Three-spined sticklebacks recognise familiar individuals by facial recognition

Social vertebrates often recognise familiar individuals by facial recognition, a basal cognitive ability by which animals establish stable sociality, including territoriality. The three-spined stickleback (Gasterosteus aculeatus), a model species for behavioural studies, is territorial; its ability to visually recognise familiar individuals remains unclear. Here, we report that this species has individual-specific facial colour morph features and can recognise 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 frequently attacked photographs of strangers (stranger-face/stranger-body) more frequently than familiar neighbours (neighbour-face/neighbour-body). Furthermore, they attacked composite photographs of stranger-face/neighbour-body more frequently (similar to the stranger model) but less frequently attacked photographs of neighbour-face/stranger-body (similar to the neighbour model). These results suggest that the three-spined stickleback distinguishes familiar neighbours from unknown fish exclusively via facial recognition. The aggressiveness of males was independent of the presence of red nuptial colour on photograph-models. Our findings suggest that this fish controls its aggressiveness against opponent conspecifics in the context of social relationships independent of the sign-stimulus.