need to share a common phenotype of cooperation in exchange for delayed benefits. This shared cooperative phenotype can also result in reciprocity between members of different species (see Trivers 1971 for examples).

3. Kin Selection

Kin selection is defined as the selection of genes for social behaviors through the sharing of these genes between the performer of the

behavior and its relatives (Bourke and Franks 1995). Kin selection (or inclusive fitness) theory was first proposed as an evolutionary prin- ciple by Hamilton (1964; see also Maynard Smith 1964). In order for an altruistic behavior to evolve under kin selection it must provide a benefit to the receiver that is greater than the cost to the actor, divided by their degree of relatedness. Mathematically, this is stated as b > c/r where b is the benefit to the recipient, c is the cost to the altruist, and r is the probability that the two individuals share a given allele. This requirement for kin selection is known as Hamilton's rule (West Eber- hard 1975).

Individuals must be able to distinguish relatives and nonrelatives, as well as to ascertain various degrees of relatedness among kin, if behaviors are to evolve through kin selection. Williams (1997) states that kin selection should be defined as the adaptive use of "cues indicative of varying degrees and probabilities of kinship." Those individuals that can distinguish among different degrees of relatedness may have an advantage at the individual level, because they will expend energy and resources only for those individuals who share their genes and are thus less likely to be manip- ulated by those who do not. In addition, organisms that recognize and associate with kin will benefit from altruistic acts by relatives. This outcome would be selected for at the level of the individual. Once an individual sac- rifices resources for the benefit of relatives, however, the kin group also experiences a higher fitness, at a cost to the individual. This leads to some confusion, since kin selection can act at many levels within family groups, and interactions of this nature between parent and offspring could be explained by classical individual-level selection (see above). If an individual exhibits greater altruism to a full sib- ling than to a cousin, the kin group being selected for is the set of all full siblings of the altruist, not the entire kin group. Although many argue that kin selection is an extension of individual selection (West Eberhard 1975; Williams 1997), herein the vehicle in kin selection is considered to be the individual, as well as various levels of kinship.

Unlike reciprocity, under kin selection true altruism can evolve at the vehicle level of the



JUNE 1999 SELECTION, AL TRUISM, AND PRIMA TE BEHA VIOR 183

individual. There is no need for repayment by the beneficiary at a future time. In kin selection, the vehicle level of the individual is sacri- ficing its own reproductive potential, whereas the vehicle level of the kin group increases its fitness. The crucial point is that the gene or replicator responsible for that altruistic behavior is still behaving selfishly, and is still increas- ing its frequency in the next generation.

4. Intrademic Group Selection

As described above, kin selection is sometimes viewed as a type of intrademic group selection (IGS) if there is a large degree of genetic similarity owing to identity by descent within the trait group. It is necessary to divide intrademic group selection theory into two kinds: kin selection, and nonkin group selection. The primary criterion for distincting these types is identity by descent, the corner- stone of kin selection theory (Wilson and So- ber 1994). The probability of relatedness for individuals within a kin group is the same at all loci, notjust the loci at which the altruistic trait is found. Therefore, the compromise between selection at the level of the individual and selection at the level of the kin group is easily made. Each replicator has an equal interest in assisting kin.

The vehicle of nonkin intrademic group selection is the trait group rather than the individual or kin group. Trait-group selection does not require physical groups, but it does require differential interactions among individuals within the population. Such differential interaction is unlikely to be observed out- side of kin groups. Since the strength of IGS is often directly proportional to the frequency of altruists in the trait group, the higher the degree of homogeneity at the locus determining altruism, the more feasible IGS becomes. The primary difference between kin selection and nonkin group selection is whether the probability of genetic similarity is the same at all loci (owing to identity by descent), or only at the loci determining selfish or altruistic behavior. Although it is theoretically possible for altruism to evolve through IGS without a high proportion of altruists in the trait group, it would require an extremely low cost to the altruist, and a large payoff to the beneficiary (as demonstrated in Table 1). The extent to

which these conditions are met in natural populations is uncertain.

