A review and assessment of the Shared-Pathway Hypothesis for the maintenance of signal honesty in red ketocarotenoid-based coloration

For decades, scientists have noted connections between individual condition and carotenoid-based coloration in terrestrial and aquatic animals. Organisms that produce more vibrant carotenoid-based coloration tend to have better physiological performance and behavioral displays compared to less colorful members of the same species. Traditional explanations for this association between ornamental coloration and performance invoked the need for color displays to be costly, but evidence for such hypothesized costs is equivocal. An alternative explanation for the condition-dependence of carotenoid-based coloration, the Shared-Pathway Hypothesis, was developed in response. This hypothesis proposes that red ketocarotenoid-based coloration is tied to core cellular processes involving a shared pathway with mitochondrial energy metabolism, making the concentration of carotenoids an index of mitochondrial function. Since the presentation of this hypothesis, empirical tests of the mechanisms proposed therein have been conducted in many species. In this manuscript, we review the Shared-Pathway Hypothesis and the growing number of studies that have investigated a connection between carotenoid-based coloration and mitochondrial function. We also discuss future strategies for assessing the Shared-Pathway Hypothesis to more effectively disentangle evidence that may simultaneously support evidence of carotenoid-resource tradeoffs.

A sensory bias overrides learned preferences of bumblebees for honest signals in Mimulus guttatus

Insect pollinators readily learn olfactory cues, and this is expected to select for ‘honest signals' that provide reliable information about floral rewards. However, plants might alternatively produce signals that exploit pollinators' sensory biases, thereby relaxing selection for signal honesty. We examined the innate and learned preferences of Bombus impatiens for Mimulus guttatus floral scent phenotypes corresponding to different levels of pollen rewards in the presence and absence of the innately attractive floral volatile compound β-trans-bergamotene. Bees learned to prefer honest signals after foraging on live M. guttatus flowers, but only exhibited this preference when presented floral scent phenotypes that did not include β-trans-bergamotene. Our results suggest that a sensory bias for β-trans-bergamotene overrides the ability of B. impatiens to use honest signals when foraging on M. guttatus . This may represent a deceptive pollination strategy that allows plants to minimize investment in costly rewards without incurring reduced rates of pollinator visitation.

Reproduction and signals regulating worker policing under identical hormonal control in social wasps

In social Hymenoptera, fertility and fertility signalling are often under identical hormonal control, and it has been suggested that such hormonal pleiotropies can help to maintain signal honesty. In the common wasp Vespula vulgaris, for example, fertile queens have much higher juvenile hormone (JH) titers than workers, and JH also controls the production of chemical fertility cues present on the females’ cuticle. To regulate reproductive division of labour, queens use these fertility cues in two distinct ways: as queen pheromones that directly suppress the workers’ reproduction as well as to mark queen eggs and enable the workers to recognize and police eggs laid by other workers. Here, we investigated the hormonal pleiotropy hypothesis by testing if experimental treatment with the JH analogue methoprene could enable the workers to lay eggs that evade policing. In support of this hypothesis, we find that methoprene-treated workers laid more eggs, and that the chemical profiles of their eggs were more queen-like, thereby causing fewer of their eggs to be policed compared to in the control. Overall, our results identify JH as a key regulator of both reproduction and the production of egg marking pheromones that mediate policing behaviour in eusocial wasps.

Trophy hunters pay more to target larger-bodied carnivores

Hunters often target species that require resource investment disproportionate to associated nutritional rewards. Costly signalling theory provides a potential explanation, proposing that hunters target species that impose high costs (e.g. higher failure and injury risks, lower consumptive returns) because it signals an ability to absorb costly behaviour. If costly signalling is relevant to contemporary ‘big game’ hunters, we would expect hunters to pay higher prices to hunt taxa with higher perceived costs. Accordingly, we hypothesized that hunt prices would be higher for taxa that are larger-bodied, rarer, carnivorous, or described as dangerous or difficult to hunt. In a dataset on 721 guided hunts for 15 North American large mammals, prices listed online increased with body size in carnivores (from approximately $550 to $1800 USD/day across the observed range). This pattern suggests that elements of costly signals may persist among contemporary non-subsistence hunters. Persistence might simply relate to deception, given that signal honesty and fitness benefits are unlikely in such different conditions compared with ancestral environments in which hunting behaviour evolved. If larger-bodied carnivores are generally more desirable to hunters, then conservation and management strategies should consider not only the ecology of the hunted but also the motivations of hunters.

Achromatic plumage brightness predicts stress resilience and social interactions in tree swallows (Tachycineta bicolor)

Theory suggests that signal honesty may be maintained by differential costs for high and low quality individuals. For signals that mediate social interactions, costs can arise from the way that a signal changes the subsequent social environment via receiver responses. These receiver-dependent costs may be linked with individual quality through variation in resilience to environmental and social stress. Here, we imposed stressful conditions on female tree swallows (Tachycineta bicolor) by attaching groups of feathers during incubation to decrease flight efficiency and maneuverability. We simultaneously monitored social interactions using an RFID network that allowed us to track the identity of every individual that visited each nest for the entire season. Before treatments, plumage coloration was correlated with baseline and stress-induced corticosterone. Relative to controls, experimentally challenged females were more likely to abandon their nest during incubation. Overall, females with brighter white breasts were less likely to abandon, but this pattern was only significant under stressful conditions. In addition to being more resilient, brighter females received more unique visitors at their nest-box and tended to make more visits to other active nests. In contrast, dorsal coloration did not reliably predict abandonment or social interactions. Taken together, our results suggest that females differ in their resilience to stress and that these differences are signaled by plumage brightness, which is in turn correlated with the frequency of social interactions. While we do not document direct costs of social interaction, our results are consistent with models of signal honesty based on receiver-dependent costs.

No honesty in warning signals across life stages in an aposematic bug

Theory predicts that warning signals should exhibit low variation to increase learning efficiency in predators. However, many species exhibit variation in warning colours within species and even within populations. An understudied example of within species variation is that between life stages, where animals change warning colouration throughout ontogeny. Understanding how warning signals change throughout life can help us identify the different ecological pressures that affect the evolution of warning signals. We used the Australasian Harlequin Cotton bug (Tectocoris diophthalmus) to explore how adults and nymphs differ in toxicity and colouration. We performed spectrophotometric colour measurements, toxicity bioassays and field predation experiments. Our results show that colour acts as an honest signal only in males, who present the highest contrast against backgrounds, highest internal contrast, and highest toxicity. However, there was no clear pattern for females and nymphs, and attack rates were similar for both. Moreover, there was no association between colour and toxicity within males, nymphs or females. Our results suggest weak signal honesty in warning signals across life stages and sexes, and demonstrate that variation in colour within species is not necessarily linked to changes in toxicity or predation rates.