The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation

Behavioural Processes 53 (2001) 21 – 40 www.elsevier.com/locate/behavproc

The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation Zuleyma Tang-Martinez Department of Biology, Uni6ersity of Missouri –St Louis, 8001 Natural Bridge Rd, St Louis, MO 63121, USA Received 23 August 1999; received in revised form 26 September 2000; accepted 4 October 2000

Abstract I re-examine the four most widely proposed mechanisms of kin discrimination among vertebrates and conclude that the current categorization of kin discrimination mechanisms has been counterproductive because it has a hindered a clear understanding of the basic mechanisms by which animals discriminate kin. I suggest that there likely is only one authentic mechanism of kin discrimination and that this mechanism is learning, particularly associative learning and habituation. Observed differences in the way animals discriminate between kin and non-kin are due only to the cues (e.g., individually-distinctive, family-distinctive, or self) that are used, and not to different mechanisms per se. I also consider whether kin discrimination is mediated by specially evolved kin recognition systems, defined as neural mechanisms that allow animals to directly classify conspecifics as either kin or non-kin. A preliminary analysis of vertebrate recognition systems suggests that specialized neural, endocrine, and developmental mechanisms specifically for recognizing kin have not evolved. Rather, kin discrimination results from an extension of other, non-specialized sensory and cognitive abilities of animals, and may be derived from other forms of social recognition, such as individual, group, or species recognition. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Evolution of recognition; Individual recognition; Kin discrimination; Kin recognition; Mechanisms of recognition; Recognition cues; Role of kin selection; Social recognition

1. Introduction Ever since Hamilton (1964) proposed his revolutionary concept of kin selection to explain social evolution and the evolution of ‘‘altruistic’’ behaviors, there has been a strong interest in kin recognition and the mechanisms by which animals are able to distinguish between their kin (geneticallyrelated individuals) and non-kin (genetically-unreE-mail address: [email protected] (Z. Tang-Martinez).

lated individuals). Kin recognition is considered such an important process for the operation of kin selection, that many behavioral ecologists seem to implicitly assume that specialized mechanisms allowing individuals to distinguish their kin from non-kin must have evolved (e.g., Hepper, 1991, p. 281; also below). The concepts of kin selection and kin recognition were so closely linked that Hamilton (1964) immediately hypothesized that kin discrimination might occur as a result of ‘‘recognition alleles’’, genes that code for

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a cue or label that would be shared by kin and would also allow the recognition of kin. Moreover, he suggested that such a system of alleles might also regulate the performance of preferential behaviors toward kin. Dawkins (1976) further developed this concept and named it the ‘‘green beard effect’’. For the purposes of this paper, recognition alleles will be treated as synonymous with the green beard effect. In doing so, I am following precedents set by Alexander and Borgia (1978), Dawkins (1982) and Wilson (1987), among others (but see also Crozier, 1987, for a clarification of the two terms). The earliest experiments on the mechanisms of ‘‘kin recognition’’ (see next section for alternative definitions) were designed to test the recognition alleles hypothesis. These experiments used separately-reared kin (cross-fostered siblings or siblings from different litters) to examine whether animals could discriminate kin with whom they had not previously associated (i.e., unfamiliar kin). The initial assumption was that, if animals did not have to associate with kin in order to distinguish them, then the discrimination must be genetically-based or ‘innate’. However, as data from studies using unfamiliar kin (e.g., Wu et al., 1980) began to be published, it became clear that it would be extremely difficult, if not impossible, to empirically demonstrate the existence of recognition genes (Holmes and Sherman, 1983) because it was not possible to eliminate learning due to kin association in the womb (in the case of most mammals) or the learning of family-specific cues from the mother, other siblings, or even from self. Moreover, repeated attempts by one of the original co-authors to replicate the Wu et al. (1980) results were unsuccessful (Frederickson and Sackett, 1984; Sackett and Frederickson, 1987). As a result, over time, several other mechanisms began to receive attention and the concept of recognition alleles fell into disfavor, although it has never been completely eliminated as a potential mechanism for recognition. The purpose of this commentary is to re-examine the currently accepted categorization of ‘kin recognition’ mechanisms (Holmes and Sherman, 1983; Sherman and Holmes, 1985; Komdeur and Hatchwell, 1999) and to suggest that an alternative

classification may not only be more realistic and parsimonious, but also more useful. Although I question many of the existing ideas on the evolution and mechanisms of kin discrimination, this critique is not intended to stifle either research or theoretical contributions in these areas. On the contrary, it is my intention to stimulate additional discussions, help generate new research, and encourage new ways of thinking about the mechanisms of kin discrimination. The prevailing categorization lists four different mechanisms of ‘kin recognition’: (1) spatial location; (2) association or familiarity; (3) phenotype matching; and (4) recognition alleles, sensu Hamilton (1964). This categorization has provided a valuable framework that has helped to organize our thinking on this topic. However, data collected over the last 25 years suggest that the time has come for a critical re-evaluation of the proposed mechanisms. I will argue that there is only one genuine ‘mechanism’, that this mechanism is learning as a result of familiarity, and that the only real difference in the processes by which animals discriminate kin from non-kin hinges on the cues that the animals use. Hence, the currently popular and widely invoked dichotomization of mechanisms into ‘recognition by association’ and by ‘phenotype matching’ is particularly misleading and confusing because, regardless of what cues an animal uses for kin discrimination, all discrimination ultimately involves both association and phenotype matching. Moreover, in vertebrates, the ability to distinguish between kin and non-kin probably represents the extension of pre-existing sensory capabilities rather than the evolution of any specialized kin recognition system or mechanism.

2. Definitions Before proceeding with this critique, it is necessary to define the relevant terms, as I will be using them in this paper. In the kin recognition literature, at least three concepts have been used and often times confounded, including at times by this author. The following definitions are modifications of those proposed by Hepper (1991) and Barnard et al. (1991).

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Kin discrimination refers to the differences in behavioral responses that an individual shows toward its kin as compared to non-kin, based on conspecific labels or cues that are correlated with kinship. In this paper, ‘kin discrimination’ refers only to these behavioral responses and does not imply anything about the cognitive substrates of the responses. It also does not require that the animal discriminate directly on the basis of kinship, defined as the sharing of common alleles as a result of common, recent descent. On the other hand, kin recognition refers to the cognitive mechanisms (i.e., neural processing) that takes place and allows animals to classify conspecifics as either kin or non-kin (see also Byers and Bekoff, 1986; Waldman et al., 1988; Barnard et al., 1991). The behavioral discrimination of kin may allow us to infer kin recognition, but the latter can never be observed directly because it is a neural process. Likewise, kin discrimination may occur without kin recognition if, for example, the animal discriminates behaviorally among kin and non-kin based on conspecific cues that function primarily in species or individual recognition (see Hepper, 1991; Barnard et al., 1991; and below). Since we do not know what neural mechanisms come into play when an animal discriminates kin from non-kin, it begs the questions to refer to these mechanisms as ‘kin recognition’ mechanisms. For this reason, in the remainder of this paper, I will use the broader and more inclusive term ‘kin discrimination’ mechanisms, unless I am referring to earlier work and it would be confusing to change the terminology used by previous authors. Ancillary kin bias occurs when individuals demonstrate differential behaviors toward kin versus non-kin as a result of indirect, locational or behavior-mediated information that is only incidentally correlated with kinship, rather than as a result of direct conspecific cues. This category corresponds to Hepper’s (1991) ‘‘kin bias’’ and Barnard et al. (1991)’s ‘‘non-discriminatory effects of genetic similarity’’. It is critical to recognize that these three terms represent very different aspects of what generally and loosely has been termed ‘kin recognition’;