Although the four major explanations for altruism can be clearly distinguished in theory, recognizing them under natural conditions may be more difficult. Individual selection predicts that what is assumed to be self- sacrificial behavior is, in reality, a maximiza- tion of relative fitness. Individual-level explanations of altruism, such as manipulation, would be very difficult to identify in wild populations, especially in groups in which social interactions are intricate and complex, such as those of monkeys and apes. Reciprocity, a frequently employed explanation for altruism, is simply another form of individual-level selection. Acts labeled as altruistic in the context of reciprocity are, in the long-term, selfish ones. True self-sacrifice on the part of the individual, on the other hand, can be explained by kin selection, which results in preferential interaction between members of a group in proportion to their degree of relatedness. Altruis- tic acts should follow Hamilton's rule (b > c/r) and genetic similarity should be a result of identity by descent. Finally, although kin selection is often viewed as a type of intrademic group selectiorn, (nonkin) trait group selection is a possible explanation for altruism as well. The strength of nonkin IGS is determined by the size of the group (A), the cost to the actor (c), the benefit to the receiver (b) and the frequency of altruists in each group (oa). A high frequency of altruists in a group would need to result from genetic similarity only at the loci for altruism. If the frequency of altruists in a group is low, the ratio of c to b must be extremely low for a trait to evolve through IGS.

EVIDENCE FOR GROUP SELECTION

AS AN EXPLANATION

Identifying altruism and its causes in natural populations is difficult. How does one con- clude that an apparently altruistic trait is a result of trait-group selection, as opposed to individual selection, reciprocity or kin selection? Wilson and Sober (1994) cite 55 papers as providing possible empirical examples of group selection, claiming that 29 of which provide direct field or laboratory evidence of IGS. Most of these articles do not address the evolu-




tion of altruism directly, however. In fact, many of the studies involve laboratory manip- ulations of the flour beetle, Tribolium (Wade 1976; Goodnight 1990), or the evolution of altruism in humans (Rushton 1989; Boehm 1993).

The flour beetle experiments involved sub- jecting different groups of beetles to various treatments, such as artificial laboratory selection for certain group traits including group size and emigration rate. Results from these experiments may demonstrate the theoretical feasibility of group selection, but they do not consider the dynamics of natural populations. Gene frequency changes in these experiments are a result of artificial selection, and therefore do not provide direct evidence for the selection of altruistic behaviors in natural populations, although they do support the theoretical feasibility of IGS.

The evolution of altruism in humans is often cited as evidence of IGS as well (see Wilson and Sober 1994 for review). These data are problematic since, unlike that of other animals, human behavior is greatly influenced by culture. The extent to which natural selection can act on cultural traits is in need of further study. Supposed evidence for IGS from studies of culturally-influenced behaviors will not be evaluated here, since the primary concern of this paper is the evolution of innate altruistic behaviors.

Although the beetle experiments and the analyses of the evolution of altruism in humans contribute little to our understanding of levels of selection, there are several studies that seem to provide more convincing evidence of group selection for altruism. These studies, which are frequently cited as evidence of IGS (Wilson 1983; Bourke and Franks 1995), include the evolution of virulence in the myxomatosis virus (Shanahan 1990; Ewald 1994), female biased sex ratios in spiders (Frank 1986, 1987; Aviles 1986, 1993) and foraging specialization in cofounding ant queens (Rissing et al. 1989).

VIRULENCE IN THE MYXOMATOSIS VIRUS

There is one kind of group, sometimes a trait group and sometimes one or more populations, for which group selection models may be especially useful-the community of para-

sites and pathogens in or on a host organism. Ewald (1983) noted that the impact of para- sites on their host populations might decrease over time. The classic example is the evolution of virulence in the myxomatosis virus that infected rabbits in Australia and Europe. Euro- pean rabbits, Oiyctolagus cuniculus, were introduced into Australia by European settlers in the mid-1800s. By the mid-1900s the rabbit populations of Australia were growing out of control and spreading rapidly throughout the continent. These rabbits were viewed as pests, and people exerted a form of biological control over the rabbit populations. In 1950 the myxomatosis virus, found in the South Ameri- can forest rabbits, Sylvilagus brasiliensis, was de- liberately introduced with the hopes that it would limit the growth and spread of Austra- lian rabbit populations (Fenner and Myers 1978; Ewald 1983; 1994).

