Does Müllerian Mimicry Work in Nature? Experiments with Butterflies and Birds (Tyrannidae)1

Pinheiro, Carlos E. G.

doi:10.1646/02128

Cited by 30 publications

(44 citation statements)

References 36 publications

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“…Experimental field and laboratory studies confirmed the importance of predator learning and experience for recognition of mimetic species (e.g. Chai 1996;Pinheiro 2003;Langham 2006) and brought extensive support for the hypothesis that bird predators are important agents in selection for mimicry and maintenance of spatial colour polymorphism in butterflies (Brower et al 1963;Bullini et al 1969;Coppinger 1970;Mallet & Barton 1989;Kapan 2001;Pinheiro 2003;Langham 2004). Experimental studies also revealed an importance of other traits in addition to coloration (shape and flight pattern) for recognition of the mimetic butterfly species by specialized bird predators (Chai & Srygley 1990;Chai 1996).…”

Section: Introductionmentioning

confidence: 77%

“…Experimental field and laboratory studies confirmed the importance of predator learning and experience for recognition of mimetic species (e.g. Chai ; Pinheiro ; Langham ) and brought extensive support for the hypothesis that bird predators are important agents in selection for mimicry and maintenance of spatial colour polymorphism in butterflies (Brower et al. ; Bullini et al.…”

Section: Introductionmentioning

confidence: 81%

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How Do Predators Learn to Recognize a Mimetic Complex: Experiments with Naive Great Tits and Aposematic Heteroptera

et al. 2013

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We tested the importance of innate wariness, avoidance learning, memory and generalization for the formation of predatory behaviour in naive great tits (Parus major) towards mimetic complex of four aposematic species of true bugs (Insecta: Hemiptera: Heteroptera): Lygaeus equestris, Spilostethus saxatilis, Pyrrhocoris apterus and Graphosoma lineatum. The birds showed almost no innate wariness against the aposematically coloured bugs, although a hidden wariness elicited by defensive chemicals of some of the bug species is not excluded. Naive birds learned to avoid different species at different rates, which resulted in different prey mortalities. The avoidance learning was faster when the defensive chemicals produced an immediate irritating effect (particularly when squirted into distance – G. lineatum) than when they caused sickness several minutes after the consumption (P. apterus). The experience of birds from learning to avoid a particular species of bug affected their subsequent behaviour to other species – experience with better‐defended species resulted in longer attack latencies, more cautious attacks, broader generalization and lower prey mortality. The least defended species, P. apterus, benefited from the experience of birds with better‐defended species, whereas the birds' experience with P. apterus did not reduce mortality risk of the other species comparably. Judging from the inexperienced young birds, the mimetic relationships are likely to be quasi‐Batesian. However, as wild‐caught great tits avoid all the four species to the same extent, the relationships may become more mutualistic (quasi‐Müllerian) in later phases of learning under natural conditions. The relationships among species in the mimetic complex thus seem to depend on the amount of experience of the bird predators.

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Section: Introductionmentioning

confidence: 77%

Section: Introductionmentioning

confidence: 81%

How Do Predators Learn to Recognize a Mimetic Complex: Experiments with Naive Great Tits and Aposematic Heteroptera

et al. 2013

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“…However, behavioural experiments studying the possible effects after consumption, probably involved in the learning of a warning signal as aposematic, might show that minute differences in cyanide concentration are relevant. Short- and long-time effects of chemicals on birds are important to test given that some natural predators have been reported to feed on Heliconius butterflies, such as tropical kingbirds ( Tyrannus melancholicus ) [70]. Furthermore, long-time dose effects of chemicals have been predicted to affect mimicry dynamics by determining the number of attacks needed for predators to learn and avoid a given warning signal [71, 72].…”

Section: Discussionmentioning

confidence: 99%

Variation in cyanogenic compounds concentration within a Heliconius butterfly community: does mimicry explain everything?

et al. 2016

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BackgroundAposematic species advertise their unpalatability using warning signals such as striking coloration. Given that predators need to sample aposematic prey to learn that they are unprofitable, prey with similar warning signals share the cost of predator learning. This reduction in predation risk drives evolutionary convergence of warning signals among chemically defended prey (Müllerian mimicry). Whether such warning signal convergence is associated to similar defence levels among co-mimics is still an open question that has rarely been tested in wild populations. We quantified variation in cyanide-based (CN) chemical protection in wild caught individuals of eight aposematic Heliconius butterfly species belonging to four sympatric mimicry rings. We then tested for correlations between chemical protection and ecological species-specific traits.ResultsWe report significant differences in CN concentrations both within and between sympatric species, even when accounting for the phylogeny, and within and between mimicry rings, even after considering inter-specific variation. We found significant correlations between CN concentration and both hostplant specialization and gregarious behaviour in adults and larvae. However, differences in CN concentrations were not significantly linked to mimicry ring abundance, although the two most toxic species did belong to the rarest mimicry ring.ConclusionsOur results suggest that mimicry can explain the variation in the levels of chemical defence to a certain extent, although other ecological factors are also relevant to the evolution of such variability.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0843-5) contains supplementary material, which is available to authorized users.

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“…Both H. erato and H. melpomene are unpalatable and have wing colour patterns that deter potential predators [9], [17], [18]. Across the Americas, each of these two species exhibits approximately 30 warning pattern morphs [3].…”

Section: Introductionmentioning

confidence: 99%

Phylogenetic Codivergence Supports Coevolution of Mimetic Heliconius Butterflies

Cuthill

Charleston

2012

PLoS ONE

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The unpalatable and warning-patterned butterflies Heliconius erato and Heliconius melpomene provide the best studied example of mutualistic Müllerian mimicry, thought–but rarely demonstrated–to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of H. erato and H. melpomene, and this was initially hailed as one of the most striking known cases of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of H. erato and H. melpomene, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of H. erato and H. melpomene. Cophylogenetic historical reconstructions support repeated codivergence of mimetic populations, from the base of the sampled radiations. Pairwise distance correlation tests, based on our coalescent analyses plus recently published AFLP and wing colour pattern gene data, also suggest that the phylogenies of H. erato and H. melpomene show significant topological congruence. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of H. erato and H. melpomene occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. Our results suggest that differences in within-species genetic divergence are the result of a greater overall effective population size for H. erato relative to H. melpomene and do not imply incongruence in the timing of their phylogenetic radiations. Repeated codivergence between Müllerian co-mimics, predicted to exert mutual selection pressures, strongly suggests coevolution. Our results therefore support a history of reciprocal coevolution between Müllerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change.

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Does Müllerian Mimicry Work in Nature? Experiments with Butterflies and Birds (Tyrannidae)1

Cited by 30 publications

References 36 publications

How Do Predators Learn to Recognize a Mimetic Complex: Experiments with Naive Great Tits and Aposematic Heteroptera

How Do Predators Learn to Recognize a Mimetic Complex: Experiments with Naive Great Tits and Aposematic Heteroptera

Variation in cyanogenic compounds concentration within a Heliconius butterfly community: does mimicry explain everything?

Phylogenetic Codivergence Supports Coevolution of Mimetic Heliconius Butterflies

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