Parameterising a public good: how experiments on predation can be used to predict cheat frequencies

Abstract

Chemical defence is superficially easy to understand as a means for individuals to protect themselves from enemies. The evolution of chemical defence is however potentially complex because such defences may cause the generation of a public good, protecting members of the population as a whole as well as individuals that deploy toxins defensively. If a public good of protection exists, it may be exploited and degraded by ''cheats'' that do not invest in defence. This can in turn lead to complex frequency (and density) dependent effects in toxin evolution. To investigate this we used ecologically relevant predators (Great tits, Parus major) and examined how individual and public benefits vary depending on the frequency of non-defended ''cheating'' prey and their spatial distribution. We found that the public benefit, of reduced attack probability, increased with increasing frequency of defended individuals. In contrast the individual benefit of chemical defence, measured as increased chance of rejection during an attack before injury, did not vary with the frequency of defended forms. Hence the selective dynamics of these two levels of benefits responded differently to the frequency of defended forms. Surprisingly, given the strong associations of chemical defences and grouping in animals, large aggregations did not help individuals in the group regardless of their defence status. The explanation for the result, may be that in our experiment birds did not have information about other potential aggregations (i.e. set up was sequential) and thus their giving up density was lower compared to the situations where set ups were simultaneous. We use behavioural data of our predators to construct a simple model of toxin evolution which can make quantitative predictions about the frequencies to which defence cheats evolve. We use this model to discuss how toxin evolution can be investigated in the wild and in laboratory settings.

Evolutionary and ecological processes influencing chemical defense variation in an aposematic and mimeticHeliconiusbutterfly

“…A further complication in chemical defense evolution is the interplay between individual and public good (Jones et al, 2016). In this respect, our data demonstrating a broad-sense genetic component in the defense trait coupled with patterns of natural variation of cyanogen levels in Heliconius erato populations are consistent with balancing selection related to automimicry, in which automimic "cheaters" exploit the protection given by their warning coloration with investing less in chemical defenses themselves.…”

“…However, it is important to note that contrasting selective agents could be acting on the defense trait associated with the warning signal, both traits equally required for aposematism and mimicry. The selection pressures acting on chemical defense traits can be expected to be complex and dynamic (Briolat et al, 2019;Jones et al, 2016;Speed et al, 2012). The role of predators as the major selective agent is clearly a key component of possible adaptive evolutionary processes herein (Briolat et al, 2019;Ruxton et al, 2018).…”

“…Theory suggests that the frequency of automimics in a population can reach an equilibrium where the fitness of the "cheaters" (which pay reduced costs of defense but are more likely to be injured or killed by predators) is equal to the fitness of the defended individuals (which pay more costs for defense but have higher probability of surviving predator attacks) 67 the protection conveyed by the warning signal against predators 18,26,27 , similarly as in Batesian and quasi-Batesian mimicry, and influence the evolutionary trajectories of the species sharing the warning signal.…”

“…These "cheaters" (automimics) benefit from the protection of their warning coloration, without investing in energetically expensive chemical defenses 18 . A decrease in population average unpalatability due to the occurrence of automimics or weakly defended individuals could dilute the protection conveyed by the warning signal 18,26,27 , as in Batesian and quasi-Batesian mimicry. Hostplant chemistry is likely to drive intraspecific variation in sequestered defensive compounds 1,2 , as demonstrated in butterflies 28,29 .…”

Intragroup and intragenomic conflict over chemical defense against predators

“…Insects and other small invertebrates are often sufficiently chemically defended to deter many predators (Eisner, Eisner, & Siegler, ), and this chemical defense is often correlated with aggregation and distinctive aposematic warning signals (Sillen‐Tullburg, ; Ruxton & Sherratt, ). Aggregation is considered to be an important aspect of chemical defense because there is considerable evidence of a “public good” element (Jones, Speed, & Mappes, ). Specifically, aggregation of chemically defended prey is often expected because a predator that experiences an adverse reaction to tasted or ingested chemicals after attacking one individual is less likely to attack similar‐looking neighbors (e.g., Sillén‐Tullberg & Leimar, ).…”