The disease, first introduced in one experimental site, the Murray Valley in southeastern Australia, quickly spread over much of south- ern Australia (Fenner and Myers 1978). Ini- tially, the decrease in rabbit populations was rapid and dramatic, killing 99.8% of the rabbits within two weeks of the initial infection. However, when another outbreak occurred in 1952, the mortality rate of infected rabbits decreased to 90%, and by 1964, twelve years later, the mortality rate of host rabbits infected with myxomatosis was only 8.3% (Fenner 1965; Fenner and Myers 1978; Ewald 1994).

This decrease in mortality rate led parasitol- ogists to two separate but not contradictory conclusions. First, it was proposed that greater resistance to the virus evolved in the rabbits. In other words, those rabbits that survived the first introduction of the virus had a greater ability to resist the virus and, therefore, the genes responsible for this resistance increased rapidly in frequency over a few generations. Support for this explanation was provided by laboratory experiments, in which both wild and laboratory-bred rabbits were inoculated with the same strain that was introduced in 1950. As predicted, feral Australian rabbits exhibited a greater resistance to the virus than rabbits bred in the laboratory (Fenner and My- ers 1978). Therefore, the hypothesis that wild rabbits resistant to the virus had a selective advantage was supported.




Further laboratory studies demonstrated that this hypothesis alone was not sufficient to explain the decreased mortality rate of infected rabbits. Additional groups of feral and laboratory-maintained rabbits were inoculated with a wild strain of the myxoma virus acquired from feral rabbit populations. It was found that both feral and laboratory-bred rabbits demonstrated a decrease in mortality rate when infected with the wild virus strain than when infected with the original strain. This led to a second explanation for the decreased mortality rate of the hosts-the virus was evolv- ing to states of lower virulence (Fenner 1965).

The first explanation-that rabbits evolved higher resistance-can be easily understood by simple individual level selection; however, the evolution of virulence in the virus cannot be so explained. Although it is commonly assumed that virulence is directly related to viral reproductive rate (Fenner and Myers 1978; Ewald 1994), the relationship between these two factors is probably much more complex. As pointed out by Sober and Wilson (1998), this relationship cannot be compared in disease-causing organisms of different kinds. Al- though some bacteria, such as most strains of E. coli, can reproduce at a high rate without causing harm to the host, other bacteria such as Mycobacterium tuberculosis may be lethal in small numbers (Bull 1994). Therefore, the generalization that viral strains with a lower level of virulence must also exhibit a lower reproductive rate applies only when comparing strains of the same kind. Within this context, decreased reproductive rates can be selected for at the level of the group when differential group extinction rates are a major force determining gene contributions to the next generation (Lewontin 1970; Wilson 1983).

Of the four possible theories for the evolution of altruism (individual selection, reciprocity, kin selection and IGS), intrademic group selection is the best explanation for the evolution of decreased virulence in the myxomatosis virus. Defining the "individual" is difficult at the level of a virus. If an individual is a genotype formed by sexual reproduction, the clone of cells produced by viral propagation may be considered an individual, and multiple clones within a single host form a group. The fact that the population of pathogens within a

host is usually initiated by more than one strain (Ewald 1994) results in each host being an environment for a different group of clones. Individual level selection, as mentioned above, would predict that each virus should optimize its reproductive rate. Al- though individual-level selection can explain decreased reproductive rates of the birds studied by Lack (1954), this same reasoning cannot be applied to viruses. Lack suggested that birds may have clutch sizes well below their physiological potential, yet maximize their total seasonal reproduction. Viruses do not allo- cate their reproductive efforts over numerous breeding seasons and, unlike birds, individual selection of viruses certainly favors higher immediate reproductive rates (Shanahan 1990).

In addition, reciprocity cannot be applicable to the evolution of virulence in myxomatosis, since viruses are not true social units. The necessary conditions for reciprocity (frequent interactions between altruists and beneficiar- ies, the recognition of individuals possessing the "reciprocity phenotype" and the exclusion of cheaters) do not apply to groups of viruses. In addition, if a "lower reproductive rate phenotype" is shared among a group of viruses, it is probably a result of genetic similarity due to identity by descent. In this case, kin selection may provide a better explanation than reciprocal altruism (although see below). However, the best reason for rejecting reciprocity as an explanation for virulence in the myxoma virus is simply the fact that individuals are not sacri- ficing their reproductive value with the expectation of repayment. Since lower reproductive rates would need to occur simultaneously in viruses inhabiting the same host, the necessary condition of repaid benefits cannot be met.

