Odor-Genes Covariance and Genetic Relatedness Assessments: Rethinking Odor-Based "Recognition" Mechanisms in Rodents

Theoretical distinctions among proposed kin recognition mechanisms in rodents are difficult to reconcile with some available data. Ambiguity remains because research on recognition mechanisms was originally driven by kin selection theory but never adequately grounded in behavioral data that could inspire principles to explain observed responses. There is a tendency to design experiments in terms of categorical distinctions, such as kin vs nonkin or conspecifics vs heterospecifics, which may be more useful for researchers than meaningful to the animals. Serendipitous findings helped clarify practical aspects of odor-based mechanisms underlying differential responses to individuals of varying degrees of genetic relatedness and their individual odors. In experiments using habituation-generalization techniques, subjects from multiple species of hamsters, mole rats, and mice consistently, across degrees of relatedness from siblings to different close species, treated the individual odors of two more closely related individuals as similar in quality in comparison with the odor of less closely related individuals. The process by which particular genes are manifest in particular proportions of compounds in individual odors remains unknown, but the genotype of each individual is clearly evident in the odor of that individual. This predictable relationship between genotypes and individual odors, namely, the greater the proportion of genes that two individuals share, the greater the similarity between their individual odors, is termed "odor-genes covariance." There were two important consequences of these studies for understanding recognition mechanisms. First, differential responses to odors of familiar and unfamiliar individuals indicated that rodents learn to associate particular individuals with their individual odors and can recognize the odors of familiar individuals irrespective of genetic relatedness. Thus "individual recognition" is a mechanism for responding both to kin and nonkin rather than a "kin recognition" process. Second, in conjunction with evidence for self-referencing in graded responses based on degrees of genetic relatedness to odors of kin, populations, and species, the odor-genes covariance findings raised the intriguing possibility that such self-referencing would be the most practical means of assessing degrees of genetic relatedness to any other individual. Differential responses could occur throughout the spectrum from siblings to across species by comparing the degree of similarity between the odor of the other individual and one's own odor, that is, "genetic relatedness assessments through individual odor similarities" or G-ratios. Individual odors are individually distinctive composites that also share common qualities with other genetically similar individuals from the same kin group, population, and species. These shared qualities in the odor gestalt enable relatedness assessments rather than specific odor markers of each group. Particular preferences for individuals with similar odors and genotypes that emerge with genetic divergence could serve as a premating ethological isolating mechanism during rodent speciation. Such a mechanism may help incipient rodent species remain genetically distinct without the necessity of species- specific odor signals. Future studies should determine the breadth of these mechanisms, the neurophysiological basis of differential responses, the extent to which they are innate or learned, and their robustness in the face of transient factors, such as diet and motivational state, that may alter the qualities of individual odors.