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these differences are important if we are to understand the processes and mechanisms that animals use to respond preferentially to kin and non-kin. For example, kin recognition can occur without kin discrimination. That is, an individual may recognize a conspecific as its kin, but not behave in a differential manner toward it as compared to a non-kin. Because we generally infer kin recognition from kin discrimination, an absence of kin discrimination can erroneously be interpreted as a failure of kin recognition. Furthermore, if we observe that an animal behaves differently toward its kin as compared to its non-kin, this does not necessarily mean that kin recognition is the process responsible for this kin-biased behavior. If littermates have a preference for a particular microhabitat, kin may be found in closer proximity and may interact more with one another than with non-kin, but this differential treatment would be only a by-product of a shared preference for the same microhabitat, an example of ancillary kin bias (see Hepper, 1991 and Barnard et al., 1991). The definitions I use in this paper are similar, but not identical to, those proposed by Barnard et al. (1991). Barnard et al. (1991) define kin discrimination as the ability to distinguish between kin and non-kin based directly on kinship, as a result of kin recognition; they consider what I term ‘kin discrimination’ to be a subcategory of ‘kin bias’. Since, at present, it is not possible to determine when an animal discriminates because it distinguishes kin from non-kin directly on the basis of kinship, and when it discriminates based on conspecific cues that merely correlate with genetic relatedness, I consider Barnard et al. (1991)’s definitions to be unnecessarily rigid and complicated and prefer the definitions used by Hepper (1991). To summarize, my definition of kin discrimination does not require that kinship, strictly speaking, be the direct basis of discrimination. Instead, discrimination occurs whenever conspecific cues that merely correlate with genetic relatedness result in differential behaviors directed to kin versus non-kin. However, I do agree with Barnard et al. (1991) that kin recognition requires an evolved neural mechanism that specifically distinguishes

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among individuals, based on kinship and that functions as a ‘decision maker’ determining appropriate responses to kin versus non-kin. I take it as a given that kin discrimination and ancillary kin bias exist. The question that remains pertains to the cognitive and neural mechanisms by which animals discriminate between kin and non-kin. I use ‘discriminator’ to refer to the animal that is attempting to discriminate between kin and non-kin, regardless of whether or not it actually is able to discriminate successfully. ‘Target’ refers to a newly encountered individual that the discriminator attempts to identify as its kin or non-kin. ‘Cue’ refers to any one phenotypic trait, combination, set, or spectrum of traits produced by the target that a discriminator uses for social ‘assessment’. Cues may be genetically coded or environmental in origin (or a combination of both). ‘Marker’ and ‘label’ are used synonymously with ‘cue’ and do not imply anything about complexity, origin, or specific function of the phenotypic trait.

3. Spatially-based recognition The first discrimination mechanism listed by Sherman and Holmes (1985) is ‘‘spatially-based recognition’’. They describe this mechanism as one in which an individual recognizes as kin any other individual encountered within a given space (recognition being defined as showing differential behaviors toward the conspecific). Thus, an individual may treat as ‘kin’ any other individuals encountered within a 25 m radius of the focal individual’s den. It is assumed that such a mechanism may evolve when there is a high probability that individuals found within a given location will be genetically related to one another. For example, an individual from a highly philopatric species, in which littermates always stay within their mother’s home range, can fairly reliably assume that any other conspecific it encounters within the mother’s home range will be a relative (e.g., a sibling or the mother) and should be treated as kin. The problem, however, is that any conspecifics found in the pertinent location will be treated as kin, regardless of whether or not they are, in fact, genetic relatives.

The concept of spatially-based recognition as formulated by Holmes and Sherman (1983) and Sherman and Holmes (1985) does not appear to depend on the learning of relevant sensory cues shared by all members of a family. That is, individuals are not discriminated as kin because they all share a family or group-specific cue or an environmentally-acquired label. Because of this, spatiallybased recognition differs from the mechanism described in some social Hymenoptera in which cues derived from the nest, from shared food, or from queen chemosignals provide all members of the nest with a common odor that serves as the cue for discriminating nestmates (e.g, Kalmus and Ribbands, 1952; Shellman and Gamboa, 1982; Pfenning et al., 1983; Gamboa et al., 1986; Breed and Bennet, 1987). To the contrary, when ‘spatially-based recognition’ is applied to vertebrates, the only cue the discriminator is presumed to use is spatial proximity to a particular locality and not an environmentally derived cue that serves as a label. Outside of the specific locality, the discriminator treats any target (related or not) as non-kin. Elsewhere (Halpin, 1991), I have argued that ‘spatial recognition’ actually represents a failure of recognition and, therefore, should not be considered a mechanism of kin recognition. It is precisely because individuals cannot recognize kin as such that all conspecifics encountered in a particular area are treated the same (presumably preferentially), regardless of their true genetic relationship to the discriminator. Rather than being a mechanism of kin recognition, ‘spatially-based recognition’ is most likely an instance of ancillary kin bias. Because in the early formulations (e.g. Holmes and Sherman, 1983), differential behaviors were accepted as ipso facto evidence of kin recognition, apparent kin discrimination and kin bias were confounded with kin recognition. This confound has resulted in theoretical confusion and has impeded a clearer understanding of the mechanisms by which animals recognize and/or discriminate between kin and non-kin. Of course, when life history characteristics are such that spatially-based preferential behaviors are directed primarily or most commonly toward kin, individuals showing such behaviors may

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benefit indirectly by an increase in their inclusive fitness, and spatially-mediated preferential behaviors may be under strong positive selection. However, the fact that animals benefit from engaging in spatially-mediated behaviors is not evidence that these animals can recognize their kin, nor does it support the conclusion that spatially-based differential behaviors represent a kin recognition mechanism. (See also discussions by Blaustein, 1983; Waldman, 1987; Halpin, 1991.) In other words, from an evolutionary perspective it may well be advantageous for kin to aggregate and for individuals to behave preferentially towards nearby kin, whether or not this behavior is the result of kin recognition per se. The dispersal patterns that result in genetic relatives settling in close proximity to one another may have been selected and may increase survival and reproductive success; kin bias behavior, exemplified by close kin interacting preferentially with one another, could then have arisen as a corollary and consequence of these dispersal patterns. Some may argue that this criticism is irrelevant if one is interested primarily in the evolutionary consequences of the behavior. This may be true, but it begs the question of the underlying cause of the behavior. A lack of knowledge, or a misunderstanding, of the proximate mechanisms of behavior can lead to erroneous conclusions about evolution and function. Real (1994) stresses the critical importance of mechanisms to an understanding of the evolutionary significance of behavior: ‘‘The only successful way to think about behavior is to unite its internal mechanistic foundations with its external effects in specific ecological settings, and to recognize that the internal and external worlds of the organism are united through the action of natural selection and evolution’’. Likewise, Stamps (1991) suggests that ‘‘...information on behavioral processes may be critical for answering a variety of evolutionary questions’’. In summary, it is not enough to argue that the consequences of a behavior (e.g., kin bias) may be adaptive and that is all that matters in the long run. To adequately understand the behavior and the evolutionary forces that have influenced it, it is imperative also to understand the underlying processes and mechanisms that have given rise to the behavior.