Nor does kin selection provide an adequate explanation for decreased virulence. It is likely that the degree of genetic similarity among viral strains within a host will be extremely high since the population of pathogens within a host tends to be initiated byjust a few strains, although more than one (Ewald 1994). This situation therefore meets the primary condition of kin selection-genetic similarity due to identity by descent. The problem with kin selection as an explanation for viral evolution is the fact that viral strains cannot be viewed as lineages in the same way that




groups of related animals are. Viral strains probably differ only by a small number of mu- tations, and to label these strains as different kin groups is misleading. Although the necessary conditions are met by this example, kin selection is probably not the best explanation for decreased virulence in myxomatosis, since different viral strains within one host are not kin groups in the traditional sense.

Group selection is the best explanation for the evolution of decreased individual reproductive rates of the myxomatosis virus. All of the necessary conditions are met. Groups are structured into isolated trait groups, each located on one host, all of which share a common fate. It should be noted, however, that since viruses are asexual, the term "structured deme" is not applicable (Shanahan 1990). The fitness of the group is directly proportional to the frequency of altruists (viruses with lower reproductive rates) in the group, the costs to the altruists (decreased reproductive rate), and the benefits to the group. Al- though a high frequency of altruists in a group is likely to be a result of identity by descent, it cannot be explained as a result of kin selection, for the reasons mentioned above. There- fore, the evolution of reduced virulence in the myxomatosis virus is best explained as a result of group selection.

FEMALE-BIASED SEX RATIOS IN SOCIAL SPIDERS

The most frequently cited example of evidence for group selection is the evolution of female-biased sex ratios (W\Vilson 1983; Wilson and Sober 1994). Williams (1966) argued that the lack of female-biased sex ratios in natural populations was strong evidence against group- level or biotic adaptations. As described by Fisher (1930), selection at the level of the individual would predict sex ratios of 1:1. In cases where this expectation is not apparent, the minority sex will always have a fitness advantage, resulting in an increase in the proportions of the minority sex. A population will eventually reach a stable equilibrium sex ratio (1:1), at which neither sex has a reproductive advantage based on gender alone. However, if selection takes place at the level of the group, female-biased sex ratios would be predicted, since group fecundity can be greatly increased by having more females than males in a group.

Populations with a female-biased sex ratio would thus have a reproductive advantage over populations with a 1:1 sex ratio. Williams (1966) argued that in all well-studied animal populations the sex ratio was typically 1:1 and, therefore, group-level adaptation was not observed. Since 1966, however, empirical examples of female-biased sex ratios have been described in the literature, especially in relation to social spiders (Hamilton 1967; Aviles 1986, 1993; Frank 1987).

Sex ratios of the social spider Anelosimus eximius have been measured in the field at the earliest stage at which sex can be determined, and an average bias of 6.7 females per male was found (Aviles 1986, 1993). If this is an ac- curate reflection of the primary sex ratio, as Aviles (1986) believes, the evolutionary pro- cess by which the female bias has evolved may contribute to an understanding of how altruism can be adaptive. The tendency on the part of some individuals to produce more females than males can be viewed as altruism since it increases the reproductive potential of the group at the expense of an individuals own fitness, relative to that of other group members (Colwell 1981; Wilson and Colwell 1981).

Although Hamilton (1967) demonstrated that it is theoretically possible to have female- biased sex ratios as a consequence of individual selection, this explanation does not appear to apply in this case. In Hamilton's model, mating occurs among the offspring of one or two foundresses within an isolated colony. Fer- tilized females then disperse to form their own colonies at some other location. If a colony is founded by a single female, it is to her advantage to produce the minimum number of males required to inseminate her female prog- eny. This would minimize competition among brothers for mates. For this reason, Hamil- ton's argument is often referred to as the local mate competition (LMC) model.

Wilson and Colwell (1981), however, demonstrated that within-group individual-level selection will result in a Fisherian 1:1 ratio if there are a number of generations of inbreed- ing. The colonies of A. eximius do not appear to fit the LMC model, since several generations of within-group mating occur. There- fore, the evolution of female-biased sex ratio in these spiders cannot be explained by the



JUNE 1999 SELECTION, ALTRUISM, AND PRIMA TE BEHA VIOR 187

individual-level selection model of Hamilton (1967). Similarly, reciprocity cannot provide an adequate explanation for female-biased sex ratios since this is not a behavior that can be repaid over a lifetime.

