Risk of social colours in an agamid lizard: implications for the evolution of dynamic signals

The forces of sexual and natural selection are typically invoked to explain variation in colour patterns of animals. Although the benefits of conspicuous colours for social signalling are well documented, evidence for their ecological cost, especially for dynamic colours, remains limited. We examined the riskiness of colour patterns of Psammophilus dorsalis , a species in which males express distinct colour combinations during social interactions. We first measured the conspicuousness of these colour patterns on different substrates based on the visual systems of conspecifics and predators (bird, snake, canid) and then quantified actual predation risk on these patterns using wax/polymer lizard models in the wild. The black and red male state exhibited during courtship was the most conspicuous to all visual systems, while the yellow and orange male aggression state and the brown female colour were least conspicuous. Models bearing the courtship colour pattern experienced the highest predator attacks, irrespective of the substrate they were placed on. Thus, social colours of males are not only conspicuous but also risky. Using physiological colours to shift in and out of conspicuous states may be an effective evolutionary solution to balance social signalling benefits with predation costs.

Predators attacking virtual prey reveal the costs and benefits of leadership

A long-standing assumption in social behavior is that leadership incurs costs as well as benefits, and this tradeoff can result in diversified social roles in groups. The major cost of leadership in moving animal groups is assumed to be predation, with individuals leading from the front of groups being targeted more often by predators. Nevertheless, empirical evidence for this is limited, and experimental tests are entirely lacking. To avoid confounding effects associated with observational studies, we presented a simulation of virtual prey to real fish predators to directly assess the predation cost of leadership. Prey leading others are at greater risk than those in the middle of groups, confirming that any benefits of leading may be offset by predation costs. Importantly, however, followers confer a net safety benefit to leaders, as prey leading others were less likely to be attacked compared with solitary prey. We also find that the predators preferentially attacked when solitary individuals were more frequent, but this effect was relatively weak compared with the preference for attacking solitary prey during an attack. Using virtual prey, where the appearance and behavior of the prey can be manipulated and controlled exactly, we reveal a hierarchy of risk from solitary to leading to following social strategies. Our results suggest that goal-orientated individuals (i.e., potential leaders) are under selective pressure to maintain group cohesion, favoring effective leadership rather than group fragmentation. Our results have significant implications for understanding the evolution and maintenance of different social roles in groups.

Individual boldness is linked to protective shell shape in aquatic snails

The existence of consistent individual differences in behaviour (‘animal personality’) has been well documented in recent years. However, how such individual variation in behaviour is maintained over evolutionary time is an ongoing conundrum. A well-studied axis of animal personality is individual variation along a bold–shy continuum, where individuals differ consistently in their propensity to take risks. A predation-risk cost to boldness is often assumed, but also that the reproductive benefits associated with boldness lead to equivalent fitness outcomes between bold and shy individuals over a lifetime. However, an alternative or complementary explanation may be that bold individuals phenotypically compensate for their risky lifestyle to reduce predation costs, for instance by investing in more pronounced morphological defences. Here, we investigate the ‘phenotypic compensation’ hypothesis, i.e. that bold individuals exhibit more pronounced anti-predator defences than shy individuals, by relating shell shape in the aquatic snail Radix balthica to an index of individual boldness. Our analyses find a strong relationship between risk-taking propensity and shell shape in this species, with bolder individuals exhibiting a more defended shell shape than shy individuals. We suggest that this supports the ‘phenotypic compensation’ hypothesis and sheds light on a previously poorly studied mechanism to promote the maintenance of personality variation among animals.

Sex-specific predation risk and the evolution of sexual dimorphism in immunocompetence: a theoretical analysis

Sexual dimorphism in immunocompetence, with males having lower immune function, is a prevalent pattern in nature. The main evolutionary explanation for this pattern is that males preferentially allocate resources away from immune function and towards reproductive effort to increase their competitiveness for limited females. However, the role of differential predation risk between the sexes has not been considered, despite predation risk being a major driver of life history strategies and male sexual traits often having associated predation costs. It is unclear whether increased predation risk should increase or decrease investment in immune function, as males have been shown to utilize both behavioural (e.g. decrease foraging activity) and/or life-history (e.g. decrease investment in sexual trait) defense strategies to manage predation risk. Here, we modelled optimal resource acquisition and allocation towards immune function under differential predation risk with multiple defense strategies. If males have limited defense strategies, increasing predation risk caused males to trade-off immune function for reproductive effort, leading to reduced immunocompetence. In contrast, if males can only decrease predation risk through reduction of reproductive effort (e.g. decrease colouration or calling rates), then increasing predation risk causes immune function to increase. If males can utilize multiple defense strategies and sexual selection is low, then males maintain a constant immune function as predation risk increases. Sexual selection robustly resulted in decreased immunocompetence. Overall, our results suggest that predation plays an important role in the evolution of sexual dimorphism in immunocompetence, but predicting its effect requires understanding the integrated defense strategies available.

