The Impact of Detoxification Costs and Predation Risk on Foraging: Implications for Mimicry Dynamics.

Prey often evolve defences to deter predators, such as noxious chemicals including toxins. Toxic species often advertise their defence to potential predators by distinctive sensory signals. Predators learn to associate toxicity with the signals of these so-called aposematic prey, and may avoid them in future. In turn, this selects for mildly toxic prey to mimic the appearance of more toxic prey. Empirical evidence shows that mimicry could be either beneficial ('Mullerian') or detrimental ('quasi-Batesian') to the highly toxic prey, but the factors determining which are unknown. Here, we use state-dependent models to explore how tri-trophic interactions could influence the evolution of prey defences. We consider how predation risk affects predators' optimal foraging strategies on aposematic prey, and explore the resultant impact this has on mimicry dynamics between unequally defended species. In addition, we also investigate how the potential energetic cost of metabolising a toxin can alter the benefits to eating toxic prey and thus impact on predators' foraging decisions. Our model predicts that both how predators perceive their own predation risk, and the cost of detoxification, can have significant, sometimes counterintuitive, effects on the foraging decisions of predators. For example, in some conditions predators should: (i) avoid prey they know to be undefended, (ii) eat more mildly toxic prey as detoxification costs increase, (iii) increase their intake of highly toxic prey as the abundance of undefended prey increases. These effects mean that the relationship between a mimic and its model can qualitatively depend on the density of alternative prey and the cost of metabolising toxins. In addition, these effects are mediated by the predators' own predation risk, which demonstrates that, higher trophic levels than previously considered can have fundamental impacts on interactions among aposematic prey species.

The benefits of being toxic to deter predators depends on prey body size.

Many prey have evolved toxins as a defense against predation. Those species that advertise their toxicity to would-be predators with conspicuous warning signals are known as "aposematic." Investment in toxicity by aposematically signaling prey is thought to underpin how aversive prey are to predators; increasing toxicity means that predators learn to avoid prey faster and attack them at lower rates. However, predators' foraging decisions on aposematic prey are determined not only by their toxicity, but also by their nutrient content: predators can trade-off the costs of ingesting toxin with the benefits of acquiring nutrients. Prey body size is a cue that positively correlates with nutrient content, and that varies within and between aposematic species. We predicted that a dose of quinine (known to be toxic to birds) would be a more effective deterrent to avian predators when prey were small compared with when they were large, and that the benefits of possessing toxin would be greater for small-bodied prey. Using an established laboratory protocol of European starlings (Sturnus vulgaris) foraging on mealworms (Tenebrio molitor), we found evidence for increased protection from a dose of quinine for small-bodied compared with large-bodied prey. This shows that larger prey need more toxin to attain the same level of defense as smaller prey, which has implications for the evolution of aposematism and mimicry.

Body size matters for aposematic prey during predator aversion learning.

Aposematic prey advertise their toxicity to predators using conspicuous warning signals, which predators learn to use to reduce their intake of toxic prey. Like other types of prey, aposematic prey often differ in body size, both within and between species. Increasing body size can increase signal size, which make larger aposematic prey more detectable but also gives them a more effective and salient deterrent. However, increasing body size also increases the nutritional value of prey, and larger aposematic prey may make a more profitable meal to predators that are trading off the costs of eating toxins with the benefits of ingesting nutrients. We tested if body size, independent of signal size, affected predation of toxic prey as predators learn to reduce their attacks on them. European starlings (Sturnus vulgaris) learned to discriminate between defended (quinine-injected) and undefended (water-injected) mealworm prey (Tenebrio molitor) using visual signals. During this process, we found that birds attacked and ate more defended prey the larger they were. Body size does affect the probability that toxic prey are attacked and eaten, which has implications for the evolutionary dynamics of aposematism and mimicry (where species share the same warning pattern).

Increased predation of nutrient-enriched aposematic prey.

Avian predators readily learn to associate the warning coloration of aposematic prey with the toxic effects of ingesting them, but they do not necessarily exclude aposematic prey from their diets. By eating aposematic prey 'educated' predators are thought to be trading-off the benefits of gaining nutrients with the costs of eating toxins. However, while we know that the toxin content of aposematic prey affects the foraging decisions made by avian predators, the extent to which the nutritional content of toxic prey affects predators' decisions to eat them remains to be tested. Here, we show that European starlings (Sturnus vulgaris) increase their intake of a toxic prey type when the nutritional content is artificially increased, and decrease their intake when nutritional enrichment is ceased. This clearly demonstrates that birds can detect the nutritional content of toxic prey by post-ingestive feedback, and use this information in their foraging decisions, raising new perspectives on the evolution of prey defences. Nutritional differences between individuals could result in equally toxic prey being unequally predated, and might explain why some species undergo ontogenetic shifts in defence strategies. Furthermore, the nutritional value of prey will likely have a significant impact on the evolutionary dynamics of mimicry systems.