The best possible explanation for female- biased sex ratios in A. eximius is a combination of kin and group selection. Single parent colonies of A. eximius split to form new colonies (Vollrath 1982). These daughter colonies con- tinue to grow until they reach a size large enough to give rise to daughter colonies of their own. However, only large colonies "reproduce," and colony extinction is reported to occur frequently in small colonies (Overal and Ferreira 1982; Aviles 1986). Colonies with a female-biased sex ratio will grow faster and therefore have a greater probability of giving rise to new colonies, compared to colonies ex- hibiting a 1:1 sex ratio.

Although A. eximius colonies do fit Wilson's model of group selection in several ways (differential fitness of groups, low b/c ratio), they cannot be viewed as trait groups as they are defined by Wilson. Mating occurs only within the colony, and each colony behaves as an isolated deme. Therefore, although sex ratio bias in A. eximius can be explained by group selection, it probably fits the group-selection model developed by Maynard Smith (1964) better than that of Wilson (1975, 1980).

Distinguishing between kin and group selection is extremely difficult in this case. Since A. eximius colonies are extremely inbred, the genetic similarity resulting from identity by descent in the colonies is high. This leads to an increase in variance among groups, while genetic variation within groups remains low. The frequency of altruists (females producing more daughters than sons) within a colony would therefore be high. The evolution of a female-biased sex ratio in A. eximius can best be explained as selection among competing groups of kin, and therefore as a result of kin selection.

FORAGING SPECIALISTS AMONG

COFOUNDING ANT QUEENS

The best example of empirical evidence for group selection is Rissing et al.'s (1989) study of specialized foragers among newly formed associations of leaf cutter ants, Acromyrmex ver-

sicolor (Wilson 1990; Dugatkin et al. 1992). In this species, ant colonies are initiated by multiple, unrelated foundresses. Some of these foundresses leave their nests before the emer- gence of the first workers to forage for leaves that will be shared communally, and in doing so are at greater risk of predation. This altruistic behavior enhances colony fitness at the expense of the relative fitness within groups of the individual foraging ant. Of the four possible explanations for this altruistic behavior (individual selection, reciprocity, kin selection and IGS), intrademic group selection provides the best possible explanation for the results of Rissing et al.'s study.

Individual selection predicts that a foundress will not share procured leaves with the entire colony. The possibility does exist that she is simply competitively inferior, and is forced into a subordinate role in the dominance hierarchy (Vehrencamp 1983). In this case she would be maximizing her individual fitness in the given social environment, and her apparently altruistic behavior may still represent an evolutionary stable strategy. However, this explanation is unlikely, since aggression and ritualized dominance among foundresses in these colonies has never been observed (Rissing et al. 1989).

In addition, reciprocity does not work as an explanation for this behavior, since not all foundresses within a colony forage equally. In fact, in all colonies observed, foraging trips were almost always performed by the same single foundress. A second foraging specialist was observed in only two of the eleven colonies studied, and in both cases the second forager appeared only after the death of the first foraging foundress. Therefore, mutual reciprocity is an unlikely explanation for this behavior, since the necessary condition of delayed pay- ment is not met. It should be noted, however, that the benefit may be repaid in some other currency (see below) . A repayment of this type was not described by Rissing et al. (1989), but further studies on this species may provide evidence for reciprocity.

Genetic studies have shown that among colonies initiated by numerous cofoundresses, the genetic similarity among them is no greater than genetic similarity of queens cho- sen at random. This means that the degree of




relatedness within the association of cofoundresses is no greater than the degree of relatedness between foundresses from different colonies. Therefore, kin selection cannot explain the presence of this altruistic behavior.

Newly founded nests of these ants are extremely vulnerable, and often only one colony from an original cluster of several will survive. The primary benefit of foundress associations is argued to be defense from conspecific ene- mies. New colonies are often spatially clumped, and often participate in reciprocal colony raids that eventually result in the survival of only one colony. In this form of intercolony competition, larger colonies tend to prevail (Rissing and Pollock 1987, Rissing et al. 1989). This means that relatively small differences in colony efficiency and reproduction could greatly influence the ultimate reproductive success of the colony.