Sex-specific predation risk and the evolution of sexual dimorphism in immunocompetence: a theoretical analysis

Sexual dimorphism in immunocompetence, with males having lower immune function, is a prevalent pattern in nature. The main evolutionary explanation for this pattern is that males preferentially allocate resources away from immune function and towards reproductive effort to increase their competitiveness for limited females. However, the role of differential predation risk between the sexes has not been considered, despite predation risk being a major driver of life history strategies and male sexual traits often having associated predation costs. It is unclear whether increased predation risk should increase or decrease investment in immune function, as males have been shown to utilize both behavioural (e.g. decrease foraging activity) and/or life-history (e.g. decrease investment in sexual trait) defense strategies to manage predation risk. Here, we modelled optimal resource acquisition and allocation towards immune function under differential predation risk with multiple defense strategies. If males have limited defense strategies, increasing predation risk caused males to trade-off immune function for reproductive effort, leading to reduced immunocompetence. In contrast, if males can only decrease predation risk through reduction of reproductive effort (e.g. decrease colouration or calling rates), then increasing predation risk causes immune function to increase. If males can utilize multiple defense strategies and sexual selection is low, then males maintain a constant immune function as predation risk increases. Sexual selection robustly resulted in decreased immunocompetence. Overall, our results suggest that predation plays an important role in the evolution of sexual dimorphism in immunocompetence, but predicting its effect requires understanding the integrated defense strategies available.

Association between shell morphology of micro-land snails (genus Plectostoma) and their predator’s predatory behaviour

Predator-prey interactions are among the main ecological interactions that shape the diversity of biological form. In many cases, the evolution of the mollusc shell form is presumably driven by predation. However, the adaptive significance of several uncommon, yet striking, shell traits of land snails are still poorly known. These include the distorted coiled “tuba” and the protruded radial ribs that can be found in micro-landsnails of the genus Plectostoma. Here, we experimentally tested whether these shell traits may act as defensive adaptations against predators. First, we identified the predators, namely, Atopos slugs and Pteroptyx beetle larvae, and their predatory strategies towards Plectostoma snails. Then, we characterised and quantified the possible anti-predation behaviour and shell traits of Plectostoma snails both in terms of their properties and efficiencies in defending against the Atopos slug predatory strategies, namely, shell-apertural entry and shell-drilling. The results showed that Atopos slugs would first attack the snail by shell-apertural entry, and, should this fail, shift to the energetically more costly shell-drilling strategy. We found that the shell tuba of Plectostoma snails is an effective defensive trait against shell-apertural entry attack. None of the snail traits, such as resting behaviour, shell thickness, shell tuba shape, shell rib density and intensity can protect the snail from the slug’s shell-drilling attack. However, these traits could increase the predation costs to the slug. Further analysis on the shell traits revealed that the lack of effectiveness these anti-predation shell traits may be caused by a functional trade-off between shell traits under selection of two different predatory strategies. Lastly, we discuss our results in the framework of Red Queen predator-prey coevolution and escalation, and propose several key elements for future study.

Association between shell morphology of micro-land snails (genus Plectostoma) and their predator’s predatory behaviour

Predator-prey interactions are among the main ecological interactions that shape the diversity of biological form. In many cases, the evolution of the mollusc shell form is presumably driven by predation. However, the adaptive significance of several uncommon, yet striking, shell traits of land snails are still poorly known. These include the distorted coiled “tuba” and the protruded radial ribs that can be found in micro-landsnails of the genus Plectostoma. Here, we experimentally tested whether these shell traits may act as defensive adaptations against predators. First, we identified the predators, namely, Atopos slugs and Pteroptyx beetle larvae, and their predatory strategies towards Plectostoma snails. Then, we characterised and quantified the possible anti-predation behaviour and shell traits of Plectostoma snails both in terms of their properties and efficiencies in defending against the Atopos slug predatory strategies, namely, shell-apertural entry and shell-drilling. The results showed that Atopos slugs would first attack the snail by shell-apertural entry, and, should this fail, shift to the energetically more costly shell-drilling strategy. We found that the shell tuba of Plectostoma snails is an effective defensive trait against shell-apertural entry attack. None of the snail traits, such as resting behaviour, shell thickness, shell tuba shape, shell rib density and intensity can protect the snail from the slug’s shell-drilling attack. However, these traits could increase the predation costs to the slug. Further analysis on the shell traits revealed that the lack of effectiveness these anti-predation shell traits may be caused by a functional trade-off between shell traits under selection of two different predatory strategies. Lastly, we discuss our results in the framework of Red Queen predator-prey coevolution and escalation, and propose several key elements for future study.

Differences in Patch Use Behavior Between an Urban and Rural Species: Effects of Distance from Shelter and Wing Molt-Gaps

It has been suggested that urban bird populations and communities are controlled by bottom-up mechanisms because predation costs are lower in urban than in non-urban habitats. We hypothesized that urban birds are less sensitive to variations in the cost of predation than non-urban birds. We predicted that the house sparrow, a widespread urban species, is less sensitive to variations in predation risk, while foraging, than its rural (less urban) congener, the Spanish sparrow. We quantified foraging behavior of these species, as affected by the proximity to shelter, in large outdoor aviaries. We then clipped feathers from the birds' wings to manipulate escape ability and increase predation risk. We predicted that birds experience increasing predation risk with increasing distance from shelter, and that reduced wing surface increases the birds' sensitivity to risk of predation with respect to distance from shelter. Both species displayed increasing giving-up densities in seed trays with increasing distance from shelter, indicating that foraging costs increase with distance from shelter. As predicted, the two species differed in their response to proximity of shelter: we concluded that house sparrows experienced a less pronounced increase in perceived predation cost with increasing distance from shelter than did Spanish sparrows. Contrary to our prediction, wing surface reduction had no effect on seed tray utilization. Therefore, it appears that, when feeding in patches at distances from shelter, as used in the present study, the cost of predation affects foraging and micro-habitat use in Spanish sparrows more than in house sparrows.