Abstract Honest signals have long posed a challenge for evolutionary biologists to explain. Here we propose a general Darwinian theory of signalling, Signalling Trade-Off Theory, to explain both honest and dishonest signalling based on recent theoretical and empirical developments. The leading explanation for honest signalling has been the Handicap Principle, which argues that signals are honest because they are costly. We summarize the main reasons why the Handicap Principle—and the related Costly Signalling paradigm—can be fully rejected. Instead, we propose an alternative and more general explanation for honest signalling. The acceptance of the erroneous Handicap Principle was based on misinterpretations of early signalling models. These models contrary to common interpretations, show that signals are honest, not because they are costly (handicaps), but because cheating (deception) is costly. Deception is costly due to differential signalling costs or differential benefits, or more generally differential trade-offs (i.e., an antagonistic constraint between two functions). Trade-offs are the basis evolutionary life-history theory, and we argue that they are also central to explaining signal honesty and deception. Unlike costs, trade-offs can fully represent both aspects of an investment (marginal cost vs. marginal benefit) over different timescales arising in evolutionary analyses. We examine the alternative explanations proposed to explain honest signalling, such as indices and social punishment, and show that these hypotheses require trade-offs, despite being overlooked. We examine more recent theoretical models that demonstrate that signalling trade-offs maintain honesty, even without signalling costs (handicaps) at the evolutionary equilibrium. Moreover, we show that differential trade-offs are both necessary and sufficient to explain honest signals in cases with conflict of interest. Based on these advances, we argue that differential signalling trade-offs provide a general evolutionary explanation for both dishonest and honest signals and also unifies earlier alternative proposals about signal honesty. Finally, we demonstrate that short-term investments under trade-offs at the proximate level (once considered handicap mechanisms) can result in long-term fitness benefits, which thus integrates proximate and evolutionary explanations for signal honesty. We also address how results from sexual selection studies (e.g., terminal investment) are consistent with our theory.
Számadó et al. (Tue,) studied this question.