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"Sherratt, Thomas N"
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The biology of color
Animals live in a colorful world, but we rarely stop to think about how this color is produced and perceived, or how it evolved. Cuthill et al. review how color is used for social signals between individual animals and how it affects interactions with parasites, predators, and the physical environment. New approaches are elucidating aspects of animal coloration, from the requirements for complex cognition and perception mechanisms to the evolutionary dynamics surrounding its development and diversification. Science , this issue p. eaan0221 Coloration mediates the relationship between an organism and its environment in important ways, including social signaling, antipredator defenses, parasitic exploitation, thermoregulation, and protection from ultraviolet light, microbes, and abrasion. Methodological breakthroughs are accelerating knowledge of the processes underlying both the production of animal coloration and its perception, experiments are advancing understanding of mechanism and function, and measurements of color collected noninvasively and at a global scale are opening windows to evolutionary dynamics more generally. Here we provide a roadmap of these advances and identify hitherto unrecognized challenges for this multi- and interdisciplinary field.
Journal Article
Body size affects the evolution of eyespots in caterpillars
Many caterpillars have conspicuous eye-like markings, called eyespots. Despite recent work demonstrating the efficacy of eyespots in deterring predator attack, a fundamental question remains: Given their protective benefits, why have eyespots not evolved in more caterpillars? Using a phylogenetically controlled analysis of hawkmoth caterpillars, we show that eyespots are associated with large body size. This relationship could arise because ( i ) large prey are innately conspicuous; ( ii ) large prey are more profitable, and thus face stronger selection to evolve such defenses; and/or ( iii ) eyespots are more effective on large-bodied prey. To evaluate these hypotheses, we exposed small and large caterpillar models with and without eyespots in a 2 × 2 factorial design to avian predators in the field. Overall, eyespots increased prey mortality, but the effect was particularly marked in small prey, and eyespots decreased mortality of large prey in some microhabitats. We then exposed artificial prey to naïve domestic chicks in a laboratory setting following a 2 × 3 design (small or large size × no, small, or large eyespots). Predators attacked small prey with eyespots more quickly, but were more wary of large caterpillars with large eyespots than those without eyespots or with small eyespots. Taken together, these data suggest that eyespots are effective deterrents only when both prey and eyespots are large, and that innate aversion toward eyespots is conditional. We conclude that the distribution of eyespots in nature likely results from selection against eyespots in small caterpillars and selection for eyespots in large caterpillars (at least in some microhabitats).
Significance Eyespots are a widespread form of antipredator defense that have long captured the imagination of evolutionary biologists, geneticists, psychologists, and artists. These markings are particularly common within Lepidoptera, and eyespots on caterpillars have been shown to deter avian predators; however, why eyespots have evolved in particular caterpillar species, and why they are not even more widespread, remain unclear. Here we answer this question using a powerful three-pronged approach. Our phylogenetically controlled analysis of hawkmoths demonstrates that eyespots are typically restricted to large caterpillars, and our field and laboratory experiments provide an explanation for this. Eyespots are costly to small caterpillars because they enhance detectability without providing a protective advantage, but they are beneficial to large caterpillars because they deter predators.
Journal Article
Taste and pheromonal inputs govern the regulation of time investment for mating by sexual experience in male Drosophila melanogaster
Males have finite resources to spend on reproduction. Thus, males rely on a ‘time investment strategy’ to maximize their reproductive success. For example, male
Drosophila melanogaster
extends their mating duration when surrounded by conditions enriched with rivals. Here we report a different form of behavioral plasticity whereby male fruit flies exhibit a shortened duration of mating when they are sexually experienced; we refer to this plasticity as ‘shorter-mating-duration (SMD)’. SMD is a plastic behavior and requires sexually dimorphic taste neurons. We identified several neurons in the male foreleg and midleg that express specific sugar and pheromone receptors. Using a cost-benefit model and behavioral experiments, we further show that SMD behavior exhibits adaptive behavioral plasticity in male flies. Thus, our study delineates the molecular and cellular basis of the sensory inputs required for SMD; this represents a plastic interval timing behavior that could serve as a model system to study how multisensory inputs converge to modify interval timing behavior for improved adaptation.
