Our enduring fascination with issues concerning language and thought may derive from our sense that these are uniquely human capacities. Despite years of devoted tutoring, even our closest genealogical relatives have yet to acquire the complex and creative linguistic systems that human infants master within the first few years of life (Petitto & Seidenberg, 1979; Premack, 1971). And although members of other species surely manifest sophisticated conceptual and representational capacities, these appear to be accessible to them only under restricted conditions (Rozin, 1976). Findings like these lend substance to the intuition that humans are uniquely endowed with the capacity to build complex, flexible, and creative linguistic and conceptual systems.

Recent research has documented the remarkable rate at which very young children naturally acquire language and develop rich conceptual systems. Researchers estimate that by the time children reach 2 years of age, they learn an average of six new words each day (Templin, 1957). They also have at their command a rich variety of conceptual relations (e.g., taxonomic, thematic, and associative relations) with which they organize and categorize the objects and events they encounter in their lives.

Introduction

It has long been held in psychological and philosophical circles that important insights into the nature of cognitive processes can be gained through an analysis of the connectives if and because (Traugott, ter Meulen, Reilly, & Ferguson, 1986). In particular, if … then statements serve the important linguistic function of expressing fundamental cognitive processes such as inference and prediction, and because statements figure prominently in the cognitive processes of argumentation and explanation. Moreover, while the structure and function of these connectives make them particularly useful for describing causal relations, they are also ideally suited for characterizing a variety of other relations among objects or events.

Linguistically, these connectives are important to study because if and because constructions fall within the category of “complex” sentences (as opposed to “simple” or “compound” sentences). Specifically, such constructions often consist of the embedding of one sentence into another. For example, in “If today is Tuesday, the bill is overdue,” each of “Today is Tuesday” and “the bill is overdue” could stand alone. Developmental psycholinguists have found it important to study how children progress from the connectiveless juxtaposition of sentences to the integration of sentences within a single connective construction (e.g., Hood & Bloom, 1979). In addition, an adequate semantic analysis of if constructions has proved to be quite a complex and vexing issue and one that has generated a great deal of interest (Fillenbaum, 1986). The elusiveness of the meaning of if for adults makes one wonder how children ever come to acquire if constructions.

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.