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Abstract

During mate choice decisions, females of many vertebrates use male olfactorycues to achieve immunogenetic optimality of their offspring. Three-spinedsticklebacks (Gasterosteusaculeatus) populating habitats that differ in theirparasite communities evolve locally adapted combinations of genetic variantsencoded at the major histocompatibility complex (MHC). Such adaptationconfers optimal resistance to the local parasite fauna. Immunogenetic signa-tures co-evolved with local parasites favour population-specific assortativemate choice behaviour. Previous studies have shown that female sticklebacksevaluate male MHC-associated olfactory cues during the process of matechoice, but how habitat-specific information is exchanged between malesand females has remained elusive. Here, we directly demonstrate themolecular nature of the olfactory cue providing habitat-specific information.Under controlled laboratory conditions, females that are ready to mateprefer mixtures of synthetic MHC peptide ligands mimicking the optimalallele number of their original population. These results imply that femalesticklebacks can determine the number of MHC alleles of their prospectivemates, compare it to their own immunogenetic status, and, if optimal withrespect to the immunogenetic complementarity, accept the male as mate.Our results suggest a potentially common mechanism of ecological speciationin vertebrates that is based on the olfactory assessment of habitat-specificimmunogenetic diversity.