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4. Recognition by association and by phenotype matching By the early 1980s, recognition by association and by phenotype matching had become the two most widely accepted mechanisms of kin discrimination (Holmes and Sherman, 1983), and most studies after 1981 were designed to distinguish between these two mechanisms (e.g., Waldman, 1981; Holmes and Sherman, 1982; Grau, 1982; O’Hara and Blaustein, 1982; Frederickson and Sackett, 1984; Halpin and Hoffman, 1987). The question became whether a period of previous association (e.g., prior to weaning or fledging) was necessary in order for kin to ‘recognize’ one another (i.e., ‘recognition by association’), or whether kin discrimination could occur even in the absence of any previous, direct association between the discriminator and the target. In the latter case, ‘recognition by phenotype matching’, it was hypothesized that the discriminator learns certain phenotypic cues from self, or from kin with which it does associate (e.g., parents or siblings), and then matches the phenotype of the newly encountered, unfamiliar target to the learned phenotype of self or known kin. Numerous studies on a variety of vertebrates documented that kin discrimination was mediated primarily by previous association (e.g. Porter et al., 1981; Dewsbury, 1982; Holmes and Sherman, 1982; Gavish et al., 1984; Boyd and Blaustein, 1985; Halpin and Hoffman, 1987), but some studies also found evidence of discrimination by phenotype matching (e.g. Blaustein and O’Hara, 1981, 1982; Grau, 1982). Despite early evidence that, in some species, both mechanisms co-exist and can be demonstrated under different experimental conditions (e.g., Waldman, 1981; Kareem and Barnard, 1982; Hepper, 1983; Porter et al., 1983; Holmes and Sherman, 1982; Grau, 1982 vs Halpin and Hoffman, 1987; Waldman, 1987; see also recent papers by Heth et al., 1998; Todrank et al., 1999) most researchers treated the two hypothetical mechanisms as dichotomous (e.g. Gavish et al., 1984; Halpin and Hoffman, 1987). Moreover, despite the clear formulations of Holmes and Sherman (1983) and Sherman and Holmes (1985) asserting that both mechanisms

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involve learning, some researchers continued to think of phenotype matching as a mechanism that has genetic (or ‘innate’) underpinnings (because early social experience with target kin is not necessary for discrimination to occur), while understanding that recognition by association represents an example of learned discrimination. The dichotomization of ‘recognition by association’ (familiarization) and by ‘phenotype matching’, as they have traditionally been defined, is not only inaccurate, but also hinders our understanding of the basic mechanisms by which animals discriminate kin. The very labels given to these two processes are fallacious and confusing. First, the use of the word ‘recognition’ assumes that we understand the underlying neural mechanism and that the animals are classifying conspecifics directly on the basis of kinship. Since we do not know the neural and cognitive mechanisms involved, this assumption is not valid. Second, ‘recognition by association’ requires the learning of a phenotype by association with an individual (the genetic relative) and the subsequent matching of this learned phenotype to that of the target. In other words, ‘recognition by association’ requires both previous association and ‘phenotype matching’. ‘Recognition by phenotype matching’ likewise requires previous association with, and learning of, phenotypic cues (in this case, cues produced by known kin or by self), followed by the subsequent matching of this learned phenotype to that of the target individual. Thus, the primary difference between ‘recognition by association’ and by ‘phenotype matching’ is the cue that is learned and later matched to the target. Specifically, in ‘recognition by association’ the animal learns the individually-distinctive cues of its kin, whereas in ‘phenotype matching’ the animal learns family cues associated either with self and/ or genetic relatives. When utilizing such familydistinctive cues, animals may rely on an absolute cue that is identical in all family members or, instead, on relative similarities between the learned phenotype and the phenotype of the target (see below), but the basic mechanism for discriminating between kin and non-kin is the same in all cases: first a phenotype is learned as a result of previous association and then it is com-

pared (matched) to the phenotype of the target. Thus, learning and familiarization are critical components for kin discrimination, an idea consistent with Bekoff (1981)’s ‘‘familiarity coefficient’’. This analysis suggests that the terms ‘recognition by association’ and ‘recognition by phenotype matching’ should be dropped from the kin recognition literature. This was first suggested by Porter (1988), but his carefully reasoned arguments were largely ignored. Porter advocated the use of the terms recognition by ‘direct familiarization’ for situations in which previous association between the discriminator and target were necessary for later recognition. On the other hand, recognition by ‘indirect familiarization’ would be used to refer to those situations in which direct association between discriminator and target were not necessary (but association and familiarization with other kin or with self are necessary). The need for new terminology is based on more than semantics. As discussed above, the terms ‘phenotype matching’ and ‘recognition by association’ are inaccurate and confusing when they are presented as dichotamous mechanisms. Moreover, words can shape our thinking. A lack of clarity in terminology can result in a lack of clarity in formulating questions, designing experiments, and interpreting results. The time has come to adopt Porter’s terminology because it provides a more accurate and less muddled formulation of the mechanisms of kin discrimination correlates well with a classification based on the cues that are used: individually-distinctive for direct familiarization and family-specific for indirect familiarization. However, for the reasons explained above, I suggest that the term ‘discrimination’ by direct or indirect familiarization be substituted for ‘recognition’. The possible use of self-generated cues (e.g., Heth et al., 1998) raises a number of interesting issues. First, an animal that uses such a cue must be able to perceive the relevant cue. While the animal can probably perceive self-generated odors or sounds quite easily, the same is unlikely to be true for many visual cues, particularly those confined to the facial area, and particularly in animals that do not have the ability to observe