Rissing et al.'s study provides an example in which selection is probably taking place most effectively at the level of the trait group or colony. All of the conditions for IGS are met. Pop- ulations are structured into isolated trait groups whose members share a common fate. Although the frequency of altruists may be low, the ratio of cost to benefit is extremely low as well. The energy expenditure required to forage is a small cost to pay for group survival. Since the presence of this altruistic behavior cannot be explained by genetic similarity (owing to identity by decent or otherwise), nonkin intrademic selection is the best possible explanation for the evolution of this form of altruism among newly formed foundress associations of ants. Although this may be an example of evolution through trait-group selection, the general paucity of examples in the literature indicates that IGS may only play a small role in explaining the majority of altruistic behaviors observed in nature.

RELEVANCE OF PRIMATES FOR

FURTHER RESEARCH

The evidence for group selection of altruistic traits discussed thus far all refer to studies conducted on invertebrates. Other than studies of altruism among humans, little evidence has been provided for group selection of altruism among more complex social animals such as mammals. Although the dilemma of altru-

ism is especially relevant to the field of primatology, where the social behaviors that are studied are well developed and complex, the topic of group selection is avoided by most primatologists. Traditionally, altruism among mammals has been attributed to either reciprocity or kin selection. However, results of studies on baboons (Noe 1986; Bercovitch 1988) and related studies on lions (Grinnell et al. 1995; Heinsohn and Packer 1995) fail to support theories of kin selection and reciprocity, suggesting that altruism among primates may require further investigation.

There are numerous examples of supposed altruism that are of particular interest to primatologists. Two will be considered here: formation of coalitions, and alarm calls. There is a need for a comprehensive review of these behaviors in relation to explanations offered for each. Although group selection may not be a driving force in the evolution of altruism in primates, as it may be in viruses or social spiders, new models of group selection need to be investigated and evaluated by primatologists, rather than simply dismissed, as they have been in the past.

FORMATION OF COALITIONS

The formation of coalitions or alliances in apes and monkeys has been widely recognized and frequently cited as an example of altruism (Axelrod and Hamilton 1981). Males often form alliances to overthrow dominant or con- sorting males and thus to gain access to sexu- ally receptive females (Packer 1977; Noe 1986). In addition, many primate females have been observed to intervene on behalf of both higher- ranking and lower-ranking individuals during acts of aggression (Silk 1982, 1987; Cheney and Seyfarth 1990). The individual who inter- venes experiences a greater risk of injury, as well as an increased expenditure of energy, in exchange for little or no immediate benefit. This behavior certainly appears to be altruistic on the part of the interloper.

Coalition formation is frequently explained as a result of kin selection, since there is over- whelming evidence that females form coalitions with related females more frequently than with members of other matrilines (Cheney and Seyfarth 1990; Silk 1982). In addition, the degree to which an individual is likely to inter-




vene seems to be proportional to the degree of relatedness between them. In other words, a female appears to be more likely to intervene in disputes with higher ranking individuals on behalf of a close relative than for a distant relative (Chapais 1983; Silk 1982). However, coalitions have also been reported to occur between unrelated females in macaques (Macaca radiata, Silk 1982) and vervet monkeys (Cerco- pithecus aethiops, Cheney and Seyfarth 1990). Hence, kin selection alone is not a sufficient explanation for the evolution of coalition formation in all primate females.

Similarly, coalition formation among male baboons cannot readily be explained by kin selection. Since males usually transfer from their natal group (Packer 1977), the degree of genetic similarity among them is assumed to be low. The possibility exists that males may have brothers or other kin within the group, but to date there is no evidence for or against males preferentially forming coalitions with relatives. Therefore, kin selection is unlikely to provide an explanation for the selection of coalition formation.

Reciprocity is the most frequently invoked explanation for primate coalitions. In a series of field experiments using playback vocaliza- tions, Seyfarth and Cheney (1984a) found that vervet monkeys were more likely to respond to a distress call of an individual who had recently groomed them than to those who had not. This type of reciprocity shows that the currency of cost (i.e., grooming) and benefit (i.e., assistance when in distress) need not be the same. In 1977, Packer also argued that male- male coalitions in Papio anubis were a result of reciprocal altruism. He found that each male sought coalitions with the same male who re- quested aid from him. In addition, males were more likely to join coalitions with males who would be capable of assisting, rather than with females or low ranking males. The males studied had transferred into the group at different times and were unlikely to be related. The results of Packer's study seemed to provide convincing evidence for the evolution of altruism through reciprocity.

