Evolutionary stability of frequency-dependent secondary defense in a soft-bodied insect with and without signals

Abstract

Secondary defenses can reduce predation risk by altering predator behavior, but their evolution may be constrained when defended prey are indistinguishable from undefended individuals. This is particularly relevant for soft-bodied prey, for which predator attacks are lethal regardless of defense level, such that the benefits of defense are frequency-dependent. We developed two sets of evolutionary models to investigate how secondary defense evolves in the presence vs. absence of signals that allow predators to distinguish defended from undefended prey. First, we used deterministic evolutionary game theory to examine the stability of defended and undefended strategies across attack likelihoods, defense levels, and initial frequencies of defended prey. Second, we developed stochastic, multi-generational models in which predators optimized foraging decisions according to their energetic state, allowing selection to emerge from state-dependent predator behavior. For both model sets, undefended prey were evolutionarily stable when predation pressure was low, whereas stronger predation favored defended phenotypes. However, in the absence of signals defended and undefended prey frequently coexisted, with stable mixed populations emerging when predation pressure was sufficiently high, defense levels low, and the initial proportion of defended prey was above a threshold frequency. In contrast, when signals were present, mixed equilibria were generally unstable and highly defended prey frequently displaced other phenotypes, particularly under high predation pressure. Stochastic models produced similar patterns while demonstrating that 1. prey population size influenced the likelihood of invasion by defended phenotypes, with smaller populations being more conducive to invasion; 2. qualitative patterns similar to the deterministic models emerged when selection was dependent on predators' state-dependent behavior. Our results identify conditions under which inconspicuous, costly secondary defenses can persist even when defense provides no benefit to the individual, presenting a plausible route towards the evolution of phenomena such as aposematism.