In the absence of adult conspecifics, newly-hatched chicks will approach a wide range of bright or moving objects. After a period of exposure to such an object they form a social attachment to it. When they are close to the object the chicks emit soft calls, and if it moves away they will follow it. If subsequently exposed to a new object the chicks will run away emitting distress calls. From these observations it may be inferred that chicks learn about some of the visual characteristics of the first object to which they are exposed. This process is referred to as filial imprinting, and has been studied most intensively in precocial birds such as domestic chicks, ducklings, and goslings (Spalding, 1873; Heinroth, 1911; Lorenz, 1935, 1937; Bateson, 1966). Similar processes may also occur in mammals, but evidence for this is harder to obtain due to their comparative lack of mobility shortly after birth. This chapter will concentrate on the neural and behavioural analysis of filial imprinting in the domestic chick, a species which readily imprints on to a wide range of visual objects.

Imprinting can be reliably reproduced in the laboratory in the following way. Chicks are dark-reared until being exposed to a conspicuous object such as a rotating, illuminated red box, for a period of time, normally several hours. From between two hours to several days later, chicks are given a choice between the object to which they were exposed and a novel object. The extent to which the chick approaches each of the two objects is compared and a preference score calculated.

Since Hamilton's oft-cited prediction regarding the unequal distribution of behaviour among genetically related (kin) and unrelated conspecifics (nonkin) (Hamilton, 1964), the phenomenon of kin recognition has been repeatedly documented among a diverse assortment of animal species (Colgan, 1983; Fletcher & Michener, 1987; this volume). As in other maturing fields of inquiry, attention has shifted from description and documentation of recognition systems to a search for the ‘mechanisms’ supporting kin recognition. This search has produced a canonical list that typically comprises four classes of mechanisms: (1) spatial distribution, (2) familiarity, (3) phenotype matching, and (4) recognition alleles. These hypotheses have been offered as explanations of the dynamic control of recognition, but generally contain reference to the developmental means by which recognition cues come to exert their effects (Hepper, 1986; Fletcher, 1987). Thus, the ontogeny of kin recognition has, explicitly or implicitly, become one of the central foci of debate in this relatively young field.

In nature, among species bearing multiple offspring in a single clutch or litter (including most mammals), a necessary concomitant to reproduction is the association of mother with offspring and of littermate siblings with one another. Therefore, some degree of prior experience with related conspecifics is virtually inevitable. A common experimental design intended to isolate effects of prior experience involves cross-fostering of some offspring to unrelated litters shortly after birth. However, even if performed within moments of birth, cross-fostering cannot separate genetic factors from experiences of siblings that share the same prenatal environment (cf. Ressler, 1962).

Co-operation can be defined as any mutually beneficial interaction between two or more individuals. By this standard definition, many, probably most, birds and mammals exhibit co-operation in one or more contexts. Cooperation can range from a simple apparently incidental group effect, such as the simultaneous mobbing of an owl by individuals of two species of songbirds, to complex mutual dependence, such as the rotating sentinel systems of some group-living animals (e.g. McGowan, 1987). Virtually all researchers recognize co-operation when they see it and its widespread occurrence is not a matter of controversy (Axelrod & Hamilton, 1981).

The phenomenon of co-operative behaviour is a fascinating one, for several reasons. First, co-operation is a universal human trait and the vast majority of interactions among individual humans are co-operative to a greater or lesser degree. Thus, it is easy for people to empathize with the cooperative behaviours they observe in animals.

Second, highly developed intra-group co-operation is often seen in species also characterized by high levels of inter-group competition. Our own species is the prime example of this relationship. Killing of conspecifics may be viewed as indicative of extreme intraspecific competition, and human warfare, the searching out and killing of male chimpanzees (Pan troglodytes) by groups of males (Goodall, 1986), the expulsion or killing of male prideholding lions, (Panthera leo) by invading coalitions of males (e.g. Packer & Pusey, 1982) and the running down and killing of a lone wolf (Canis lupis) by a pack (Mech, 1970), illustrate this relationship between co-operation and competition.

