Diversity in Müllerian mimicry: The optimal predator sampling strategy explains both local and regional polymorphism in prey

Aubier, Thomas G.; Sherratt, Thomas N.

doi:10.1111/evo.12790

Cited by 39 publications

(46 citation statements)

References 83 publications

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“…The incorporation of some of this complexity in predator behaviour into models, e.g. optimal predator sampling strategies based on exploration-exploitation trade-offs (Sherratt, 2011), has started to close the gap between theory and empirical examples resulting in scenarios where warning colour variation is predicted to arise within and among species (Aubier & Sherratt, 2015;Kikuchi & Sherratt, 2015).…”

Section: Theorymentioning

confidence: 99%

Diversity in warning coloration: selective paradox or the norm?

et al. 2018

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Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency‐dependent learning. However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population. Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals. Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal. The mechanisms producing warning coloration are also important. Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation. Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator–prey interactions. Predator variability in a range of factors (e.g. perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated. With complex selection regimes at work, polytypisms and polymorphisms may even occur in Müllerian mimicry systems. Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures. Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore. As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species. Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research. A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once‐paradoxical phenomenon, yields a new perspective for the field of aposematic signalling.

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Section: Theorymentioning

confidence: 99%

Diversity in warning coloration: selective paradox or the norm?

et al. 2018

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“…Another possibility 95 is that a model in which predators only learn to avoid unpalatable prey only after sampling a 96 fixed number is overly simplistic. Specifically, if predators are neophobic and generally avoid 97 prey with unfamiliar phenotypes, novel signaling phenotypes might be favoured when they 98 are rare (Aubier and Sherratt 2015). Here we propose an additional factor that may contribute 99 to the origin of novel warning patterns -specifically, that females may benefit from 100 uncommon wing patterns because they will lead to reduced harassment by males, which use 101 colour pattern as a mating cue.…”

Section: Introduction 35mentioning

confidence: 87%

Experimental manipulation ofHeliconiuswarning patterns reduces harassment of previously mated females

Merrill

Neggazi²,

Morrison³

et al. 2018

Preprint

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9Why warning patterns are so diverse is an enduring evolutionary problem. Because predators 10 learn to associate particular patterns with unpleasant experiences, an individual's risk of 11 predation should decrease as the local density of its warning pattern increases. Heliconius 12 butterflies, however, are known for their diversity of warning patterns, and the establishment 13 of entirely new phenotypes is difficult to explain under strict frequency-dependent selection. 14 One possibility is that during periods of relaxed selection, drift may allow new variants to rise 15 above a threshold density until mimicry selection takes over. We propose an alternative 16 hypothesis where novel pattern phenotypes arise due to a conflict of interests between the 17 sexes. It is well established that male Heliconius use warning patterns as a mating cue. This 18 will likely be beneficial to males as it will increase the efficiency of finding mates. However, 19 already mated females may suffer fitness costs if these cues lead to harassment by males 20 during oviposition or foraging. When constraints imposed by predation are locally relaxed, 21 this could lead to rapid divergence in pattern phenotypes through chase-away sexual 22 selection. To begin to test this hypothesis, we experimentally manipulated the warning 23 patterns of mated Heliconius erato demaphoon females and recorded their interactions with 24 conspecific males, and the effect of male presence on laying rate. As predicted, males 25 interacted less with mated females whose red forewing band was blacked-out, as compared to 26 control females whose warning pattern remained intact. We also show that females lay less 27 eggs in the presence of males, but we were unable to detect a significant interaction between 28 warning pattern treatment and the presence of males on female fecundity. Our results suggest 29 that male attraction to conspecific warning patterns, may impose a previously unrecognized 30 cost on Heliconius females. 31 32

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“…Potential processes preventing mimicry might include ecological differences across space, high levels of maladaptive gene flow and the stability of co-distributions among taxa. Because predators are the selective force maintaining mimicry [18], shifts in predator communities across regions might change the selective landscape for mimicry causing strong selection for colour convergence in some areas versus weak selection for colour convergence in others [5]. Alternatively, positive frequency-dependent selection on similarly abundant aposematic morphs [19], or microhabitat partitioning of mimicry patterns to exploit different predator assemblages [20] could also preclude selection for convergence.…”

Section: (A) Potential Insights On Mimicry From Ceroglossus Beetlesmentioning

confidence: 99%

“…The taxa are widely co-distributed and characterized by high intraspecific variation ( [5]; figure 1). In addition, some striking covariation in elytral coloration has been noted among co-occurring species [7].…”

Section: Introductionmentioning

confidence: 99%

Mimics here and there, but not everywhere: Müllerian mimicry inCeroglossusground beetles?

et al. 2016

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The ground beetle genus Ceroglossus contains co-distributed species that show pronounced intraspecific diversity in the form of geographical colour morphs. While colour morphs among different species appear to match in some geographical regions, in others, there is little apparent colour matching. Mimicry is a potential explanation for covariation in colour patterns, but it is not clear whether the degree of sympatric colour matching is higher than expected by chance given the obvious mismatches among morphs in some regions. Here, we used reflectance spectrometry to quantify elytral coloration from the perspective of an avian predator to test whether colour similarity between species is, indeed, higher in sympatry. After finding no significant phylogenetic signal in the colour data, analyses showed strong statistical support for sympatric colour similarity between species despite the apparent lack of colour matching in some areas. We hypothesize Mü llerian mimicry as the responsible mechanism for sympatric colour similarity in Ceroglossus and discuss potential explanations and future directions to elucidate why mimicry has not developed similar levels of interspecific colour resemblance across space.

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Diversity in Müllerian mimicry: The optimal predator sampling strategy explains both local and regional polymorphism in prey

Cited by 39 publications

References 83 publications

Diversity in warning coloration: selective paradox or the norm?

Diversity in warning coloration: selective paradox or the norm?

Experimental manipulation ofHeliconiuswarning patterns reduces harassment of previously mated females

Mimics here and there, but not everywhere: Müllerian mimicry inCeroglossusground beetles?

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