Sight-line hypothesis explains facial color patterns in terns and allies

Conspicuous coloration in animals is generally thought to evolve and be maintained through inter- or intraspecific interactions such as mate choice, but this might not always be the case. The sight-line hypothesis proposes that conspicuous light-dark contrast in front of the eyes (hereafter, eyeline) evolves and is maintained due to viability selection, enhancing an individual visual acuity and thus evolutionarily associated with a particular foraging behavior that requires accurate aiming. However, empirical evidence that supports the sight-line hypothesis is virtually absent, with no studies demonstrating the key prediction that the direction of eyelines matters. Here, I tested the sight-line hypothesis using macroevolutionary analyses in terns and allies, which are a suitable study system, because they have variation in facial color patterns, including presence/absence and, if any, various angles of eyelines. They also have a large variation in foraging behavior, including picking, plunge diving, and skimming. As predicted by the sight-line hypothesis, tern lineages that require accurate aiming at foraging (e.g., plunge diving) are more likely to have eyelines. In addition, the evolutionary transition to the state with eyelines and these foraging behaviors was more likely to occur than the reverse transition. Furthermore, as expected by the fact that the direction of travel is upwardly deviated from the direction of the bills during skimming, the eyeline angle from bills was evolutionarily positively associated with the occurrence of skimming behavior. To my knowledge, the current study is the first to demonstrate that the direction of the eyeline matters, thereby strongly supporting the sight-line hypothesis.