Introduction

Kinship underlies many facets of vertebrate sociality. Yet vertebrate societies rarely consist exclusively of kin. Typically, individuals interact both with kin and non-kin in numerous and often unpredictable contexts. Clear advantages accrue to those individuals that discriminate behaviourally among conspecifics based on their genetic relatedness. The ability to recognize relatives permits individuals (1) to favour their kin, thereby enhancing their inclusive fitness (Hamilton, 1964; Grafen, 1985), and (2) to avoid incest or even to choose an optimally related mate (Shields, 1982; Bateson, 1983), potentially increasing their own reproductive success. Possible benefits of kin discrimination are easily enumerated in birds and mammals (reviewed in Waldman, 1988), so their kin recognition abilities (e.g. Holmes & Sherman, 1982; Hepper, 1983; Beecher, 1988) should not be surprising. Less is known about the social life of fishes, amphibians, and reptiles, but they also may recognize their kin. Some fishes and larval amphibians, for example, recognize their siblings and preferentially school with them (e.g. Waldman, 1982b; O'Hara & Blaustein, 1985; Quinn & Busack, 1985; Van Havre & FitzGerald, 1988; Olsen, 1989). Similarly, iguana hatchlings associate in social groups with their siblings rather than with unrelated individuals (Werner et ah, 1987).

Mechanisms of kin recognition have been more thoroughly examined in amphibians than in other vertebrates. Indeed, information on the ontogeny and sensory bases of kin recognition comparable in detail to that known about social insects (e.g. Gamboa et aL, 1986; Hölldobler & Carlin, 1987; Michener & Smith, 1987) and some invertebrates (Linsenmair, 1987) is currently available only for larval amphibians. Warm-blooded vertebrates can be unwieldy as subjects for ontogenetic studies in the laboratory.

In practice, although not in theory, the subject of this chapter – the genetic determination of body scents that distinguish one individual from another individual of the same mammalian species – is fairly new. Systematic work on this topic was made possible by certain incidental observations made by animal technicians responsible for deriving and maintaining congenic mouse strains in a special facility for that purpose at Sloan Kettering Institute, in New York, USA.

Studies on the major histocompatibility complex (MHC)

In general, mice of an inbred strain are genetically identical to one another. Mice of an inbred congenic strain are likewise identical with one another and differ from a selected standard inbred strain only in the vicinity of a particular gene or gene complex. This discrete genetic difference between a pair of congenic strains, meaning a standard inbred strain and its congenic companion strain, is achieved by crossing two inbred strains and then serially back-crossing to the selected inbred parental strain for many generations with selection for an allelic genetic trait of interest, derived from the opposite parental strain, in each generation. Any difference that distinguishes a pair of congenic strains, provided that this is shown to be genetic by appropriate segregation tests, must be due to the selected gene or a gene in that vicinity, i.e. within the small segment of donor chromosome carried over together with the selected gene (Boyse, 1977; Foster et ai, 1981).

Introduction

Much evidence has now accumulated to demonstrate that individuals respond differentially to conspecifics according to their genetic relatedness (e.g. Hepper, 1986a; Fletcher & Michener, 1987; see also this book). Furthermore, this differential responding is not confined to one particular behaviour but is found in a diverse variety of situations and behaviours (see this book). This strongly suggests that individuals have some means which enable them to identify genetic relatedness. It is the aim of this chapter to explore how individuals recognize their kin. Previously (e.g. Hepper, 1986a; Porter, 1987; Waldman, 1988) this ability has been considered under the general rubric of the ‘mechanisms’ of kin recognition. This chapter will discuss factors which contribute to the individual recognizing its kin and will, by addressing these factors, enable the underlying basis of kin recognition to be elucidated. Although the chapter will concentrate on mammalian kin recognition it is hoped that the considerations presented will be applicable to other animal groups. I shall first discuss present approaches to mechanisms of kin recognition.

In Hamilton's seminal papers of 1964 (a,b), as well as demonstrating the fitness benefits to an individual of responding differentially to kin and nonkin, a number of ways were proposed by which individuals would be able to discriminate between kin and non-kin in social situations. From this discussion (Hamilton, 1964b) and that of others (e.g. Alexander, 1979; Bekoff, 1981; Hölldobler & Michener, 1980) four basic ‘mechanisms’ have been proposed to explain how individuals recognize their kin (Holmes & Sherman, 1983). These have become firmly rooted in the literature and I shall outline each briefly.

Parental care is one form of parental investment and investing in one young detracts from the ability of a parent to invest in others (Trivers, 1974). Parents are thus expected to allocate investment to one young until the cost of giving that care exceeds the benefit in terms of survival of the infant or, more correctly, in terms of survival of the half set of genes a diploid organism passes on to its sexually produced offspring. Each parent should attempt to maximize its production of viable offspring, that is by judicious allocation of resources it should attempt to maximize its genetic contribution to the next generation. Investment in unrelated young, however, will detract from the ability of an animal to produce its own offspring and hence will lead to a reduction in fitness. Mechanisms are, therefore, expected to evolve to ensure that investment is not wasted. It is the purpose of this chapter to examine some of these mechanisms by which parents reduce the possibility of investing in non-kin.

