Our understanding of animal communication has been largely driven by advances in theory since empirical evidence has been difficult to obtain. Costly signaling theory became the dominant paradigm explaining the evolution of honest signals, according to which communication reliability relies on differential costs imposed on signalers to distinguish animals of different quality. On the other hand, mathematical models disagree on the source of costs at the communication equilibrium. Here we present an empirical framework to study the evolution of honest signals that generates predictions on the form, function and sources of reliability of visual signals. We test these predictions on the facial color patterns of the cooperatively breeding Princess of Burundi cichlid, Neolamprologus brichardi. Using theoretical visual models and behavioral experiments we show that these patterns possess stable chromatic properties for efficient transmission in the aquatic environment, while dynamic changes in signal luminance are used by the fish to communicate switches in aggressive intent. By manipulating signal into out-of-equilibrium expression and simulating a cheater invasion, we demonstrate that social costs (receiver retaliation) promote the honesty of this dynamic conventional signal. By directly probing the sender of a signal in real time, social selection is likely to be the mechanism of choice shaping the evolution of inexpensive, yet reliable context-dependent social signals in general.

Male secondary sexual traits are targets of inter- and/or intrasexual selection, but can vary due to a correlation with life-history traits or as by-product of adaptation to distinct environments. Trade-offs contributing to this variation may comprise conspicuousness toward conspecifics versus inconspicuousness toward predators, or between allocating resources into coloration versus the immune system. Here, we examine variation in expression of a carotenoid-based visual signal, anal-fin egg-spots, along a replicate environmental gradient in the haplochromine cichlid fish Astatotilapia burtoni. We quantified egg-spot number, area, and coloration; applied visual models to estimate the trait's conspicuousness when perceived against the surrounding tissue under natural conditions; and used the lymphocyte ratio as a measure for immune activity. We find that (1) males possess larger and more conspicuous egg-spots than females, which is likely explained by their function in sexual selection; (2) riverine fish generally feature fewer but larger and/or more intensely colored egg-spots, which is probably to maintain signal efficiency in intraspecific interactions in long wavelength shifted riverine light conditions; and (3) egg-spot number and relative area correlate with immune defense, suggesting a trade-off in the allocation of carotenoids. Taken together, haplochromine egg-spots feature the potential to adapt to the respective underwater light environment, and are traded off with investment into the immune system.