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their own reflections in pools or other ‘mirrors’. Thus, one can predict that species that rely on self-generated cues for kin discrimination should use olfactory and auditory cues rather than visual cues (unless these cues are located on easily seen areas of the body, such as limbs). In a survey of cues used for kin discrimination (Halpin, 1991), there were no cases found in which animals use vision for discrimination by indirect familiarization. In the few species in which visual cues may play some role in parent-offspring or sibling discrimination (e.g., cliff swallows, Hirundo pyrrhonota: Stoddard and Beecher, 1983; sheep, O6is aries: Alexander, 1977; Alexander and Shillito Walser, 1978) the cues seem to be individually distinctive and must be learned by the discriminator during social experience with the target. A second consequence of the use of self-generated cues for kin recognition is that the discriminator does not always need to retain a long-term memory of its own phenotype. Instead, in some cases (e.g., when using olfactory cues) it may be sufficient for the discriminator to match the phenotype of the target to the self phenotype stored in procedural or working memory, as a result of previous self-inspection or familiarity with self. Such a mechanism would require less complex neural processing, but it is not known if such a mechanism actually exists. A corollary of this observation is that, while animals that use direct familiarization may forget the learned phenotype after some period of separation from the relevant kin (e.g., Paz y Min˜o and Tang-Martinez, 1999), those that use indirect familiarization, particularly if they utilize self-generated cues, may be able to discriminate between kin and non-kin throughout their lives. In these cases, ‘forgetting’ becomes irrelevant since the discriminator always has its own phenotype to use as a reference when encountering a target. It is also to be expected that some species may have evolved the ability to use both direct and indirect familiarization. Perhaps, in such species individuals will rely on indirect familiarization when cues learned during early development are not present or have been forgotten.

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The characteristics of the cues used for discrimination also influence whether discrimination of kin is discrete or proportional. By discrete I mean that the discriminator behaves as if it can determine only whether a target is, or is not, a genetic relative but cannot determine different degrees of relatedness. This would represent a threshold effect and the behavior of the discriminator would depend on whether or not there is a tight match between the learned template and the label of the target. On the other hand, when discrimination is proportional (sometimes also called ‘graded’ or ‘continuous’) the discriminator will behave as if it is able to make finer discriminations and will treat close relatives differently from the way it treats more distant relatives (e.g., Hepper, 1987a; Heth et al., 1998). Discrimination by direct familiarization must be discrete, since targets appear to be discriminated as individuals. Discrimination by indirect familiarization, on the other hand, may be either discrete or proportional. In the case of discrete indirect familiarization the discriminator can be expected to learn a discrete cue (or cue components) that is family-specific. That is, from the perspective of the discriminator, all members of the family will share the exact same cue and the discriminator uses presence or absence of this cue to shape the way in which it responds to the target. Alternatively, if the discriminator uses the relative similarity of the target’s phenotype compared to the learned family or self phenotype, then it may discriminate by behaving differently toward more closely related individuals (the target phenotype is more similar to the learned phenotype) in contrast to the way it behaves to less closely related individuals (the target phenotype is less similar to the learned phenotype but there are enough similarities that the discriminator generalizes to the phenotype that it has learned). Hence, this type of discrimination would rely on ‘goodness of fit’ between the learned and target phenotypes. Which type of discrimination occurs will depend in large part on the nature of the individualand family-specific cues used in recognition. Many of these cues are probably quite complex and consist of a number of different components. Thus, if we consider an odor as the cue that is

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learned, the odor may be produced by a number of chemical components found in varying proportions in different individuals. In discrimination by direct familiarization, we can expect the discriminator to respond to the target as kin only if all essential components (including proportions of the different chemicals — the ‘chemical profile’) of the target odor match that of the learned odor. For all practical purposes, this is equivalent to individual discrimination and no specialized kin discrimination mechanism sensu stricto is necessary. In discrimination by indirect familiarization, the discriminator may also rely on an exact match of components in the family-specific odor, or it may rely on the relative similarity of shared components between the target odor and the learned family odor. The latter situation could result in proportional discrimination. Fig. 1 illustrates how discrete and proportional discrimination may occur when complex cues are employed. In the case of odors, Heth and Todrank (2000) have suggested that ‘‘odor-genes covariance’’ (i.e., the similarity between the odors of any two individuals directly reflects the genetic similarity between them), coupled with self-reference (matching to self), would result in behavioral responses that support such a ‘goodness of fit’ model. The key point here is that the ability to discriminate among different categories of kin does not

mean that the neural mechanisms mediating discrimination are genetically-based or have an innate component. Complex cues, odor-genes covariance, learning, and the generalization of the learned cues (based on the degree of similarity among cues) are all that is needed in order to generate a pattern of kin-directed behavior that correlates with the degree of genetic relatedness between the discriminator and the targets.

5. Are recognition alleles a mechanism for kin discrimination? Recognition alleles is probably the most problematic of all the proposed kin recognition mechanisms. According to this hypothesis, the same gene, or set of genes, will: (1) code for the expression of a phenotypic marker or label; (2) code for the recognition of the same phenotypic marker or label in others; and (3) cause preferential behaviors to be directed towards other individuals carrying the same allele(s). Based on the definitions presented earlier, this is the only mechanism that would meet the requirements of a genuine kin recognition mechanism. Each of the elements of the recognition alleles hypothesis, and the problems inherent in their formulation, will now be considered in turn.

Fig. 1. Schematic diagram of discrimination models. Upper circle in each case represents the ‘template’. Lower circles represent the phenotype of the target. ‘ +’ means that discrimination occurs; ‘ − ’ means that discrimination does not occur. Strength of discrimination responses are indicated by the number of + signs. (A) Only individuals whose phenotype is identical to the template are discriminated. (B) Only individuals that share many characteristics with the template are discriminated. (C) The strength of the discriminatory response depends on the relative similarity of target phenotype to template.

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The first element predicts that the markers used for kin discrimination will be genetically-based. A substantial body of data has shown that, in some cases, the cues used for kin discrimination have a genetic basis (e.g., the MHC system in mice), but that in others they are environmentally acquired; moreover, genetic and environmental factors may interact in complex ways (reviewed by Halpin, 1991; also Yamazaki et al., 1980; Hepper, 1987a). However, it is not the ontogenetic origin of the cues that determines the kin discrimination mechanisms that are used. Therefore, the fact that some cues used for kin discrimination have a genetic basis does not address the other, more critical predictions of the recognition alleles hypothesis. In other words, even when cues have a genetic origin, kin discrimination may involve learning, as in direct and indirect familiarization. Knowing that cues used for kin discrimination may have a genetic basis does not provide information on how such cues are processed in the nervous system; thus, knowledge of the ontogenetic origin of cues contributes little to our ability to distinguish among the various kin discrimination mechanisms. The second element of the recognition alleles hypothesis — that genes code for recognition — says nothing about what this coding entails or about the proximate mechanisms by which recognition actually occurs. Although this element implies a neural process that classifies conspecifics according to kinship (e.g., see discussion of Hepper’s, 1991 ‘‘kinship center’’ below), at present there is no information on how the hypothetical allele translates to a classification mechanism or a neural process for recognition. Thus, this aspect of the hypothesis describes that kin-related cues will be ‘recognized’ and categorized based on kinship but does not explain the mechanism by which this categorization will be accomplished or even where in the nervous system we might expect such recognition to be processed. The third element of the hypothesis presents a similar problem. The behavioral outcome is described — preferential behavior toward kin — but there is no explanation of the proximate mechanisms for this outcome. What neural processes are involved in the decision to behave