A parent could also suffer a loss of fitness if it were to harm its own offspring. This is a possibility because males and females of many species commonly utilize conspecific infants as food. For example, this occurs in fish (reviewed by Dominey & Blumer, 1984), gulls (reviewed by Mock, 1984), and rodents (Elwood, 1977; Sherman, 1981). It is important that parents should avoid cannibalizing their own offspring except in extreme circumstances (Labov et al, 1985).

Non-random mating can be an important cause of evolutionary change within populations (see, e.g. Partridge, 1983). While several factors can lead to non-randomness in mating – dispersal patterns, intrasexual competition, mating preferences, etc. – it is the possible role of mate choice in differential mating success that has excited the greatest interest among evolutionary biologists. In part this is because, while mate choice is at the heart of part of Darwin's (1859, 1871) original theory of sexual selection, attempts to model the evolution of mating preferences have proved contentious and tests of models often equivocal (Read, 1990; Bateson, 1983; Bradbury & Andersson, 1987). Nevertheless, there is no shortage of suggestions as to the criteria on which mating preferences might be based (e.g. Halliday, 1978; Hamilton & Zuk, 1982; Bateson, 1983) and, in some cases, convincing empirical support has been forthcoming (e.g. Semler, 1971; Andersson, 1982; Majerus, 1986).

A number of lines of argument point to the degree of relatedness between potential mates as a criterion in mate choice (Bateson, 1983, 1988; Smith, 1979; Shields, 1982, 1983; Partridge, 1983). The degree to which individuals of sexually reproducing species outbreed and therefore mate with others of differing genotype is likely to have important consequences for their reproductive success, mainly through the effects of dispersal costs, changes in the level of homozygosity and indirect fitness (e.g. Smith, 1979; Bateson, 1983; Partridge, 1983). It seems likely that extremes of inbreeding or outbreeding will incur both advantages and disadvantages for individual reproductive success and that an optimal balance between them might be expected under selection.

Studies of kin recognition have progressed rapidly during the past decade. One of the most exciting aspects of this research is that the ability to recognize kin has been found, in some form or other, throughout the animal kingdom, from single-celled organisms to man. The increase in studies reporting kin recognition has led to a widespread acceptance of the role of kinship in behaviour. There is, of course, good theoretical reasons, provided by kin selection theory and mate choice theory, why this should be so, however, the importance of kinship for behaviour has often been unquestioned. One of the reasons for compiling this volume was to critically assess the role of kinship in behavioural interactions: is kin recognition responsible for the many observed differential interactions between kin and non-kin? Whilst many species have been demonstrated to recognize their kin, little attention has been given to determining how this is achieved and consequently the mechanisms underlying this ability are poorly understood. A second goal of this book was to present research which has investigated how individuals recognize their kin.

Rather than provide a taxonomic discussion of kin recognition, I have aimed to provide a book which deals with particular themes. Leading researchers in these areas were asked to discuss these issues with respect to their own expertise and species or group studied. The book may be broadly divided into two sections – that dealing with function and that dealing with mechanisms.

The importance of kinship for human societies has long been recognized, indeed the interest in kinship is reflected in the large number of works, plays, books, operas, etc., which have kinship, often mistaken, as their central theme. Whilst there has been little doubt that humans recognize their kin and respond differentially to them, the ability of animals to recognize and respond differentially to kin has received little attention. In recent years, however, study of the influence of kinship on the social behaviour of animals has increased dramatically. Much of the impetus for this research can be attributed to the seminal works of Hamilton (1964a,b) and later Wilson (1975). Evidence that kinship, or genetic relatedness, influences an individual's behaviour has now been documented in all the major groups of animals – from single-celled organisms (e.g. Grosberg & Quinn, 1986) to man (e.g. see Porter, this volume). Reptiles remain an exception to this and only recently have studies appeared providing evidence of kin recognition in this group (e.g. Werner et al, 1987), which probably reflects a lack of empirical investigation rather than a lack of ability to recognize kin. As diverse as the groups of animals which exhibit evidence of kin recognition are the behaviours in which individuals respond differentially on the basis of kinship; colonization patterns, mating, play, aggression, feeding, schooling, swarming, defence, etc. all are influenced by kinship. Investigations of the ability to recognize kin have revealed that individuals have well developed capabilities to recognize kin; siblings, half-siblings, cousins, parents, offspring, grandparents, aunts and uncles are all capable of being discriminated. Kinship thus appears to influence behaviour throughout the animal kingdom.