Journal Article
Similar Survival Rates of Territorial and Sneaker Males in a Polymorphic Damselfly: A Multi-Year Study
Male alternative reproductive tactics (ARTs) have been documented across diverse taxa and typically involve a male morph that defends resources to attract females and an alternate morph that exploits this behavior to obtain matings by stealth (territorial-sneaker tactics). One might expect that territorial morphs would live shorter lives than sneaker morphs due to their higher vulnerability to predators, their propensity to get injured and higher energetic costs. To date, there have been few direct field tests of this prediction. A mark-release-resighting (MRR) study conducted in 1992 found that orange-winged territorial morphs of the damselfly
had on average a shorter minimum reproductive lifespan than clear-winged sneaker morphs, if one assumed that they all emerged on a single day, but not if they were assumed to be of age 0 at the time of capture. We fitted Cormack-Jolly-Seber models to these 1992 data, as well as MRR studies conducted on
in four subsequent years. These models allowed us to jointly estimate the daily survival and resighting rates of the morphs and identify consistent predictors of their survival and detectability. There was no evidence of a significant difference in survival between male morphs or between males and females, although daily survival did consistently rise then fall with time since capture (age) and consistently declined with temperature above 17°C. By contrast, there was strong evidence that the resighting rates of individuals differed among morphs, with orange-winged males being more detectable. While there is no compelling evidence that the territorial and sneaker morphs have different daily survival rates, this does not preclude the possibility that orange-winged territorial males have high reproductive success on the days they are able to maintain a territory while the reproductive success of clear-winged sneaker males has reproductive success that is more broadly distributed across their lives.
Journal Article
Response of adult dragonflies to artificial prey of different size and colour
Aposematism is an evolved, cross-species association between a preys' unprofitability and the presence of conspicuous signals. Avian predators have been widely employed to understand the evolution of these warning signals However, insect predators are abundant, diverse, and highly visual foragers that have been shown to be capable of learned aversion. Therefore, it is likely that their behaviour also shapes the nature of anti-predator traits. In this study, we evaluated the rates of attack of a community (13 species) of mature adult dragonflies (Odonata) on artificial prey of varying size (2.5-31 mm lengthwise) and colour pattern (black, black/yellow striped). The relative attack rates of dragonflies on prey increased as prey size decreased, but there was no evidence that the attack rates by dragonflies were affected by prey colour pattern and no evidence for an interaction between colour pattern and size. To investigate prey selection by specific predator species under field conditions, we compared the time to attack distributions of black-painted prey presented to two common dragonflies: Leucorrhinia intacta and the larger, Libellula pulchella. We found that the two dragonfly species, as well as the two sexes, had different foraging responses. L. pulchella was more likely to attack larger prey, and females of both species more likely to attack prey than males. Collectively, our results indicate that dragonflies are highly size selective. However, while the nature of this selectivity varies among dragonfly species, there is little evidence that classic black/yellow warning signals deter attack by these aerial invertebrate predators.
Journal Article
Signal categorization by foraging animals depends on ecological diversity
Warning signals displayed by defended prey are mimicked by both mutualistic (Müllerian) and parasitic (Batesian) species. Yet mimicry is often imperfect: why does selection not improve mimicry? Predators create selection on warning signals, so predator psychology is crucial to understanding mimicry. We conducted experiments where humans acted as predators in a virtual ecosystem to ask how prey diversity affects the way that predators categorize prey phenotypes as profitable or unprofitable. The phenotypic diversity of prey communities strongly affected predator categorization. Higher diversity increased the likelihood that predators would use a ‘key’ trait to form broad categories, even if it meant committing errors. Broad categorization favors the evolution of mimicry. Both species richness and evenness contributed significantly to this effect. This lets us view the behavioral and evolutionary processes leading to mimicry in light of classical community ecology. Broad categorization by receivers is also likely to affect other forms of signaling.