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differentially toward kin as compared to non-kin? The existence of neural centers that would recognize kin and regulate appropriate behaviors based on degree of kinship have been hypothesized (Hepper, 1991) but never demonstrated. The lack of information on the biological and neural processes hypothesized by these last two elements of the recognition alleles hypothesis cannot, by itself, be considered a fatal flaw because so little is known about brain function and the ways in which genes affect cognitive processes and behaviors. It is theoretically possible that neural processing akin to that suggested by Hepper occurs without the involvement of a particular neural center. Similarly, the existence of genes that mediate kin recognition and preferential behaviors is hypothetically possible. For example, in some species the learning of socially relevant cues may be influenced by genes (e.g., ‘‘immediate early genes’’ — IEGs — in the case of mouse pheromones; see Brennan and Keverne, 1997). Genes also have been shown to control song production and mate preferences in crickets (Hoy et al., 1977), and there is indirect evidence in some taxa that species recognition may be under genetic control (e.g., in some species of ducks: Williams, 1983; in avian brood parasites). Additionally, recent studies on mice, rats and humans also suggest that, in some situations, an individual’s MHC type may strongly influence its mate preferences; nonetheless, the exact mechanims of MHC-based preferences are not well understood and it is clear that learning plays an important role (Penn and Potts, 1998; Arcaro and Eklund, 1999; Tregenza and Weddel, 2000). Likewise, the t-complex in mice affects mate preferences but early experience can modify these effects (Lenington, 1991; Lenington and Egid, 1989). Although interesting, these examples all involve species recognition and/ or mate preferences, processes that may or may not be similar to kin discrimination. Moreover, the nature of species recognition mechanisms is still being debated. For example, Paterson (1993)’s ‘‘recognition concept of species’’ suggests that species recognition is itself only a by-product of genetic changes that accumulate as a result of geographic isolation and adaptation to a new habitat during speciation, and that there is no

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direct selection for species isolating mechanisms or for species recognition. Heth and Todrank (2000) suggest that mate recognition in rodents could be a result of odor-genes covariance, with animals comparing the phenotype of the potential mate to their own and showing a preference for those individuals with odors that are more like their own as compared to those of other species or subspecies — a process comparable to ‘phenotype matching’ to self at the species level. Although genetic variation is important in both of these formulations, neither relies on genetically controlled recognition processes. Thus, the existing evidence and theory on the mechanisms animals use to select mates, whether from their own species or from within their own population, is still being debated, may vary from species to species, and cannot be used to unequivocally support or refute the recognition alleles hypothesis. It also could be argued that all learning processes have been shaped by evolution and, therefore, have a genetic foundation. This likely is true in a general sense if we consider biological constraints on learning. However, with a few exceptions (e.g., Hoy et al., 1977) there is scant evidence that the neural process of recognition per se, whether of kin or other socially relevant conspecifics, is under direct genetic influence. Similarly, no one has yet provided any evidence for the existence of genes mediating kin recognition in any vertebrate species, despite an enormous body of literature on the mechanisms of kin discrimination and recognition. Although the failure to identify such genes does not prove that recognition alleles do not exist, it does counsel substantial caution in accepting the hypothesis. In summary, since the recognition alleles hypothesis was first proposed, there has been no direct evidence generated that clearly supports it. Moreover, no adequate predictions have been made that would allow one to distinguish between this and other more parsimonious hypotheses. Holmes and Sherman (1983) stated that recognition alleles are ‘‘unlikely’’, ‘‘improbable’’, and that ‘‘...an empirical search for recognition alleles would be difficult at best, because their existence could be inferred only after systematically eliminating all environmental and experiential cues,

including a subject’s experience with its own phenotype’’. Almost twenty years and hundreds of publications later, no new information has been reported that would require a reassessment and additional problems have been identified (see Komdeur and Hatchwell, 1999). There is, however, a possible test of the hypothesis. In a previous section I suggest that indirect familiarization (‘phenotype matching’), with self as the referent, should not occur in animals that rely on vision and have no means of inspecting their own visual characteristics. Finding a species that uses both visual cues and self-reference for kin discrimination, has no means of inspecting its own relevant phenotype, and does not associate with genetic relatives during early life, would very strongly support a genetically-based recognition process. In addition, more research involving appropriate genetic tests, and/or elucidating the details of genetic-neural interactions responsible for kin discrimination, would be necessary to determine unequivocally whether the recognition alleles hypothesis is valid and whether a geneticallybased, specialized mechanism of kin recognition has evolved. At present, however, the lack of direct supporting evidence, the intractability of the hypothesis to rigorous empirical testing (but see Table 1), and the existence of more parsimonious hypotheses, suggest that the recognition alleles hypothesis should not be considered a high-priority contender for a kin recognition mechanism.

6. Are there specialized kin recognition neural systems? There are two markedly different viewpoints on the evolution of kin discrimination mechanisms. One viewpoint is represented by Hepper (1991, p. 281): Hamilton’s kinship theory…gives clear reasons why responding differentially to kin and nonkin is advantageous to fitness and it would thus be expected that a means to enable the recognition of kin would evolve.

4. Recognition alleles

3. Self recognition with refined discrimination

2. Group/species recognition with refined discrimination

(b) Generalization

1. Individual recognition (a) Exact match

Hypothesis

Test

Expose discriminator to amicable conspecific (whether kin or non-kin) labeled with artificial cue (e.g., odor). Test with unfamiliar conspecific labeled with the same cue. Responses should be same as to the familiar conspecific. Discriminator responds positively to siblings of familiar, Expose discriminator to amicable conspecific amicable individuals regardless of whether these (whether kin or non-kin) labeled with artificial individuals are kin or non-kin. cue. Modify label cue gradually when presenting unfamiliar targets. Discriminator should respond based on similarity of modified cue to original cue. Responses are proportional to similarity of target cue Expose discriminator to group of amicable to the learned group or species cue. conspecifics (kin or non-kin) labeled with artificial cue. Discriminator is not labeled with same cue. Test with targets labeled with modified cues. Responses should be proportional to similarity of modified cue to original one. Responses are proportional to similarity of target cue Label discriminator with artificial cue but do not to own self cue. label other conspecifics in group with same cue. Test with targets labeled with modified cues. Responses should be proportional to similarity of modified cues to the original self cue. Other cues, similar to ones used to label the other conspecifics in the group, should not elicit positive responses. All positive responses will be directed at kin. Under no Exposure to artificial cues (labels) will not result circumstances will discriminator responses be positive in positive responses by discriminator. If toward non-kin. artificial cue blocks perception of natural phenotype, discriminator will show neutral or negative responses to kin and non-kin alike. If artificial cue does not block perception of the natural phenotype, then discriminator will show positive responses toward kin, but negative or neutral responses toward non-kin. Labeling should begin immediately after birth or hatching to hinder exposure to self phenotype.

