Defensive posture and eyespots deter avian predators from attacking caterpillar models

Hossie, Thomas J.; Sherratt, Thomas N.

doi:10.1016/j.anbehav.2013.05.029

Cited by 55 publications

(45 citation statements)

References 17 publications

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“…Batesian mimics are harmless organisms that resemble a more dangerous 'model' in order to deceive potential predators [3], and while some show an astonishing level of similarity to their models, others bear only a passing resemblance. Both theory [4] and experiments [5][6][7] show that, in practical terms, mimicry is a continuum rather than a simple binary category: inaccurate mimics are attacked less frequently than non-mimics, but more often than more accurate ones (but see [8,9]). We would, therefore, expect the most accurate mimics in a population to have the highest fitness, and that natural selection should drive ever-increasing perfection in resemblance to the model.…”

Section: Introductionmentioning

confidence: 99%

Why many Batesian mimics are inaccurate: evidence from hoverfly colour patterns

2016

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Mimicry is considered a classic example of the elaborate adaptations that natural selection can produce, yet often similarity between Batesian (harmless) mimics and their unpalatable models is far from perfect. Variation in mimetic accuracy is a puzzle, as natural selection should favour mimics that are hardest to distinguish from their models. Numerous hypotheses exist to explain the persistence of inaccurate mimics, but most have rarely or never been tested against empirical observations from wild populations. One reason for this is the difficulty in measuring pattern similarity, a key aspect of mimicry. Here, we use a recently developed method, based on the distance transform of binary images, to quantify pattern similarity both within and among species for a group of hoverflies and their hymenopteran models. This allowed us to test three key hypotheses regarding inaccurate mimicry. Firstly, we tested the prediction that selection should be more relaxed in less accurate mimics, but found that levels of phenotypic variation are similar across most hoverfly species. Secondly, we found no evidence that mimics have to compromise between accuracy to multiple model species. However, we did find that darker-coloured hoverflies are less accurate mimics, which could lead to a trade-off between mimicry and thermoregulation in temperate regions. Our results shed light on a classic problem concerning the limitations of natural selection.

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Section: Introductionmentioning

confidence: 99%

Why many Batesian mimics are inaccurate: evidence from hoverfly colour patterns

2016

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“…Previous field experiments using similar model caterpillars have shown a protective effect of eyespots (11,12), yet large prey with and without eyespots had approximately equal mortality in our current field experiment. Indeed, although there was significant (overall deleterious) effect of eyespots in our present field experiment, there was no evidence of a significant eyespots × body size interaction.…”

Section: Discussionmentioning

confidence: 58%

“…Our phylogenetic analysis clearly demonstrates that the evolution of eyespots is associated with large body size, and our field and laboratory experiments provide an explanation for this; eyespots increase predation rates on small caterpillars by making them easier to detect, but-at least as far as our laboratory data and previous studies (11,12) indicate-large eyespots decrease predation rates on large caterpillars, likely because they intimidate predators (see also ref. 33).…”

Section: Discussionmentioning

confidence: 74%

“…This idea was explored more formally by Pough (10) and again more recently by Janzen et al (4), who updated and expanded this hypothesis, arguing that the aversion to eye-or facelike stimuli is likely innate. Subsequent work has now empirically confirmed the protective value of eyespots for caterpillars (11,12), and has shown that the mimetic fidelity of many caterpillars with eyespots to dangerous snakes increases when they adopt their defensive posture (13). Although some research has questioned the degree to which eyespots confer protection through eye mimicry in adult Lepidoptera (14,15), other work has convincingly supported the original hypothesis of eye mimicry (16)(17)(18); however, there remain fundamental gaps in our understanding of the function and evolution of eyespots.…”

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confidence: 97%

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Body size affects the evolution of eyespots in caterpillars

Hossie

Stachurski

Breinholt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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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

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“…great tits (Parus major), Rowland et al 2007;starlings (Sturnus vulgaris), Halpin et al 2013) or, when wild birds have been used in a natural setting, experimental manipulation of artificial prey has varied prey appearance in a way that does not reflect natural variation (Cuthill et al 2005). However, the use of ecologically valid manipulations of artificial prey with birds foraging in a natural environment has provided great insights into the evolution of caterpillar eyespots (Hossie and Sherratt 2012;Hossie and Sherratt 2013), and other studies would benefit from adopting such an approach. An example of such a study that is much needed involves the manipulation of stripe number (mimetic fidelity) and prey size (profitability) using realistic ranges of each parameter to validate the relaxed selection hypothesis (where smaller prey are under weaker selection due to reduced profitability) that was supported by Penney et al's (2012) comparative analysis.…”

Section: Discussionmentioning

confidence: 99%

Field estimates of survival do not reflect ratings of mimetic similarity in wasp-mimicking hover flies

Easley

Hassall

2013

Evol Ecol

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The evolution of mimicry, and particularly the persistence of undefended Batesian mimetic forms that are imperfect copies of their defended models, remains a central question in evolutionary biology. Previous work has demonstrated that variation in mimetic fidelity in artificial prey can alter survival. However, no studies have validated the assumption that detailed laboratory-based measurements of mimetic fidelity are actually reflected in survival in natural field experiments. Here, we demonstrate that, in line with previous studies, the mimetic similarity of 77 hover fly (Diptera: Syrphidae) species to the common wasp Vespula alascensis is strongly related to the number of abdominal stripes exhibited by the flies. We then produce three artificial pastry baits: (i) a "model" which is chemically defended and has two stripes, (ii) a one-stripe mimic, and (iii) an unstriped mimic. Based on the ratings study, we predicted that the one-stripe mimic would exhibit survival intermediate between the unstriped mimic and the model. Baits were deployed in experiments each involving 81 baits (27 of each kind), at 3 sites, with experiments replicated 10 times at each site for a total deployment of 2430 baits. Proportional hazards models show that both one-striped and model baits survived equally well and significantly better than the unstriped baits, suggesting categorical prey identification rather than the use of stripe number as a continuous trait, as was suggested by the laboratory study. These findings suggests that, while humans and avian predators can distinguish mimics and models in the laboratory using a range of traits, behaviour in the field may not reflect this ability. This absence of a link between continuous measures of mimetic fidelity and prey selection may contribute to the maintenance of imperfect mimicry, but more studies using near-natural experimental paradigms are needed to investigate the phenomenon further.

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Defensive posture and eyespots deter avian predators from attacking caterpillar models

Cited by 55 publications

References 17 publications

Why many Batesian mimics are inaccurate: evidence from hoverfly colour patterns

Why many Batesian mimics are inaccurate: evidence from hoverfly colour patterns

Body size affects the evolution of eyespots in caterpillars

Field estimates of survival do not reflect ratings of mimetic similarity in wasp-mimicking hover flies

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