Three-spined sticklebacks recognize familiar individuals by facial recognition

Social vertebrates often recognize familiar individuals through facial recognition, a basal cognitive ability through which animals establish stable sociality, including territoriality. The three-spined stickleback (Gasterosteus aculeatus), a model species for behavioural studies, is territorial and its ability to visually recognize familiar individuals remains unclear. Herein, we report that this species has individual-specific facial features and recognizes familiar individuals by facial recognition. Territorial neighbours of the same sex established a 'dear enemy relationship' with each other. These focal fish were exposed to composite photographic models of four combinations of faces and bodies of familiar neighbours and unknown strangers of the same sex. Focal fish of both sexes attacked photographs of strangers (stranger-face/stranger-body) more frequently than familiar neighbours (neighbour-face/neighbour-body). Furthermore, they attacked composite photographs of the stranger-face/neighbour-body more frequently (similar to the stranger model) but less frequently attacked photographs of the neighbour-face/stranger-body (similar to the neighbour model). These results suggest that the three-spined stickleback exclusively distinguishes familiar neighbours from unknown fish via facial recognition. The aggressiveness of males was independent of the presence of a red nuptial colour in the photographs. Our findings suggest that this fish controls its aggressiveness against opponent conspecifics in the context of social relationships independent of the red area.