Responses are based on previous experiences with target phenotypes regardless of targets’ relatedness to discriminator. Responses to familiar, amicable non-kin are similar to those toward kin.

Predicted discriminator response

Table 1 Predicted discriminator responses and possible tests for hypotheses presented in the text, as compared to the recognition alleles hypothesis. See Section 6 for additional details and explanations

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Hepper (1991, p. 264) also proposes a model for a ‘kinship center’, apparently, a neural center that determines exact degrees of relatedness between discriminator and target (a sort of meter for the coefficient of relatedness, ‘r’) and that assesses decision rules to determine the appropriate behavior that the discriminator should show toward the target. Thus, this hypothetical kinship center would represent a specialized mechanism that evolved for the specific function of directly processing kinship and determining the appropriate behaviors that should be directed toward conspecifics of different degrees of relatedness. A radically different perspective has been articulated by Grafen (1990, p. 42). He asserts that even when we observe examples of kin discrimination: …we cannot then conclude that individuals of this species have evolved to distinguish kin from non-kin, we cannot conclude that possession of the ability has anything to do with kin selection, and we should not presume that this ability to discriminate has an evolutionary function at all…an ability to discriminate by genetic similarity can easily arise as an incidental byproduct of either species recognition, or individual or group member recognition. Subsequently, Barnard et al. (1991) supported this position. In short, while Hepper (1991) believes that the benefits conferred by kin selection gave rise to specialized kin recognition systems, Grafen (1990) and Barnard et al. (1991) argue that there is no evidence for a specialized mechanism, that kin selection may not be relevant in this case (but see Pfenning et al., 1999 for an opposing opinion), and that what is referred to as ‘kin recognition’ may, in reality, be nothing more than an extension of individual or species recognition. One way of examining these two different hypotheses is to look at the neural mechanisms involved in the ability to discriminate between kin and non-kin. The existence of specialized neural pathways or brain centers is not an absolute requirement for genuine kin recognition, but evidence of a specialized kin recognition center, or of

unique or specific neural processing of kin recognition cues (i.e., differing from the processing of other cues unrelated to kinship), would provide strong support to Hepper’s view that a specialized kin recognition mechanisms has evolved. On the other hand, a failure to find such evidence would lend support to Grafen’s perspective. In that case, one would expect cues correlated with kinship to be processed in the same manner as other cues in the same modality and that kin discrimination could be explained by invoking nothing more than the conventional ability of the nervous system to habituate, generalize or discriminate on the basis of learned stimuli. I have recently examined the literature on vertebrate neural pathways for kin discrimination and for other forms of social recognition (e.g., individual discrimination, species discrimination, mate discrimination) in the case of one sensory modality: olfaction (Tang-Martinez, 1998; see also Gheusi et al., 1994; Kendrick, 1994; Brennan and Keverne, 1997). Olfactory cues relevant to reproductive functions and sexual behavior are mediated primarily through the accessory olfactory system (the vomeronasal system) but, for the most part, all other odors, including most cues relevant to kin discrimination and to all other forms of social recognition are mediated through the exact same pathways of the main olfactory system. This is true regardless of whether the relevant odors are genetically-specified, environmentally-acquired under natural circumstances, or artificially-acquired (e.g., perfumes or other artificial odors that become associated with conspecifics). There are also no differences in neuropharmacology when vertebrates process kin odors as compared to other odors used in social recognition. Certain hormones (e.g., vasopressin, noradrenaline, acetylcholine, oxytocin) are known to play a role in social learning and memory but there does not appear to be a difference in the endocrine substrates for learning kin-relevant odors as compared to other social recognition odors. A quick survey of other modalities (e.g., visual, auditory) revealed a similar pattern and also failed to provide evidence of specialized pathways or physiological processes.

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Developmental studies can also provide insights into the evolution of kin recognition mechanism. In several species, the neonatal central nervous system has evolved to be particularly sensitive to learning cues that are later used to discriminate kin from non-kin. For example, in some species there are imprinting or imprinting-like processes that result in the learning of relevant cues during certain stages in ontogeny. Filial imprinting, using visual cues, is well known among precocial birds and some baby birds learn their mother’s calls prior to hatching. Although young birds use these cues to discriminate between their own mother and other conspecifics, the cues that are learned appear to be individually distinctive (Johnson and Horn, 1987; Johnson, 1991). Parental discrimination as a result of imprinting may, thus, represent an extension of individual recognition (species characteristics may also be learned as a consequence of learning these individual cues). The processes that result in filial imprinting differ from the usual pattern of learning individuallydistinctive cues only because there is a predisposition to learn these cues during a particular stage of ontogeny. Learning such individually-distinctive cues is undeniably important in the subsequent ability to distinguish between relatives and non-relatives and genes may well affect the timing of learning, making it more likely that the learned cues will be those of kin. Although this suggests that developmental mechanisms facilitating learning of kin relevant cues have been favored during evolution, this does not necessarily mean that these mechanisms evolved specifically for the purpose of kin discrimination per se, nor that brain centers and neural processes specialized for the recognition of kin actually exist. Moreover, there appears to be no predisposition to learn kin cues as compared to cues associated with other conspecifics, or even other conspicuous environmental cues, as is evidenced by cases of inappropriate imprinting to heterospecifics and inanimate objects by birds. Thus, imprinting may have evolved, not to insure kin recognition per se, but rather to increase the probability that young precocial birds would be most attracted to objects that are familiar and likely to offer them protection. The ability to recognize parents as individuals may have been

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under direct selection, while the ability to discriminate kin from non-kin may be a by-product. There is also no evidence that the learning and processing of cues relevant to imprinting rely on specialized, kin-specific, neurobiological mechanisms. In neonatal chickens, the IMHV (the intermediate and medial areas of the hyperstriatium ventrale) is critical for recognition of individual conspecifics regardless of their relationship or the social context (Bolhuis et al., 1989; Johnson, 1991). Thus, although the IMHV is necessary for filial imprinting, it is also necessary for other social preferences that depend on individual recognition. Therefore, the IMHV does not represent a specialized neural mechanism for recognizing kin. A function similar to that of the IMHV in chickens has not been demonstrated in any other vertebrate species. Among rodents, neonatal learning of cues associated with the mother are also important for kin discrimination. Baby rats, Rattus nor6egicus (Leon, 1975), and spiny mice, Acomys cahirinus (Porter and Doane, 1977), are preferentially attracted to maternal odors influenced by their mother’s diet. Under natural conditions they probably use these odors to orient to their mothers, but they cannot discriminate between their own mother and another lactating female that is on the same diet as the mother. Thus, these odors are associated with maternal diet and do not seem to function as markers of genetic relatedness per se. Rat pups also orient to artificial odors daubed on the mother or nestmates (Hepper, 1987b). Not all sensitive periods for learning kin-related odors occur in neonatal animals. Female goats, Capra hircus (e.g. Klopfer and Gamble, 1966), and sheep, O6is aries (Poindron and Levy, 1990; Kendrick et al., 1992), appear to be predisposed to learn the odors of their newborn offspring immediately after giving birth. However, Gubernick (1981) has suggested that female goats label their young with maternal saliva following parturition and then use this label to ‘recognize’ their offspring. Thus, the odors that are learned are likely to be individually-distinctive and it is well known that mothers can be deceived into accepting alien young (non-kin) as long as they are introduced immediately after parturition (Levy et

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al., 1991). The sensitive period for learning the odors associated with own young appears to be triggered by hormonal changes and mechanical stimulation of the cervix and vagina during birth, but there is no evidence of specialized ‘kinship centers’ for learning and responding to kin odors as compared to other social odors (Brennan and Keverne, 1997). In summary, there is no evidence of a specialized kin recognition mechanism or of anything that approximates a ‘kinship center’ that assesses degrees of relatedness and controls behaviors directed toward kin. This does not mean that a ‘kinship center’ does not exist; our knowledge of cognitive neural processes and pathways is still wanting. However, if such a center does exist, no evidence of its existence has yet been found.

