Stuart-Fox D. 2005. Deception and the origin of honest signals. TRENDS in Ecology and Evolution 20: 521-523.

The April 2^nd Animal Communications lecture discussed the inherently tricky subject of honest signaling, a subject I have been interested in since taking courses in evolutionary psychology in college. As Stuart-Fox asserts in her 2005 article, communication should on average be honest, or the expected response would never be elicited. But, as seen in situations of “sensory trapping,” where males produce signals that affect female mate choice, “cheating” does occur. The question remains—what maintains overall signal honesty and seems to prevent widespread invasion of dishonest communicators?

The sensory trap hypothesis—where males exploit female sensory biases, such as feeding preferences—presumably sets up females to suffer fitness costs because of being deceived into mating with some sub-prime males with good signaling capabilities. In these situations, females should be selected to evolve the ability to discriminate between sub-prime males with good signals and prime males with the same signals. Eventually, if female discrimination gets so precise that only prime males are chosen, a signal that began as dishonest will become honest again.

Stuart-Fox reviews an article by Macias Garcia and Ramirez from Nature (2005) that concerns a system of central Mexican fish of the subfamily Goodeinae that appears to exhibit the preceding dishonest-to-honest signaling scheme. Males in this subfamily show differing amounts of terminal yellow carotenoid banding (TYB) on the tail, which, when wiggled, approximates the movement of worms that make up a significant part of the fish diet. Marginally conspicuous TYB elicit the strongest foraging behavior by females, forming the basis for a sensory trap males can use to lure in potential mates. In a separate study, however, Macias Garcia and Ramirez showed that while in species where TYB are absent, worms elicit a strong feeding response from both sexes, in species where TYB are very conspicuous there is little feeding response on worms. Given that the intense TYB species are also phylogenetically the most derived in Goodeinae, Stuart-Fox’s explanation for the decrease feeding response of intense TYB species is that females in these species no longer associate the TYB with food and instead the TYB has become a prime indicator of male attractiveness. Interestingly enough, as both a potential food source and a sexual character, the TYB remains costly: maintenance of the tail is linked to diet since the color is produced by carotenoids, but male body condition will take a double hit if females cannot discern the tail from food and bite the tail.

Ultimately, Stuart-Fox explains that true deception must be accompanied by some sort of fitness cost for the deceived party. The cost promotes selection for progeny to avoid such costs in the future, but the selection could allow females to 1) resist dishonest signals, 2) disregard the signals altogether or, as Macias Garcia and Ramirez found, 3) reattribute dishonest signals to honest ones.