Shared pathways, physiological constraint, and the evolutionary origins of an honest signal. A commentary on Számadó...

A recent review of honest signalling theory criticised constraint-based (index) explanations for traits that serve as honest signals of individual quality, contending that such explanations offer only proximate mechanisms and fail to explain evolutionary stability or the origin of reliability. A key point in this critique is the contention that ultimate explanations require the possibility of cheating. The authors advocate for the Signaling Trade-off Theory-where trade-offs make cheating evolutionarily unfavourable-as essentially a complete explanation for the evolution of signal honesty. Here, we argue that this critique rests on a false dichotomy between proximate and ultimate explanation. When signal production is mechanistically embedded within vital cellular processes, this shared pathway inherently restricts the evolution of cheating. Using avian ketocarotenoid colouration as a model, we show that condition-dependent signal production is not explained by trade-offs because pigment transformation is coupled to mitochondrial energy metabolism and core cellular performance, making high-signal expression unattainable for low-condition individuals. Deception may therefore be physiologically inaccessible rather than merely costly. Moreover, the enzymatic machinery underlying ketocarotenoid production likely evolved for visual function before being co-opted for social assessment, such that condition-dependent colour expression preceded assessment of colouration in social interactions. Uncheatable honest signals can thus arise as an exaptation of biochemical processes needed to sustain complex life rather than as outcomes of unfavourable trade-offs.