7. General conclusions and alternative mechanisms The prevailing categorization of kin discrimination mechanisms into ‘recognition by association’ and ‘recognition by phenotype matching’ has impeded our understanding of the basic processes by which animals distinguish between kin and nonkin. In both cases the fundamental mechanism that leads to kin discrimination is the learning of cues that may be either individually-distinctive (direct familiarization) or shared by members of a family (indirect familiarization). The primary difference between the two processes is the cues that are learned. Moreover, an individual can learn both individually-distinctive and family-specific cues, allowing it to discriminate both known kin and unfamiliar kin respectively, depending on the context of an interaction. I propose that ‘spatial recognition’ be dropped from our categorization of kin discrimination mechanisms. In most, if not all, cases involving vertebrates, what has been called spatial recognition is probably ‘ancillary kin bias’. If anything, it could be argued that animals in this situation do not recognize kin and, consequently, cannot discriminate between kin and non-kin encountered in a given locality. The concept of recognition alleles is challenged because it only describes expected results but has

little explanatory power. Most importantly, after 35 years of intense research on kin discrimination and recognition, there has been no empirical demonstration that recognition alleles exist (see also Hepper, 1991). Although theoretical models (e.g., Hepper, 1986; Crozier, 1987) are interesting and alert us to the range of possibilities, they are not a substitute for convincing empirical evidence. The ability of animals to discriminate between kin and non-kin can best be understood as an extension of individual, species, and/or group recognition, an idea consistent with those of Waldman (1987), Grafen (1990), and Barnard et al. (1991). Based on the evidence, there is no need to invoke the evolution of special mechanisms and traits for kin discrimination. Instead, traits that have evolved for other reasons and in other contexts have been co-opted for their current use in kin discrimination. Thus, kin discrimination may be an epiphenomenon of learning processes involved in individual, species, or group recognition. If the premise that there are no recognition genes and no specialized system has evolved to enable the recognition of kin is correct, then how is it that animals are able to discriminate behaviorally between kin and non-kin? Several models (summarized in Table 1), all of which rely on familiarization and on general characteristics of learning such as habituation, generalization, and discrimination, are possible:

7.1. Animals learn indi6idual phenotypes as a consequence of association with certain conspecifics The learned phenotypes are stored as ‘templates’ and compared to those of newly encountered targets. The phenotype of the target may be (a) identical to the template; (b) somewhat similar but not identical to the template; or (c) very or totally different from the template. In the first case, the discriminator may respond positively (i.e., with approach and/or amicable behaviors) to the target as a result of previous, positive experiences with the target. Such behaviors would be expected any time the discriminator meets a conspecific with which it previously has

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had positive interactions, regardless of whether the conspecific is a genetic relative or not. Previous negative experiences should result in negative behaviors (e.g., avoidance, aggression). This prediction can be tested by comparing the responses of discriminators to non-kin with whom they have had positive interactions, to the responses shown to kin. Cross-fostering studies in which individuals behave similarly to true kin with whom they grew up and to foster kin provide such evidence. Moreover, unpublished results from my laboratory demonstrate that rodents behave toward known kin in much the same way as they do to familiar but unrelated, adult individuals with whom they have not had negative encounters. In fact, in several species of rodents and other mammals (see references in Bekoff, 1981), one of the best ways to reduce aggression and increase amicable behaviors between unrelated individuals is to provide the animals with a period of limited familiarization (e.g., separated by a screen barrier) prior to housing them together. With regard to both kin and non-kin, these responses would be the result of individual recognition; in terms of kin discrimination mechanisms, the responses to kin could be perceived as discrimination by association or by direct familiarization. In the second case, when there is an imperfect match between template and target phenotype, the discriminator may generalize the learned individual template(s) to targets with similar, albeit not exact, phenotypes. In this case, the responses shown by the discriminator should be similar to those shown in the previous situation, but would be due to ‘erroneous’ individual discrimination. Because of the similarities, the discriminator reacts to the target as if it were the individual it previously has encountered and interacted with. From the perspective of kin discrimination this would be equivalent to discrimination by indirect familiarization (‘phenotype matching’). In the third case, when there is little or no match between template and the phenotype of the target, the discriminator would be expected to show either neutral behaviors to the target, or agonistic behaviors depending on the social system of the species. The behavior of the discriminator may not reflect any assessment of

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relatedness or degree of kinship but rather may be the default condition due to a lack of familiarity.

7.2. Animals learn group or species-rele6ant cues as a result of association with certain conspecifics The phenotypes of associates (most commonly nestmates) are stored as templates that provide information on the species or the group. Refined discrimination of targets with phenotypes most similar to the template results in differential behaviors toward the target. Thus, instead of generalizing from individually-specific stimuli, the animal discriminates from a broader stimulus to classify unfamiliar individuals as members of the ‘group’. When the group happens to be the family, the discriminator compares the learned family phenotype to the target’s and, if the target resembles family, it is treated as if it were a familiar individual. Behavior is adjusted based on the perceived similarity between target and group phenotypes. Consequently, targets that more closely resemble the group cue will be perceived as more similar, and therefore more familiar, than would targets whose phenotypes have less resemblance to the template phenotype. The behavioral results will be equivalent to those expected from proportional recognition by phenotype matching. Responses are not due to assessment of genetic relatedness per se, but rather to familiarity with certain cues, combined with sensory discrimination.

7.3. Animals learn cues from self The cognitive process is exactly the same as that in the previous example. However, in this case the discriminator compares the phenotype of the target with its own phenotype (a familiar cue) rather than a group phenotype. Depending on the degree of similarity or difference between self and target phenotypes, it behaves toward the target as a familiar or unfamiliar individual. The results, as in the previous example, would represent proportional phenotype matching. As noted previously, since the discriminator always has access to its own phenotype, short-term or procedural memory, allowing for immediate comparisons, will be sufficient for discrimination to occur.

