Russell A. Ligon

Chameleons communicate with complex colour changes during contests: different body regions convey different information.

Many animals display static coloration (e.g. of feathers or fur) that can serve as a reliable sexual or social signal, but the communication function of rapidly changing colours (as in chameleons and cephalopods) is poorly understood. We used recently developed photographic and mathematical modelling tools to examine how rapid colour changes of veiled chameleons Chamaeleo calyptratus predict aggressive behaviour during male–male competitions. Males that achieved brighter stripe coloration were more likely to approach their opponent, and those that attained brighter head coloration were more likely to win fights; speed of head colour change was also an important predictor of contest outcome. This correlative study represents the first quantification of rapid colour change using organism-specific visual models and provides evidence that the rate of colour change, in addition to maximum display coloration, can be an important component of communication. Interestingly, the body and head locations of the relevant colour signals map onto the behavioural displays given during specific contest stages, with lateral displays from a distance followed by directed, head-on approaches prior to combat, suggesting that different colour change signals may evolve to communicate different information (motivation and fighting ability, respectively).

Defeated chameleons darken dynamically during dyadic disputes to decrease danger from dominants

Research on intraspecific aggression has typically focused on dominant individuals, but a better understanding of the consequences and mechanisms of agonistic encounters requires a balanced perspective that includes knowledge of subordinate animal behaviors. In contrast to signals of fighting ability, signals of submission are an understudied component of agonistic communication that could provide important insights into the dynamics, function, and evolution of intraspecific competition. Here, I use a series of staged agonistic trials between adult male veiled chameleons Chamaeleo calyptratus to test the hypothesis that rapid skin darkening serves as a submissive signal to resolve agonistic activity. Concordant with this hypothesis, I found that losing chameleons darkened over the course of aggressive trials while winners brightened, and the likelihood of darkening increased when individuals were attacked more aggressively. Additionally, I found that the degree of brightness change exhibited by individual chameleons was tied to both overall and net aggression experienced during a trial, with chameleons who received high levels of aggression relative to their own aggression levels darkening to a greater extent than individuals receiving relatively less aggression. Lastly, I found that aggression increased for losers and winners prior to the onset of darkening by the eventual loser but that both chameleons reduced aggression after the losing chameleon began to darken. Based on the theoretical prediction that signals of submission should be favored when retreat options are restricted, I suggest that limited escapability imposed by chameleon morphology, physiology, and ecology favored the evolution of a pigment-based signal of submission in this group.

Biochemical regulation of pigment motility in vertebrate chromatophores: a review of physiological color change mechanisms

Abstract The fundamental unit of rapid, physiological color change in vertebrates is the dermal chromatophore unit. This unit, comprised of cellular associations between different chromatophore types, is relatively conserved across the fish, amphibian, and reptilian species capable of physiological color change and numerous attempts have been made to understand the nature of the four major chromatophore types (melanophores, erythrophores, xanthophores, and iridophores) and their biochemical regulation. In this review, we attempt to describe the current state of knowledge regarding what classifies a pigment cell as a dynamic chromatophore, the unique characteristics of each chromatophore type, and how different hormones, neurotransmitters, or other signals direct pigment reorganization in a variety of vertebrate taxa.

Social costs enforce honesty of a dynamic signal of motivation

Understanding the processes that promote signal reliability may provide important insights into the evolution of diverse signalling strategies among species. The signals that animals use to communicate must comprise mechanisms that prohibit or punish dishonesty, and social costs of dishonesty have been demonstrated for several fixed morphological signals (e.g. colour badges of birds and wasps). The costs maintaining the honesty of dynamic signals, which are more flexible and potentially cheatable, are unknown. Using an experimental manipulation of the dynamic visual signals used by male veiled chameleons (Chamaeleo calyptratus) during aggressive interactions, we tested the idea that the honesty of rapid colour change signals is maintained by social costs. Our results reveal that social costs are an important mechanism maintaining the honesty of these dynamic colour signals—‘dishonest’ chameleons whose experimentally manipulated coloration was incongruent with their contest behaviour received more physical aggression than ‘honest’ individuals. This is the first demonstration, to the best our knowledge, that the honesty of a dynamic signal of motivation—physiological colour change—can be maintained by the social costliness of dishonesty. Behavioural responses of signal receivers, irrespective of any specific detection mechanisms, therefore prevent chameleon cheaters from prospering.

Evolutionary innovation and diversification of carotenoid‐based pigmentation in finches

The ornaments used by animals to mediate social interactions are diverse, and by reconstructing their evolutionary pathways we can gain new insights into the mechanisms underlying ornamental innovation and variability. Here, we examine variation in plumage carotenoids among the true finches (Aves: Fringillidae) using biochemical and comparative phylogenetic analyses to reconstruct the evolutionary history of carotenoid states and evaluate competing models of carotenoid evolution. Our comparative analyses reveal that the most likely ancestor of finches used dietary carotenoids as yellow plumage colorants, and that the ability to metabolically modify dietary carotenoids into more complex pigments arose secondarily once finches began to use modified carotenoids to create red plumage. Following the evolutionary “innovation” that enabled modified red carotenoid pigments to be deposited as plumage colorants, many finch species subsequently modified carotenoid biochemical pathways to create yellow plumage. However, no reversions to dietary carotenoids were observed. The finding that ornaments and their underlying mechanisms may be operating under different selection regimes—where ornamental trait colors undergo frequent reversions (e.g., between red and yellow plumage) while carotenoid metabolization mechanisms are more conserved—supports a growing empirical framework suggesting different evolutionary patterns for ornaments and the mechanistic innovations that facilitate their diversification.

