Holmes and Sherman (1982) on Ground Squirrels
KeywordsGenetic Relatedness Ground Squirrel Inclusive Fitness Unrelated Female Arctic Ground Squirrel
Phenotype matching refers to the ability to detect genetic relatedness based on phenotypic cues of the self or close kin.
In laboratory studies it was found that Belding’s ground squirrels (Spermophilus beldingi) are able to recognize kin with which they did not share natal burrows. Related female individuals, even if they were unfamiliar to each other, were less agonistic than unrelated individuals. Field studies also showed that littermate full-sisters treat each other differently than maternal half-sisters. This suggests that both rearing environment and relatedness have crucial contribution to nepotistic behavior in ground squirrels. Similar results with other rodent species imply that learning and recognition of cues of probable genetic relatedness, known as phenotype matching, might be a mechanism which influences social interactions.
Mechanisms of Kin Recognition
First, spatial cues (i.e., co-residence) can inform individuals about relatedness.
Second, early association is a somewhat better heuristic for the estimation of kinship. For species which disperse after the juvenile period and, therefore, may easily find themselves in the proximity of nonrelated conspecifics, co-residence is an uncertain cue of genetic closeness.
Third, as a theoretical possibility, it has been proposed that recognition alleles could serve the recognition of related individuals. This allele should be expressed phenotypically, recognized by others and it is expected to increase the likelihood of preferential treatment of the individuals with that cue.
Fourth, if there is a correlation between the similarity of phenotypic traits and the amount of shared genes, phenotype matching can provide individuals with the necessary information about relatedness. During the juvenile period they can learn either the cues (e.g., odors) of their littermates and other co-residing conspecifics (other-referent phenotype matching), or that of their own (self-referent phenotype matching), and later use these as a recognition template to assess genetic relatedness to unfamiliar individuals.
Ground Squirrels as Model Animals
Holmes and Sherman (1982) used Belding’s ground squirrels (Spermophilus beldingi) and Arctic ground squirrels (S. parryii) as model animals to test whether phenotype matching is used for kin recognition in these species. They cross-fostered preweaned pups in a laboratory environment and tested the behavior of related and familiar individuals and related and unfamiliar individuals in pairs. It turned out that ground squirrels which were reared together treat each other as siblings, that is, they are not more agonistic than sibling pairs. Besides, female siblings reared apart showed less aggressiveness than unrelated female pairs. Field observations of Belding’s ground squirrels revealed also females’ ability to discriminate between full-sisters and maternal half-sisters, despite they shared the natal burrow with both sibling types. They are more cooperative and less agonistic with full-sisters than with half-sisters – an impressive demonstration of the inclusive fitness theory. Hence, it was suggested, shared environment shape prosocial behavior and so does genetic relatedness.
In subsequent experiments, the role of phenotype matching in kin recognition was studied further. It was shown that females of S. beldingi treat paternal half-sisters differently than unrelated females (Holmes 1986a). In this case, as these siblings were reared apart, familiarity could not contribute to the biased behavior. When female ground squirrels were cross-fostered and reared in a mixed group of related and unrelated littermates, paired arena tests confirmed that both shared natal environment and relatedness affects the frequency of agonistic acts (Holmes 1986b). On the one hand, when females encountered unrelated females, the level of aggression was modest. Note that due to cross-fostering they were mutually the sisters of each other’s littermates. This shows that exposure to a certain phenotype in the natal burrow is used later as a template to which other individuals are compared (Holmes 1984). In this case, information about phenotypic cues of nonrelated littermates is used to recognize kin of that littermates (other-referent phenotype matching). On the other hand, unfamiliar sisters are recognized and preferred as well, even in case the pup does not share its natal environment with any relatives, preventing the use of phenotypic cues other than her own (self-referent phenotype matching).
The ability to recognize kin, and to prefer them over conspecifics who are genetically not related, has been observed in many taxa, including insects and mammals. It has been suggested that this bias was selected for during evolution and might be best explained by the theory of inclusive fitness. Several mechanisms have been put forward to account for kin recognition, most notably phenotype matching. In their influential paper, Holmes and Sherman (1982) provided evidence that ground squirrel pups (Spermophilus sp.) learn phenotypic cues of both their littermates and their own, to which unfamiliar individuals are compared at later encounters. Though theoretically both sexes might use this ability the discriminate between conspecifics with different degrees of relatedness, biased behavior is limited to female–female interactions. This suggests that kin-recognition is used in these rodent species as a means of nepotism, rather than that of optimal mate choice.
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