Evolution of conspicuousness in defended species involved in Müllerian mimicry

Abstract

Abstract Variation in warning pattern resulting in different levels of conspicuousness is observed within and among chemically-defended prey species. Toxin acquisition and predator avoidance behaviour have been shown to affect the evolutionary processes underlying such warning signal diversity. Predators learn to associate warning colour pattern with unpalatability and this results in a decrease in predation risk for individuals displaying a locally abundant warning pattern. This positive number-dependent selection generated by predators causes evolutionary convergence across defended prey species toward a common warning colour pattern (Mullerian mimicry). Mullerian mimicry has a strong effect on the local diversity of warning patterns in tight connexion with the local abundance of mimetic species. Moreover, because chemical defences often stem from diet, the levels of defences might depend on resource specialisation, therefore impacting species abundance and the evolution of aposematic colour patterns. To investigate the effect of Mullerian mimicry on the evolution of the conspicuousness of warning signal and unpalatability, we built a single-species model where warning signal and unpalatability can evolve, assuming that (1) predation risk depends on both the number of individuals sharing a warning signal within the studied species and the local abundance of mimetic species and (2) the level of unpalatability depends on resource specialisation, implying that specialists suffer from reduced carrying capacity. We found that Mullerian mimicry can promote the evolution of more conspicuous colouration in cryptic species. Nevertheless, by favouring locally abundant signals, Mullerian mimicry stabilizes the persistence of mildly conspicuous patterns, explaining for instance the evolution of partially transparent colour patterns in some chemically-defended butterflies. Our model also show that Mullerian mimicry limits the emergence of new aposematic signals associated with reduced unpalatability. Altogether, our theoretical approach highlights complex interplays between resource specialisation, mimicry and predator behaviour on the evolution of aposematic signals and associated defences. Impact summary Aposematism, whereby chemically-defended species display conspicuous colouration acting as warning signal is still a debated question, involves the joint evolution of two independent traits, namely colour pattern and chemical defences. Evolution of new conspicuous warning signal is an evolutionary puzzle, because individuals exhibiting increased conspicuousness suffer from increased detection by predators. Convergence in warning pattern is frequently observed among defended prey (i.e. Mullerian mimicry), because sharing a common warning signal decreases individual predation risk. Mimicry among defended prey species may therefore profoundly influence the evolution of warning signals conspicuousness and chemical defences both within and among prey species. The origin of variations in chemical defences is still largely unknown for a wide range of prey species, but toxic compounds are frequently sequestered from food intake so that specialized species may be more likely to successfully accumulate toxins from their diet. In turn, such specialization may limit species abundance locally, because of restricted range of resource and have a profound importance on the dynamics of aposematic signals. Understanding the evolution of aposematism therefore requires integrating ecological parameters linked to the evolution of defence levels and species abundance. Here we use a theoretical approach to investigate the evolution of colour pattern conspicuousness in a chemically-defended species, involved in Mullerian mimicry. We explore the impact of ecological parameters, such as composition of local mimetic communities and diet specialisation on the evolution of aposematic signal and chemical defences. We show that (i) mimetic interactions are a key factor enhancing fixation of new patterns with increased conspicuousness (ii) even mildly conspicuous signals can persist in species involved in Mullerian mimicry and that (iii) the evolution of chemical defences in Mullerian mimics tightly depends on the resource acquisition pathway.