Body size affects the evolution of eyespots in caterpillars

Abstract

Many caterpillars have conspicuous eye-like markings, called eyespots. Despite recent work demonstrating the efficacy of eyespots in deterring predator attack, a fundamental question remains: Given their protective benefits, why have eyespots not evolved in more caterpillars? Using a phylogenetically controlled analysis of hawkmoth caterpillars, we show that eyespots are associated with large body size. This relationship could arise because (i) large prey are innately conspicuous; (ii) large prey are more profitable, and thus face stronger selection to evolve such defenses; and/or (iii) eyespots are more effective on large-bodied prey. To evaluate these hypotheses, we exposed small and large caterpillar models with and without eyespots in a 2 × 2 factorial design to avian predators in the field. Overall, eyespots increased prey mortality, but the effect was particularly marked in small prey, and eyespots decreased mortality of large prey in some microhabitats. We then exposed artificial prey to naïve domestic chicks in a laboratory setting following a 2 × 3 design (small or large size × no, small, or large eyespots). Predators attacked small prey with eyespots more quickly, but were more wary of large caterpillars with large eyespots than those without eyespots or with small eyespots. Taken together, these data suggest that eyespots are effective deterrents only when both prey and eyespots are large, and that innate aversion toward eyespots is conditional. We conclude that the distribution of eyespots in nature likely results from selection against eyespots in small caterpillars and selection for eyespots in large caterpillars (at least in some microhabitats).antipredator defense | caterpillars | Lepidoptera | predator-prey | mimicry

Camouflage

“…Defences which putatively rely on intimidation, like eyespots, are ineffective on animals with smaller body sizes (Hossie et al, 2015). Furthermore, the switch between camouflage and aposematism can be size dependent (Valkonen et al, 2014).…”

A review of the sentinel prey method as a way of quantifying invertebrate predation under field conditions

“…Countershading (Edmunds & Dewhirst, 1994;Rowland et al, 2007), or reverse countershading (Rowland et al, 2008) can reduce bird predation, although not in all cases (Speed et al, 2005;Hossie & Sherratt, 2012). The defensive value of eyespots remains unclear, as it can be effective in itself (Hossie & Sherratt, 2013) or when interacting with countershading (Hossie & Sherratt, 2012), but it can also cause increased mortality (Hossie et al, 2015). Mimicking bird dropping can significantly reduce bird predation only when interacting with prey posture (Suzuki & Sakurai, 2015).…”

Evolution and losses of spines in slug caterpillars (Lepidoptera: Limacodidae)

“…It has been demonstrated that defensive characters such as warning coloration are more effective when displayed in insects with large bodies (Forsman & Merilaita, 1999;Hossie, Skelhorn, Breinholt, Kawahara, & Sherratt, 2015). It has been demonstrated that defensive characters such as warning coloration are more effective when displayed in insects with large bodies (Forsman & Merilaita, 1999;Hossie, Skelhorn, Breinholt, Kawahara, & Sherratt, 2015).…”

“…The first hypothesis is that spines get lost or reduced because they confer no advantage below a certain size threshold. It has been demonstrated that defensive characters such as warning coloration are more effective when displayed in insects with large bodies (Forsman & Merilaita, 1999;Hossie, Skelhorn, Breinholt, Kawahara, & Sherratt, 2015). For example, defensive eyespots are effective in big caterpillars, but costly in small caterpillars, because they enhance detectability without providing a protective advantage in small caterpillars (Hossie et al, 2015).…”

“…It has been demonstrated that defensive characters such as warning coloration are more effective when displayed in insects with large bodies (Forsman & Merilaita, 1999;Hossie, Skelhorn, Breinholt, Kawahara, & Sherratt, 2015). For example, defensive eyespots are effective in big caterpillars, but costly in small caterpillars, because they enhance detectability without providing a protective advantage in small caterpillars (Hossie et al, 2015). In tree-feeding insects, avian predation risk increased with larger prey body size (Remmel, Davison, & Tammaru, 2011;Remmel & Tammaru, 2009).…”