Additional research on baboon coalitions, however, by Bercovitch (1988) and Noe (1986), and studies of lions by Packer and colleagues (Grinnell et al. 1995; Heinsohn and Packer

1995; Packer and Pusey 1982) suggest that reciprocity may not always provide an adequate explanation for the evolution of male-male coalitions. Mutualism (that is, cooperation with immediate benefits for both actors) is now believed by these workers to provide a sufficient explanation for coalitions. Therefore, coalitions are not truly altruistic, but rather simply a result of selection for immediate benefit. Bercovitch (1988) found that males who so- licit other males tojoin coalitions do not have a higher probability of gaining access to females than males who respond to the solicita- tion. Since both males probably have an equal chance of gaining access to the female, and the cost of coalition formation is relatively low (although see Packer 1977; Smuts 1985), individual-level selection can explain the evolution of some male-male coalition formation. There is no evidence for delayed benefit in this case, as would be expected if coalitions were a form of reciprocal altruism.

In related work, Grinnell et al. (1995) and Heinsohn and Packer (1995) found similar results in their study of coalition formation among lions. These studies employed play-back experiments simulating the approach of an intruder to evaluate the formation of territorial defense coalitions. Results demonstrated that some individuals consistently approached the "intruder" while others consistently lagged be- hind. This behavior cannot therefore be explained by reciprocal altruism, because there is no apparent delayed benefit for the altruist (the individual who participates in the group defense).

There is a crucial distinction to be made between the results of Bercovitch's (1988) study on baboons and those of the lions (Grin- nell et al. 1995; Heinsohn and Packer 1995). Coalition formation among the baboons was against other group members, whereas lion coalitions were formed for group defense. Be- cause of this difference, coalitions among baboons cannot be attributed to intrademic group selection, while lion coalitions can. IGS cannot explain baboon coalitions because groups that have "altruists" would not have a higher overall fitness than groups that do not. Baboon coalitions are likely to be a result of simple individual-level selection for a mutually beneficial behavior.




IGS may provide a possible explanation for coalition formation among the lions. Like Ber- covitch (1988), Grinnell et al. (1995) attri- bute coalition formation to mutualism. How- ever, within the lion groups, those individuals that partake in group defense have a lower fitness relative to group members who lag be- hind. Although the cost of cooperation in this case is likely to be high, the benefit to group members (access to territory and mates) is presumed to be higher. Overall, groups containing altruists will have a higher survival rate than groups that do not. This conforms to Wil- son's (1980) definition of "weak altruism."

If females within a lion group are closely related, female group defense may be a result of kin selection (Packer et al. 1991). However, in a lion group, lagging females are also closely related to defending females, and males are generally unrelated to other group members (Grinnell et al. 1995), so kin selection alone could not maintain this behavior in lion prides. Therefore, it is possible that cooperative defense among lions could have evolved through intrademic group selection, although coalition formation among baboons is best explained as a result of individual-level selection. The results of the lion studies therefore suggest that primate coalitions formed for defense against outsiders or predators need to be more closely examined.

ALARM CALLS

Biologists, including Darwin (1871), have long debated the functional significance and evolution of alarm calls (Sherman 1977; Cheney and Seyfarth 1985). Alarm calls and group defense are different from other altruistic acts such as food sharing, grooming, and coalition formation (against fellow group members) in that they are undirected forms of altruism. The benefits derived from alarm calls and group defense are shared equally by all members of the group, while only one or a few individuals benefit from food sharing, grooming, and coalitions.

Virtually all primates produce alarm calls (Cheney and Wrangham 1986), and many species have an extensive vocal repertoire in which different alarm calls warn against different kinds of predators (Struhsaker 1967; Sey- farth and Cheney 1984b) . Whether alarm calls

are truly an altruistic behavior is a matter of debate. Trivers (1971) argued that alarm calls are not altruistic, but rather they are directly advantageous to the caller. According to Triv- ers, if predators are successful in catching members of a given species, they are likely to learn the habits of that species and revisit the habitat in which members of that species are found. Trivers, therefore, argues that alarm calls, which prevent predators from eating conspecifics, are selected for at the level of the individual and do not result in a sacrifice on the part of the caller.