Introduction

The mechanisms of kin recognition have received much attention in recent years (e.g. reviews by Holmes & Sherman, 1983; Sherman & Holmes, 1985; Hepper 1986a; Waldman, 1987). However, most treatments of this topic have concentrated almost exclusively on the mechanisms by which animals are able to ‘recognize’ or classify conspecifics as either kin or nonkin. The signals or cues produced by animals and utilized by conspecifics to identify kin have, on the other hand, received only scant attention (but see Beecher, 1982; Hepper, 1986a; Waldman, 1987). Beecher (1982) stresses that ‘identification’ (the production of a signal that indicates the identity of the sender) is an important component of kin recognition which may have a significant impact on the fitness of the recipients of altruistic or nepotistic acts. Thus, discussions that focus only on the ‘recognition’ component of kin recognition address only one half of the question. An understanding of the ‘identification’ component and of the cues used for identification is essential if we are to develop a complete understanding of the mechanisms of kin recognition.

Halpin & Hoffman (1987) suggest that, in studying the cues used in kin recognition, two related but separate sets of questions need to be addressed: (1) whether the cues used for recognition are phenotypic labels shared by all genetic relatives (e.g. a family-specific label), or whether such cues are individually distinctive and, as such, provide no direct information on the genetic relatedness of conspecifics; and (2) whether the sensory cues used for kin recognition have a genetic basis or are environmentally acquired.

Recognition operates at many levels in biological organisms. At the suborganismal level, immune systems manufacture antibodies that are able to recognize and bind to foreign substances (antigens), thereby initiating a process that leads to antigen destruction. At the organismal level, individuals discriminate between objects in their environments as a function of the objects', say, nutritional value. At the population level, social structures are set up by individuals who are able to classify their conspecifics in terms of belonging to a particular group or class of individuals. If group structure is based on kinship between individuals then some type of kin recognition system is usually required to maintain the integrity of kin groups.

Recognition systems at all levels involve communication of information, whether the information is stored in the stereochemistry of molecules or the morphology of body features. In the simplest recognition systems, the messenger carrying the information is the object itself (e.g. an antigen) and the entity receiving the information executes the action (e.g. a lymphocyte). In more complex recognition processes, an object encodes a message in the form of a signal that is propagated by some physical (light, sound) or chemical transport (odour) process. Communication is completed when this signal is intercepted by a sensory system, decoded, and processed by the brain (an action may be initiated or the organism may decide not to respond). This definition is not limited to biological systems: it covers machines such as barcode readers.

In 1986 Carolyn Ehardt and I published a paper, ‘The influence of kinship and socialization on aggressive behaviour in rhesus monkeys (Macaca mulatta)’ The title of this paper is not unusual; it asserts that kinship is an independent variable that influences aggressive behaviour, as a dependent variable. This suggests that manipulation of the first will alter the second. Naturally we would be quick to deny a causal relationship and would repeat that science only demonstrates correlations, not causation. But why then did we not title the paper, ‘The influence of aggressive behaviour on kinship’? If we had done so, many would have quickly pointed to this as an example of a backward causal argument. In fact, despite our denials, we do attempt to suggest causal relationships in our correlations and, in this case, as in many others, there is a clear correlation between two variables but there may be no direct causal relationship.

Perhaps we have acknowledged the contributions of Tinbergen (1951) only to fail to apply them to our own thinking. All too often we confuse function with proximal cause, evolutionary cause, and even structure (as in definitions like ‘the process leading to’). Functional outcomes are argued to be the motivational cause of behaviour (the animal was ‘trying to drive the predator away’) and if something functions in an adaptive fashion we often assume that this is because it was selected for this function during evolution birds developed wings in order to fly south in the winter).

Introduction

Animals show both impressive feats and surprising failures of recognition. On the one hand, we have the Mexican free-tailed bat mother finding her young in a maternity cave of a million bats. On the other we have the redwinged blackbird parent failing to eject from its nest the conspicuously different eggs of a brood parasitic cowbird. From the evolutionary point of view, the failures of recognition are, on the face of it, much more difficult to explain than the successes. Any treatment of the evolution of recognition systems, therefore, must consider both faces of recognition – the failures as well as the successes. This is the perspective I take in this paper, drawing my examples from the parent-offspring context.

A source of conceptual confusion in the analysis of ‘failures’ of recognition has been the tendency of investigators to equate ‘recognition’ with ‘discrimination’. Typically, recognition is operationally defined in terms of discrimination, an animal being said to recognize a particular individual or class of individuals if it discriminates that individual or class from others (e.g. discriminates its offspring from other, unrelated young). For successes of recognition, this operational definition is perfectly reasonable. A failure of discrimination, however, could imply either that (1) discrimination is not possible, a true failure of recognition, or (2) discrimination is not adaptive in this circumstance.