Rethinking cross-fostering designs for studying kin recognition mechanisms

Differential treatment of kin and nonkin depends on mechanisms by which animals are able to make reliable discriminations between conspecifics. One strategy to make such distinctions in species that associate exclusively with nestmates during early rearing is to learn to recognize familiar individuals that happen to be kin and to treat them differently (‘recognition by association’; Halpin 1991). Another strategy that is particularly useful for species that are likely to encounter unfamiliar individuals that may or may not be their relatives is to discriminate between kin and nonkin based on genetic relatedness by comparing a conspecific’s phenotype with a known kin phenotype (‘phenotype matching’; Halpin 1991). Considerable research efforts have been devoted to distinguishing between the use of these mechanisms in differential aggression towards conspecifics and in mate selection in many rodent species. The phenotypematching mechanism raises additional questions because the assessment of relatedness can depend either on a kin template learned from one’s nestmates or on one’s own phenotype as a comparator (‘self-referent matching’; Holmes & Sherman 1982). Cross-fostering techniques were conceived to distinguish between the importance of familiarity and the importance of genetic relatedness in differential responses to kin and nonkin both in terms of distinctions between recognition by association and by phenotype matching and in terms of assessing whether phenotype matching is accomplished by using a learned family template or through self-referent matching. The assumption has typically been that animals use only one type of recognition mechanism (but see Holmes & Sherman 1982) and that the results from studies with subjects from cross-fostered litters will enable an accurate determination of which mechanism is used in a particular species. In their efforts to minimize prior social experience with kin, researchers typically use an individual cross-fostering design in which a single individual from each litter is reared in a foster litter (e.g. Beauchamp et al. 1988; Yamazaki et al. 1988; Aldous 1989; but see D’Amato 1994). The assumption underlying this design is that in follow-up tests individuals reared under these conditions (1) will treat their familiar foster siblings as kin and unfamiliar biological siblings as nonkin (indicating the importance of learning to recognize familiar ‘relatives’) or (2) will treat unfamiliar relatives of their foster siblings as kin (indicating the importance of learning a family template from one’s nestmates) or (3) will treat their unfamiliar genetic relatives as kin (indicating selfreferent matching, i.e. the importance of genetic relatedness apart from familiarity with particular individuals or learning a family template). Too often, unfortunately, the discriminative tests are designed in a way that biases the results towards familiarity. Tests designed to assess the relative importance of recognition by association and by phenotype matching often fail to demonstrate phenotype matching because animals tend to treat familiar and unfamiliar individuals differently regardless of whether they are relatives. Although researchers attempting to distinguish between phenotype matching by a learned family template and by self-referent matching are usually careful to control for one aspect of familiarity by testing subjects’ responses to unfamiliar relatives of their foster siblings as opposed to unfamiliar genetic relatives, these tests neglect the important fact that, for the subjects in this condition, the only ‘familiar’ phenotype they have encountered in interactions with other individuals is the foster-sibling phenotype. (Of course, subjects have experience with their own phenotype through self inspection, but familiarity with oneself is hardly comparable to familiarity with other individuals.) This means that genetic relatedness and phenotype familiarity are confounded, that is, the foster-family phenotype is familiar through encounters with foster siblings, but the subject’s own phenotype is familiar only through self inspection, thus the own family phenotype is encountered in another individual for the first time during the experimental test. The relative novelty of encountering a biological sibling (or its odour) for the first time could affect the subject’s interest in that individual (or the odour) and make it difficult to distinguish between the possible influence of familial imprinting and the possible effects of stimulus novelty. These biases are masked only when the consequences of choosing based on familiarity rather than genetic relatedness are particularly dire (as in mice carrying a lethal allele at the t locus; Lenington et al. 1992). Correspondence: J. Todrank, Institute of Evolution, University of Haifa, Haifa 31905, Israel (email: heth@research.haifa.ac.il).