Sherman's (1977) classic studies of Belding's ground squirrels, Spermophilus beldingi, provided evidence that alarm calls were a result of kin selection in this species. Females with offspring and kin in the group were found to call more frequently than females without kin. In addition, the frequency of male calls decreased significantly after they left their natal group.

The evidence for kin selection for alarm calling among primates is not as obvious. Among some baboons, the most vocal individuals were males who had recently immigrated into the group (Busse 1984) and therefore were unlikely to be related to other group members. Studies of captive vervets, Cercopi- thecus aethiops, suggest that when females are located near kin, they will call more frequently than when in the presence of nonkin (Cheney and Seyfarth 1985). However, studies of free- ranging vervets find no correlation between frequencies of calls and presence of kin (Cheney and Seyfarth 1990).

Alarm calls among primates may be a result of reciprocal altruism. If true, one would expect all members of a group to call at relatively the same frequency, but this does not seem to be the case. In fact, the rate of alarm calling often varies greatly between individual animals within the same group. In vervets, frequency of calling has been found to differ significantly among animals of different ranks, with higher ranking individuals calling more often (Struhsaker 1969). However, alarm calls may be a result of reciprocity if the caller is "repaid" in a different currency. This is difficult to determine in observational field studies, and new methods of investigating variable currencies of reciprocal altruism are needed.




Primate alarm calls may also be favored by intrademic group selection. Neither reciprocity nor kin selection seem to provide an adequate explanation for this behavior. The conditions required for IGS with respect to alarm calls are met for most primate groups. The cost of alarm calling could be high (if calls draw attention to the caller) or low (if the acoustics of the call make the source difficult to locate). However, the benefit to the group is large even if there are only a few callers in the group. Groups that contain altruists, or callers, are likely to have a lower mortality rate than those that do not. Within the group, animals that call may have a relatively lower fitness compared to those that do not call. Com- pared to the population at large, however, callers may have a relatively high fitness, as their group size will not diminish significantly because of predation. They may therefore re- tain all the benefits of group living, such as resource defense (Wrangham 1980) and decreased probability of predation (Hamilton 1971).

Future studies of primate alarm calls will need to investigate intergroup variation in alarm calling frequencies and group mortality rates. Most studies of altruism among primates have focused on differences in fitness among individuals within a single group. When test- ing the four possible explanations for the evolution of altruism, it is necessary to have data on group variation in altruistic behaviors. Al- though intrademic group selection is unlikely to have been a significant force in the evolution of food sharing or baboon coalition formation, it may provide an explanation for alarm calls or other types of cooperative group defense observed in primates.

CONCLUSION

It is clear that seeking adequate explanations for the evolution of altruism presents a challenge for those who study animal behavior. Historically, researchers have turned to models of selection that acts at various group levels, all higher than the individual, to explain this phenomenon. The validity of these models has been debated at length, and there is no current consensus. Different altruistic behaviors are likely to have evolved through different forms of selection and, therefore, each example of apparent altruism needs to be evaluated separately.

The four hypotheses commonly employed to explain altruism (individual selection, reciprocity, kin selection, and group selection) can be clearly delineated, and predictions based on each hypothesis can be tested. Of these mechanisms, group selection has proven to be the most controversial. The extent to which group selection hypotheses are supported by empirical data still is open to ques- don. Nevertheless, possible evidence for group selection models has been documented in studies of avirulent virus strains (Ewald 1994) and foraging ant queens (Rissing et al. 1989).

Researchers studying mammal behavior, particularly primatologists, up to now have largely dismissed models of group-level selection. Although primates exhibit a wide variety of altruistic behaviors, they may not be ideal subjects for studying group selection, as their life spans are long and reproductive success is difficult to measure. Even so, there is a growing need for those who study behavior, especially primatologists, to reevaluate the traditional paradigms for the evolution of altruism. Once group selection hypotheses have been investigated and predictions have been tested, ethologists can acquire a better understanding of how natural selection explains altruistic behaviors.

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