Journal Article
Coevolutionary patterns between coloration and diel activity in moths
Anti-predator coloration is part of a key survival strategy in animals, often coevolving with behavioural traits such as diel activity. While previous studies have explored the link between conspicuous sexual signals and diurnality, the association between defensive coloration and diel activity remains unresolved. Here, we investigate the coevolutionary relationship between anti-predator coloration and diel activity in moths, a diverse clade with variable colour and activity patterns. Using a dataset of 322 moth species, we classified coloration of each species as cryptic or conspicuous and diel activity as diurnal, nocturnal, crepuscular or both day and night active (‘All’). We applied phylogenetic comparative methods to assess evolutionary transitions between these traits. Our findings suggest that moths ancestrally exhibited cryptic coloration and nocturnality. Conspicuous coloration was more frequent in diurnal species, supporting an evolutionary association between daytime activity and being conspicuous. Transitions between nocturnal and diurnal activity occurred predominantly through an intermediate All state, particularly in cryptic species. Cryptic diurnality also evolved in some lineages, possibly driven by specific ecological factors such as when thermoregulatory needs are high. These findings provide insights into the interplay between diel activity and anti-predator coloration, with implications for understanding correlated evolution between these two traits.
Journal Article
Conspicuous Coloration in Males of the Damselfly Nehalennia irene (Zygoptera: Coenagrionidae): Do Males Signal Their Unprofitability to Other Males?
In damselflies, sexual colour dimorphism is commonly explained as a consequence of selection on traits that increase male attractiveness to females. However, while many species in the damselfly family Coenagrionidae (Insecta: Odonata) are sexually dimorphic, the males do not engage in displays, and male competition for mates resembles a \"scramble\". An alternative explanation for the sexual differences in coloration within these species is that sexual dimorphism has evolved as a sex-related warning signal, with males signalling their uprofitability as mates to other males, thereby avoiding harassment from conspecifics. We evaluated an underlying assumption of the theory that male-male harassment rate is influenced by colour by comparing harassment of males of the species Nehalennia irene that had been painted to make them appear: (i) similar to an unaltered male (blue), (ii) different from a male (orange) and (iii) more similar to a female (black). When caged together we found that blue-painted males experienced significantly lower harassment than black-painted males. When unpainted males were caged with each type of painted male we found that blue-painted males and the unpainted males housed in the same cages experienced lower rates of harassment than males housed in cages where some males were painted black, suggesting that a single, reliable signal of unprofitability may benefit the individuals that carry it. While our results do not in themselves demonstrate that sexual colour dimorphism originally evolved as an intra-specific warning signal, they do show that harassment is influenced by coloration, and that such selection could conceivably maintain male coloration as a warning signal.
Journal Article
Mixed Signals? Morphological and Molecular Evidence Suggest a Color Polymorphism in Some Neotropical Polythore Damselflies
The study of color polymorphisms (CP) has provided profound insights into the maintenance of genetic variation in natural populations. We here offer the first evidence for an elaborate wing polymorphism in the Neotropical damselfly genus Polythore, which consists of 21 described species, distributed along the eastern slopes of the Andes in South America. These damselflies display highly complex wing colors and patterning, incorporating black, white, yellow, and orange in multiple wing bands. Wing colors, along with some components of the male genitalia, have been the primary characters used in species description; few other morphological traits vary within the group, and so there are few useful diagnostic characters. Previous research has indicated the possibility of a cryptic species existing in P. procera in Colombia, despite there being no significant differences in wing color and pattern between the populations of the two putative species. Here we analyze the complexity and diversity of wing color patterns of individuals from five described Polythore species in the Central Amazon Basin of Peru using a novel suite of morphological analyses to quantify wing color and pattern: geometric morphometrics, chromaticity analysis, and Gabor wavelet transformation. We then test whether these color patterns are good predictors of species by recovering the phylogenetic relationships among the 5 species using the barcode gene (COI). Our results suggest that, while highly distinct and discrete wing patterns exist in Polythore, these \"wingforms\" do not represent monophyletic clades in the recovered topology. The wingforms identified as P. victoria and P. ornata are both involved in a polymorphism with P. neopicta; also, cryptic speciation may have taking place among individuals with the P. victoria wingform. Only P. aurora and P. spateri represent monophyletic species with a single wingform in our molecular phylogeny. We discuss the implications of this polymorphism, and the potential evolutionary mechanisms that could maintain it.
Journal Article