Are aposematic signals honest? A review

We explore the relevance of honest signalling theory to the evolution of aposematism. We begin with a general consideration of models of signal stability, with a focus on the Zahavian costly signalling framework. Next, we review early models of signalling in the context of aposematism (some that are consistent and some inconsistent with costly honest signalling). We focus on controversies surrounding the idea that aposematic signals are handicaps in a Zahavian framework. Then, we discuss how the alignment of interests between signaller and predator influences the evolution of aposematism, highlight the distinction between qualitative and quantitative honesty and review theory and research relevant to these categories. We also review recent theoretical treatments of the evolution of aposematism that have focused on honest signalling as well as empirical research on a variety of organisms, including invertebrates and frogs. Finally, we discuss future directions for empirical and theoretical research in this area.     

Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display

Although sexual selection through female choice explains exaggerated male ornaments in many species, the evolution of the multicomponent nature of most sexual displays remains poorly understood. Theoretical models suggest that handicap signaling should converge on a single most informative quality indicator, whereas additional signals are more likely to be arbitrary Fisherian traits, amplifiers, or exploitations of receiver psychology. Male nuptial plumage in the highly polygynous red-collared widowbird (Euplectes ardens) comprises two of the commonly advocated quality advertisements (handicaps) in birds: a long graduated tail and red carotenoid coloration. Here we use multivariate selection analysis to investigate female choice in relation to male tail length, color (reflectance) of the collar, other aspects of morphology, ectoparasite load, display rate, and territory quality. The order and total number of active nests obtained are used as measures of male reproductive success. We demonstrate a strong female preference and net sexual selection for long tails, but marginal or no effects of color, morphology, or territory quality. Tail length explained 47% of male reproductive success, an unusually strong fitness effect of natural ornament variation. Fluctuating tail asymmetry was unrelated to tail length, and had no impact on mating success. For the red collar, there was negative net selection on collar area, presumably via its negative relationship with tail length. None of the color variables (hue, chroma, and brightness) had significant selection differentials, but a partial effect (selection gradient) of chroma might represent a color preference when tail length is controlled for. We suggest that the red collar functions in male agonistic interactions, which has been strongly supported by subsequent work. Thus, female choice targets only one handicap, extreme tail elongation, disregarding or even selecting against the carotenoid display. We discuss whether long tails might be better indicators of genetic quality than carotenoid pigmentation. As regards the evolution of multiple ornaments, we propose that multiple handicap signaling is stable not because of multiple messages but because of multiple receivers, in this case females and males.     

Sexual selection when the female directly benefits

Why do females of many species mate with males on the basis of traits apparently detrimental to male survival? The answer may lie in the fact that these male traits are correlated with male condition. We consider the argument that high male condition directly benefits female fecundity and/or viability (e.g. through lower transmission of parasites, improved control of resources, or better paternal care). Using a quantitative genetic model we show how female preferences for male traits that indicate condition can evolve, even if the male traits themselves have deleterious effects on both the male and the female's fecundity. So-called ‘arbitrary preferences’ can spread in this way because male traits subject to sexual selection are often under additional selection to become correlated with condition. At equilibrium the positive effects of male condition on a female's fecundity and the negative effects of the male trait on her fecundity are balanced and the female preference is under stabilizing selection. The male trait will often be correlated with viability, but not with fecundity, even though the preference evolved as a result of differences in male fecundity. The mean fecundity of females is not maximized, and can steadily decline as the male trait and female preference evolve. If the male trait has no direct deleterious effects on female fecundity, as may happen in species with no paternal care, female preferences are under continuous directional selection to increase.     

By‐product information can stabilize the reliability of communication

Although communication underpins many biological processes, its function and basic definition remain contentious. In particular, researchers have debated whether information should be an integral part of a definition of communication and how it remains reliable. So far the handicap principle, assuming signal costs to stabilize reliable communication, has been the predominant paradigm in the study of animal communication. The role of by‐product information produced by mechanisms other than the communicative interaction has been neglected in the debate on signal reliability. We argue that by‐product information is common and that it provides the starting point for ritualization as the process of the evolution of communication. Second, by‐product information remains unchanged during ritualization and enforces reliable communication by restricting the options for manipulation and cheating. Third, this perspective changes the focus of research on communication from studying signal costs to studying the costs of cheating. It can thus explain the reliability of signalling in many communication systems that do not rely on handicaps. We emphasize that communication can often be informative but that the evolution of communication does not cause the evolution of information because by‐product information often predates and stimulates the evolution of communication. Communication is thus a consequence but not a cause of reliability. Communication is the interplay of inadvertent, informative traits and evolved traits that increase the stimulation and perception of perceivers. Viewing communication as a complex of inadvertent and derived traits facilitates understanding of the selective pressures shaping communication and those shaping information and its reliability. This viewpoint further contributes to resolving the current controversy on the role of information in communication.     

Low-quality birds do not display high-quality signals: The cysteine-pheomelanin mechanism of honesty

The mechanisms that make that the costs of producing high-quality signals are unaffordable to low-quality signalers are a current issue in animal communication. The size of the melanin-based bib of male house sparrows Passer domesticus honestly signals quality. We induced the development of new bibs while treating males with buthionine-sulfoximine (BSO), a substance that depletes the levels of the antioxidant glutathione (GSH) and the amino acid cysteine, two elements that switch melanogenesis from eumelanin to pheomelanin. Final bib size is negatively related to pheomelanin levels in the bib feathers. BSO reduced cysteine and GSH levels in all birds, but improved phenotypes (bibs larger than controls) were only expressed by high-quality birds (BSO birds with largest bibs initially). Negative associations between final bib size and cysteine levels in erythrocytes, and between pheomelanin and cysteine levels, were observed in high-quality birds only. These findings suggest that a mechanism uncoupling pheomelanin and cysteine levels may have evolved in low-quality birds to avoid producing bibs of size not corresponding to their quality and greater relative costs. Indeed, greater oxidative stress in cells was not observed in low-quality birds. This may represent the first mechanism maintaining signal honesty without producing greater relative costs on low-quality signalers.