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.