Body mass and immune function, but not bill coloration, predict dominance in female mallards

Competition over indivisible resources is common and often costly. Therefore, selection should favor strategies, including efficient communication, that minimize unnecessary costs associated with such competition. For example, signaling enables competitors to avoid engaging in costly asymmetrical contests. Recently, bill coloration has been identified as an information-rich signal used by some birds to mediate aggressive interactions and we evaluated this possibility in female mallards Anas platyrhynchos. Specifically, we conducted two rounds of competitive interactions among groups of unfamiliar adult female ducks. By recording all aggressive behaviors exhibited by each individual, as well as the identity of attack recipients, we were able to assign dominance scores and evaluate links between numerous physiological, morphological, and experimental variables that we predicted would influence contest outcome and dominance. Contrary to our predictions, dominance was not linked to any aspect of bill coloration, access to dietary carotenoids during development, two of three measures of immune function, or ovarian follicle maturation. Instead, heavier birds were more dominant, as were those with reduced immune system responses to an experimentally administered external immunostimulant, phytohemagglutinin. These results suggest that visual signals are less useful during the establishment of dominance hierarchies within multi-individual scramble competitions, and that immune function is correlated with contest strategies in competitions for access to limited resources.

Evolution of correlated complexity in the radically different courtship signals of birds-of-paradise

Ornaments used in courtship often vary wildly among species, reflecting the evolutionary interplay between mate preference functions and the constraints imposed by natural selection. Consequently, understanding the evolutionary dynamics responsible for ornament diversification has been a longstanding challenge in evolutionary biology. However, comparing radically different ornaments across species, as well as different classes of ornaments within species, is a profound challenge to understanding diversification of sexual signals. Using novel methods and a unique natural history dataset, we explore evolutionary patterns of ornament evolution in a group - the birds-of-paradise - exhibiting dramatic phenotypic diversification widely assumed to be driven by sexual selection. Rather than the tradeoff between ornament types originally envisioned by Darwin and Wallace, we found positive correlations among cross-modal (visual/acoustic) signals indicating functional integration of ornamental traits into a composite unit - the courtship phenotype. Furthermore, given the broad theoretical and empirical support for the idea that systemic robustness - functional overlap and interdependency - promotes evolutionary innovation, we posit that birds-of-paradise have radiated extensively through ornamental phenotype space as a consequence of the robustness in the courtship phenotype that we document at a phylogenetic scale. We suggest that the degree of robustness in courtship phenotypes among taxa can provide new insights into the relative influence of sexual and natural selection on phenotypic radiations. Author Summary Animals frequently vary widely in ornamentation, even among closely related species. Understanding the patterns that underlie this variation is a significant challenge, requiring comparisons among drastically different traits - like comparing apples to oranges. Here, we use novel analytical approaches to quantify variation in ornamental diversity and richness across the wildly divergent birds-of-paradise, a textbook example of how sexual selection can profoundly shape organismal phenotypes. We find that color and acoustic complexity, along with behavior and acoustic complexity, are positively correlated across evolutionary time-scales. Positive covariation among ornament classes suggests that selection is acting on correlated suites of traits - a composite courtship phenotype - and that this integration may be partially responsible for the extreme variation we see in birds-of-paradise.

Climate, habitat, and geographic range overlap drive plumage evolution

Organismal appearances are shaped by selection from both abiotic and biotic drivers 1–5. For example, Gloger’s rule describes the pervasive pattern that more pigmented populations are found in more humid areas 1,6,7, and substrate matching as a form of camouflage to reduce predation is widespread across the tree of life 8–10. Sexual selection is a potent driver of plumage elaboration 5,11, and species may also converge on nearly identical colours and patterns in sympatry, often to avoid predation by mimicking noxious species 3,4 To date, no study has taken an integrative approach to understand how these factors determine the evolution of colour and pattern across a large clade of organisms. Here we show that both habitat and climate profoundly shape avian plumage. However, we also find a strong signal that many species exhibit remarkable convergence not explained by these factors nor by shared ancestry. Instead, this convergence is associated with geographic overlap between species, suggesting strong, albeit occasional, selection for interspecific mimicry. Consequently, both abiotic and biotic factors, including interspecific interactions, are potent drivers of phenotypic evolution.

Behavioral Evolution: Can You Dig It?

Behaviors are among the most complex phenotypes, making the genetic dissection of behavioral differences extremely challenging. A careful dissection of ontogenetic differences in burrowing behavior between mouse species highlights the importance of integrative approaches to the study of behavioral evolution.

A chorus of color: hierarchical and graded information content of rapid color change signals in chameleons

Dynamic color signals represent a rare signaling strategy but there are numerous parallels between rapid color changes and the vocalizations used to mediate aggressive interactions in other taxa. Here, we used a robochameleon to elicit color change from live chameleons and linked these signals to individual-specific performance and behavior.