Olfactory imprinting on environmental, population- and kin-specific cues is a specific form of life-long memory promoting homing of salmon to their natal rivers and the return of coral reef fish to natal sites. Despite its ecological significance, natural chemicals for olfactory imprinting have not been identified yet. Here, we show that MHC peptides function as chemical signals for olfactory imprinting in zebrafish. We found that MHC peptides consisting of nine amino acids elicit olfactory imprinting and subsequent kin recognition depending on the MHC genotype of the fish. In vivo calcium imaging shows that some olfactory bulb neurons are highly sensitive to MHC peptides with a detection threshold at 1 pM or lower, indicating that MHC peptides are potent olfactory stimuli. Responses to MHC peptides overlapped spatially with responses to kin odour but not food odour, consistent with the hypothesis that MHC peptides are natural signals for olfactory imprinting.

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Kin recognition can drive kin selection and the evolution of social behaviour. In zebrafish (Danio rerio, Hamilton 1822), kin recognition is based on olfactory and visual imprinting processes. If larvae are exposed to visual and chemical cues of kin at day 5 and 6 post fertilization they will recognize kin throughout life, while exposure to non-kin fails to trigger any recognition. Chemical imprinting signals are transcribed by polymorphic genes of the major histocompatibility complex (MHC) code; however, the underlying mechanism for visual imprinting remains unclear. Here we provide evidence for the existence of family-specific differences in morphometry and pigmentation pattern of six day old zebrafish larvae. While rump, tail and body pigmentation were dependent on relatedness, iris pigmentation and morphometry were also influenced by MHC class II genotype. Our study revealed that the MHC not only influences the chemical signature of individuals, but also their visual appearance.

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