Mating experience shapes male mating behavior across species, from insects, fish, and birds, to rodents. Here, we investigated the effect of multiple mating experiences on male mating behavior in “naïve” (defined as sexually inexperienced) male medaka fish. The latency to mate with the same female partner significantly decreased after the second encounter, whereas when the partner was changed, the latency to mate was not decreased. These findings suggest that mating experiences enhanced the mating activity of naïve males for the familiar female, but not for an unfamiliar female. In contrast, the mating experiences of “experienced” (defined as those having mated > 7 times) males with the same partner did not influence their latency to mate. Furthermore, we identified 10 highly and differentially expressed genes in the brains of the naïve males after the mating experience and revealed 3 genes that are required for a functional cascade of the thyroid hormone system. Together, these findings suggest that the mating experience of naïve male medaka fish influences their mating behaviors, with neural changes triggered by thyroid hormone activation in the brain.

The first mating (sexual) experience leads to the maturation of male mating behavior across species (insects, fish, rodents). Here, we investigated whether the first mating experience leads to maturation of male mating behavior in medaka using repeated mating tests. In “naïve” (sexually inexperienced) males after the first mating experience, the latency to mate with the same female partner was significantly decreased, whereas when the partner was swapped, the latency to mate was not affected. These findings suggest that repeated matings (3 times) enhanced male mating activity for the familiarized female, but not for an unfamiliarized female. In “experienced” (> 7 matings) males, repeated matings (3 times) with the same partner did not influence the latency to mate, suggesting that multiple matings (> 7 times) abolish the mate preference of naïve males. Furthermore, we identified 10 highly and differentially expressed genes after the mating experience in the brains of the post-naïve males, and revealed 3 genes that are required for a functional cascade of the thyroid hormone system. These findings together suggest that the first mating experience abolishes the preference to mate with a familiarized female via neural maturation triggered by thyroid hormone activation in the medaka brain.

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