Predators' decisions to eat defended prey depend on the size of undefended prey.

Predators that have learned to associate warning coloration with toxicity often continue to include aposematic prey in their diet in order to gain the nutrients and energy that they contain. As body size is widely reported to correlate with energetic content, we predicted that prey size would affect predators' decisions to eat aposematic prey. We used a well-established system of wild-caught European starlings, Sturnus vulgaris, foraging on mealworms, Tenebrio molitor, to test how the size of undefended (water-injected) and defended (quinine-injected) prey, on different coloured backgrounds, affected birds' decisions to eat defended prey. We found that birds ate fewer defended prey, and less quinine, when undefended prey were large compared with when they were small, but that the size of the defended prey had no effect on the numbers eaten. Consequently, we found no evidence that the mass of the defended prey or the overall mass of prey ingested affected the amount of toxin that a predator was willing to ingest, and instead the mass of undefended prey eaten was more important. This is a surprising finding, challenging the assumptions of state-dependent models of aposematism and mimicry, and highlighting the need to understand better the mechanisms of predator decision making. In addition, the birds did not learn to discriminate visually between defended and undefended prey based on size, but only on the basis of colour. This suggests that colour signals may be more salient to predators than size differences, allowing Batesian mimics to benefit from aposematic models even when they differ in size.

The relationship between sympatric defended species depends upon predators' discriminatory behaviour.

Toxic prey species living in the same environment have long been thought to mutually benefit from having the same warning signal by sharing the education of naïve predators. In contrast, 'saturation theory' predicts that predators are physiologically limited by the amount of toxin that they can eat in a given time period. Therefore, sympatric species that contain the same toxin should mutually benefit from reduced predation even when they are visually distinct, reducing the benefits to visual mimicry. For the first time, we found that mutualism can occur between unequally defended prey that are visually distinct, although the benefits to each prey type depends on the predators' abilities and/or motivation to visually discriminate between them. Furthermore, we found that this variability in predatory behaviour had a significant impact on the benefits of mimicry for unequally defended prey. Our results demonstrate that variability in the foraging decisions of predators can have a significant effect on the benefits of shared toxicity and visual mimicry between sympatric species, and highlights the need to consider how predators exert selection pressures on models and mimics over their entire lifetimes.

Taste-rejection behaviour by predators can promote variability in prey defences.

The evolution and maintenance of toxicity in a prey population is a challenge to evolutionary biologists if the investment in toxin does not benefit the individual. Recent experiments suggest that taste-rejection behaviour enables predators to selectively ingest less toxic individuals, which could stabilize investment in defences. However, we currently do not know if taste rejection of defended prey is accurate across different contexts, and that prey always benefit according to their investment. Using avian predators, we show that the rejection probability does not solely depend on the investment in defence by an individual, but also on the investment by other individuals in the same population. Therefore, taste rejection by predators could lead to destabilization in the investment in defences, and allow variability in prey defences to exist.

A common intron 2 polymorphism of the glucocorticoid receptor gene is associated with insulin resistance in men.

OBJECTIVE: Clinical similarities between the metabolic syndrome and Cushing's syndrome have led to speculation of genetic association between them. The Bcl1 polymorphism in intron 2 of the glucocorticoid receptor (GR) gene has been associated with insulin resistance/hyperinsulinaemia. Our objective was to test the association of rs2918419, a T-->C single nucleotide change in intron 2 downstream of the Bcl1 locus, with components of the metabolic syndrome and its interaction with the Bcl1 locus. DESIGN AND METHODS: We genotyped a subsample of 325 White subjects (116 men) in the Newcastle Heart Project (NHP), a population-based study in north-east England. Gender-specific statistical analysis by stepwise backward multiple regression was performed to test the association of allele status with adiposity, glucose and insulin responses to oral glucose tolerance test (OGTT), fasting lipids and blood pressure. RESULTS: Minor allele frequency was 0.14 for rs2918419 and 0.39 for the Bcl1 polymorphism. rs2918419 was associated with higher fasting insulin concentration and insulin resistance in men but not in women. Contrary to earlier studies, the Bcl1 polymorphism on its own was not associated with insulin resistance/hyperinsulinaemia in either gender. Subjects carrying variant rs2918419 alleles also had variant alleles at the Bcl1 locus. In men, but not women, Bcl1 variant alleles on a background of rs2918419 wild-type alleles associated with lower fasting insulin compared to wild-type alleles at both loci or variant alleles at both loci. CONCLUSIONS: We report that rs2918419 was linked with hyperinsulinaemia and insulin resistance in men. Carrying Bcl1 variant alleles without rs2918419 was not associated with hyperinsulinaemia/insulin resistance. Previous reports of the association of Bcl1 polymorphism with obesity-related characteristics may reflect linkage disequilibrium with rs2918419.