Ontogenetic Color Switching in Lizards as a by-Product of Guanine Cell Development

Many animals undergo dramatic changes in colour during development1,2. Changes in predation risk during ontogeny are associated with spectacular switches in defensive colours, typically involving the replacement of skin or the production of new pigment cells3. Ontogenetic colour systems are ideal models for understanding the evolution and formation mechanisms of animal colour which remain largely enigmatic2. We show that defensive colour switching in lizards arises by reorganization of a single photonic system, as an incidental by-product of chromatophore maturation. The defensive blue tail colour of hatchling A. beershebensis lizards is produced by light scattering from premature guanine crystals in underdeveloped iridophore cells. Camouflaged adult tail colours emerge upon reorganization of the guanine crystals into a photonic reflector during chromatophore maturation. The substituent guanine crystals form by the attachment of individual nanoscopic plates, which coalesce during growth to form single crystals. Our results show that the blue colour of hatchlings is a fortuitous, but necessary, precursor to the development of adult colour. Striking functional colours in animals can thus arise not as distinct evolutionary innovations but via exploitation of the timing of naturally occurring changes in chromatophore cell development.

Relaxed risk of predation drives parallel evolution of stickleback behaviour

The occurrence of similar phenotypes in multiple independent populations (viz. parallel evolution) is a testimony of evolution by natural selection. Parallel evolution implies that populations share a common phenotypic response to a common selection pressure associated with habitat similarity. Examples of parallel evolution at the genetic and phenotypic levels are fairly common, but the driving selective agents often remain elusive. Similarly, the role of phenotypic plasticity in facilitating early stages of parallel evolution is unclear. We investigated whether the relaxation of predation pressure associated with the colonization of freshwater ponds by nine-spined sticklebacks (Pungitius pungitius) likely explains the divergence in complex behaviours between marine and pond populations, and whether this divergence is parallel. Using laboratory-raised individuals exposed to different levels of perceived predation risk, we calculated vectors of phenotypic divergence for four behavioural traits between habitats and predation risk treatments. We found a significant correlation between the directions of evolutionary divergence and phenotypic plasticity, suggesting that habitat divergence in behaviour is aligned with the response to relaxation of predation pressure. Finally, we show that this alignment is found across multiple pairs of populations, and that the relaxation of predation pressure has likely driven parallel evolution of behaviour in this species.

Welcome to the Dark Side: Partial Nighttime Illumination Affects Night-and Daytime Foraging Behavior of a Small Mammal

Differences in natural light conditions caused by changes in moonlight are known to affect perceived predation risk in many nocturnal prey species. As artificial light at night (ALAN) is steadily increasing in space and intensity, it has the potential to change movement and foraging behavior of many species as it might increase perceived predation risk and mask natural light cycles. We investigated if partial nighttime illumination leads to changes in foraging behavior during the night and the subsequent day in a small mammal and whether these changes are related to animal personalities. We subjected bank voles to partial nighttime illumination in a foraging landscape under laboratory conditions and in large grassland enclosures under near natural conditions. We measured giving-up density of food in illuminated and dark artificial seed patches and video recorded the movement of animals. While animals reduced number of visits to illuminated seed patches at night, they increased visits to these patches at the following day compared to dark seed patches. Overall, bold individuals had lower giving-up densities than shy individuals but this difference increased at day in formerly illuminated seed patches. Small mammals thus showed carry-over effects on daytime foraging behavior due to ALAN, i.e., nocturnal illumination has the potential to affect intra- and interspecific interactions during both night and day with possible changes in personality structure within populations and altered predator-prey dynamics.

Comparative vulnerability of Indosylvirana temporalis and Clinotarsus curtipes (Anura: Ranidae) tadpoles to water scorpions: importance of refugia and swimming speed in predator avoidance

The comparative vulnerability of two co-existing tadpole species (Indosylvirana temporalis and Clinotarsus curtipes) to their common predator, water scorpions (Laccotrephes sp.; Hemiptera: Nepidae), and the importance of refugia in predator avoidance were studied in the laboratory. In a total of 60 experimental trials, 10 tadpoles each of I. temporalis and C. curtipes of comparable body sizes were exposed to water scorpions (starved for 48 h). Thirty trials included refugia while 30 did not. The results of this study showed that in both the absence and the presence of refugia C. curtipes tadpoles fell prey to water scorpions more frequently than I. temporalis tadpoles. A main difference between the two species is the speed of swimming; Vmax of C. curtipes (24.73 cm/s) tadpoles is lower than that of I. temporalis (30.78 cm/s) tadpoles. This is likely to be the reason why more C. curtipes tadpoles were preyed upon than were I. temporalis tadpoles. Predation risk of tadpoles of both species was affected significantly by the presence of refuge sites. The vulnerability of both tadpole species was lower where refuge sites were available. The present study clearly shows that I. temporalis tadpoles avoid predation by water scorpions more effectively than do C. curtipes tadpoles.

Odour-Mediated Interactions Between an Apex Reptilian Predator and its Mammalian Prey

An important but understudied modality for eavesdropping between predators and prey is olfaction, especially between non-mammalian vertebrate predators and their prey. Here we test three olfactory eavesdropping predictions involving an apex reptilian predator, the sand goanna Varanus gouldii, and several species of its small mammalian prey in arid central Australia: 1) small mammals will recognise and avoid the odour of V. gouldii; 2) V. gouldii will be attracted to the odour of small mammals, especially of species that maximise its energetic returns; and 3) small mammals will be less mobile and will show higher burrow fidelity where V. gouldii is absent compared with where it is present. As expected, we found that small mammals recognised and avoided faecal odour of this goanna, feeding less intensively at food patches where the odour of V. gouldii was present than at patches with no odour or a pungency control odour. Varanus gouldii also was attracted to the odour of small mammals in artificial burrows, and dug more frequently at burrows containing the odour of species that were energetically profitable than at those of species likely to yield diminished returns. Our third prediction received mixed support. Rates of movement of three species of small mammals were no different where V. gouldii was present or absent, but burrow fidelity in two of these species increased as expected where V. gouldii had been removed. We conclude that olfaction plays a key role in the dynamic interaction between V. gouldii and its mammalian prey, with the interactants using olfaction to balance their respective costs of foraging and reducing predation risk. We speculate that the risk of predation from this apex reptilian predator drives the highly unusual burrow-shifting behaviour that characterises many of Australia's small desert mammals.

Both Prey and Predator Features Determine Predation Risk and Survival of Schooling Prey

Predation is one of the main evolutionary drivers of social grouping. While it is well appreciated that predation risk is likely not shared equally among individuals within groups, its detailed quantification has remained difficult due to the speed of attacks and the highly-dynamic nature of collective prey response. Here, using high-resolution tracking of solitary predators (Northern pike) hunting schooling fish (golden shiners), we not only provide detailed insights into predator decision-making but show which key spatial and kinematic features of predator and prey influence individual's risk to be targeted and survive attacks. Pike tended to stealthily approach the largest groups, and were often already inside the school when launching their attack, making prey in this frontal "strike zone" the most vulnerable to be targeted. From the prey's perspective, those fish in central locations, but relatively far from, and less aligned with, neighbours, were most likely to be targeted. While the majority of attacks (70%) were successful, targeted individuals that did manage to avoid capture exhibited a higher maximum acceleration response just before the attack and were further away from the pike's head. Our results highlight the crucial interplay between predators' attack strategy and response of prey in determining predation risk in mobile animal groups.