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The effects of familiarity are critical. In all three models, the learned template depends on the discriminator’s familiarity with conspecific (or self) phenotypes. Moreover, in the last two models, when there is a correlation between the similarity of the cues being used and the genetic relatedness of discriminator and target, the behavioral responses mimic kin discrimination by indirect familiarization (phenotype matching). In reality, however, the behavior is shaped by familiarity rather than by genetic relatedness. Since relatives are more genetically similar and, consequently, also likely to have more similar phenotypic cues, it is easy to misinterpret responses due to familiarity as responses due to kin recognition. Thus, the mechanism for the response may be misunderstood, resulting in erroneous assumptions about the evolution of kin discrimination. The behavioral effects of familiarity may be mediated by habituation or dishabituation. When an animal responds differently to those phenotypes that are most similar to self or to nestmates, it may do so as a result of habituation to familiar cues. Habituation could result in an attenuated response (e.g., less agonism) due to lower levels of excitation when a familiar cue is encountered. On the other hand, exposure to a very different (unfamiliar) cue could cause dishabituation and/or increased sensory and neural excitation, yielding a quantitatively and qualitatively different response, perhaps including increased investigation and agonism. These models are hypotheses that may explain how kin discrimination can occur without the existence of neural systems specialized for recognizing kin. Hypotheses, however, are by their very nature speculative. Careful testing of these hypotheses should contribute to a better understanding of the mechanisms by which animals discriminate behaviorally between kin and nonkin. I emphasize that I am not saying that kin discrimination and kin bias do not exist. Moreover, under certain circumstances, kin discrimination and even ancillary kin bias could result in an increase in the inclusive fitness of the discriminator. Yet even this statement is an assumption based primarily on theoretical considerations. There are significant caveats. First, there is a

paucity of rigorous, empirical demonstrations of the fitness consequences of kin discrimination (Sherman et al., 1997; Komdeur and Hatchwell, 1999). Second, serious misconceptions about the meaning and calculations of inclusive fitness have plagued most studies on this topic (Dawkins, 1986; Armitage, 1989). Third, the importance of the indirect component of inclusive fitness (the component that is relevant when one considers the fitness consequences of preferential behaviors directed at kin) may have been overly emphasized. Thus, Armitage (1989) states that in most instances kin discrimination may ‘‘function primarily to increase direct fitness, with indirect fitness a minor component of total fitness and important primarily where the association with other individuals is necessary in order to maximize direct fitness’’. Such admonitions suggest caution in accepting axiomatic formulations that automatically link kin discrimination to kin selection and increases in inclusive fitness (e.g., Komdeur and Hatchwell, 1999). From an adaptationist perspective it could be argued that if there is any increase in inclusive fitness, this is all that matters. However, this ignores the even more fundamental question of the evolutionary origins of the behavior: What are the behavioral antecedents and selective forces that have favored the ability of animals to discriminate behaviorally between kin and non-kin? Selection for processes such as individual recognition, species recognition, group recognition, habituation, and associative learning can easily explain the ability of animals to discriminate between kin and non-kin without a need to invoke kin selection. Kin discrimination may be a byproduct or consequence of these other, more generalized, recognition processes and abilities of peripheral and central vertebrate nervous systems. Nonetheless, even if kin discrimination arose as an epiphenomenon of other selective forces, it could have been secondarily favored if it conferred an advantage in terms of inclusive fitness. Such selection may have further strengthened certain learning processes, constrained the cues that are likely to be learned, and affected the timing of learning so that it facilitates learned associations of cues correlated with kinship. But, even if this is

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the case, it is not necessary to invoke kin selection as the driving force in the evolution of kin discrimination and the caveats mentioned above still apply. Evolutionary processes do not evolve de novo. Pre-existing cognitive processes, such as associative learning, habituation, discrimination, and generalization, likely gave rise to kin discrimination as an extension of individual and/or species recognition. Individual and species recognition may then have been exapted (sensu Gould and Vrba, 1982) for kin discrimination. The role of kin selection, if any, may well have been limited to refining and reinforcing some of these pre-existing processes. In conclusion, I acknowledged that the controversial issues addressed in this paper have a philosophical underpinning. The fundamental question is: How does natural selection operate and how do we know that a particular trait has been selected for (i.e., that it is an ‘adaptation’ directly acted upon by natural selection because it increases survival and reproductive success)? It is not enough to assume that because a trait exists and can be shown to be beneficial, then it must be the result of natural selection acting directly on that trait. Beneficial traits may come about as corollary by-products, effects, or consequences of other traits that are under direct selection. This point has been repeatedly emphasized by both philosophers of science and evolutionary biologists. For example, Sober (1984) distinguishes between ‘selection for’ and ‘selection of’. He provides an illuminating analogy involving marbles of different sizes and colors, with all the smaller marbles being green; if all marbles are subjected to a filter that only allows the smallest marbles to pass, all the marbles that make it through will be green. The fact that these marbles are green is a by-product of selection for size. In Sober’s terminology, size was ‘selected for’ (an adaptation), while green is the result of ‘selection of’ (a consequence, side effect, or epiphenomenon). Similarly, Williams (1966), a champion of natural selection, understood that benefit does not imply direct selection for a trait, and differentiated clearly between effects or consequences and adaptations. He writes: ‘‘A frequent practice is to recognize adaptation in any recog-

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nizable benefit arising from the activities of an organism. I believe this is an insufficient basis for postulating adaptation and that it has led to some serious errors. A benefit can be the result of chance instead of design’’. (p. 12); ‘‘One should never imply that an effect is a function unless he can show that it is produced by design and not by happenstance. The mere fact of the effect’s being beneficial from one or another point of view should not be taken as evidence of adaptation’’. (Williams, 1966, p. 261). Thus, an insistence on distinguishing between effects and adaptations, and a reluctance to assume that any beneficial trait must have been directly selected, does not imply a lack of appreciation for, or belittling of, the power of natural selection. On the contrary, only by rigorously dissecting the evolutionary processes responsible for mechanisms, and clearly distinguishing between adaptations and effects, can we hope to develop a more complete understanding of behavioral evolution. It is my hope that this critique will contribute to that understanding.

Acknowledgements I am grateful for support from the National Science Foundation (RII-9003041 and IBN 9728767). Informal conversations and discussions with many colleagues, including the late William J. Bell, and also George T. Taylor, Rudolf Jander, Josephine Todrank, Giora Heth, Wendy Sera, John Kaprowski, Stanton Braude, Guillermo Paz y Min˜o C., Karen Koeninger Ryan, Klaus Jaffe´, Allan Larson and Manuel Leal alerted me to relevant references and/or aided the development of these ideas. However, my acknowledgement does not imply that they agree with all of my critiques or conclusions. Stanton Braude, Manuel Leal, Andrea Bixler, Josephine Todrank, Giora Heth, and Arlene Zarembka made particularly valuable suggestions on the manuscript. I am also grateful to Marc Bekoff and an anonymous reviewer for constructive criticisms of the submitted manuscript. David Chisholm did the drawings for the figure.

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