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The Coevolution of Toucan and Kiskadee Mimicry

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The Coevolution of Toucan and Kiskadee Mimicry vol. 187, no. 6 the american naturalist june 2016 Mimicry Cycles, Traps, and Chains: The Coevolution of Toucan and Kiskadee Mimicry Richard O. Prum1,* and Larry Samuelson2 1. Department of Ecology and Evolutionary Biology, Yale University, 21 Sachem Street, New Haven, Connecticut 06520; 2. Department of Economics, Yale University, 30 Hillhouse Avenue, New Haven, Connecticut 06520 Submitted May 31, 2015; Accepted October 6, 2015; Electronically published April 6, 2016 Online enhancements: appendix. fi abstract: Interspecific social dominance mimicry (ISDM) is a form 2014). Speci cally, Prum and Samuelson (2012) analyzed a of social parasitism in which a subordinate species evolves to mimic new two-species, four-strategy variation of the classic hawk- and deceive a dominant interference competitor in order to avoid dove game to explore the evolutionary dynamics of ISDM. attack by the dominant species. ISDM has been proposed to result Named after the proposed example of ISDM between the in (1) antagonistic coevolutionary arms races in appearance between dominant hairy and subordinate downy woodpeckers (Pi- the model and the mimic (e.g., Ramphastos toucans) and (2) the evo- coides villosus and Picoides pubescens, respectively), the hairy- lution of complexes of multiple species converging on a common vi- downy game explored the evolutionary equilibria and dy- sual appearance (e.g., kiskadee flycatchers). We present evolutionary games of antagonistic coevolution in appearance between pairs and namics of ISDM between species involved in interference triplets of sympatric species under interference competition. We iden- competition for codistributed resources. The game estab- tify conditions for the existence and stability of (1) coevolutionary lished the evolutionary plausibility of this mimicry mecha- mimicry cycles in appearance between evader and pursuer strategies nism and made both quantitative and qualitative predictions of models and mimics, (2) mimicry chains in which three or more spe- about the process. cies are coevolutionarily entrained to evolve a single common appear- Subsequently, Prum (2014) surveyed likely examples of fi ance despite differences in their costs and bene ts, and (3) mimicry ISDM in birds. Prum proposed 50 phylogenetically inde- traps in which a subdominant species is evolutionarily constrained from evading mimicry by a third, subordinate mimic species. Mimicry pendent examples involving 60 model and 93 mimic species cycles will result in the evolutionary divergence of models and mimics from all across the diversity of birds. On the basis of the un- from their ancestral phenotypes. The hierarchical evolutionary dy- usual phylogenetic patterns of covariation in appearance be- namics of ISDM traps and chains resemble Müllerian mimicry with tween clades of model and mimic species, Prum (2014) made variable costs to toxicity. several distinct coevolutionary predictions. fi Keywords: mimicry, social dominance mimicry, interspecificsocial First, because ISDM produces negative effects on the t- dominance mimicry (ISDM). ness of the model species, models should come under natural selection to diverge in appearance from their socially para- sitic mimics (Prum 2014). Likewise, as models evolve to be Introduction more dissimilar in appearance, mimic species will come un- der natural selection to maintain deceptive similarity to the Interspecific mimicry can evolve through natural selection as model. Thus, ISDM is predicted to result in antagonistic co- a means for mimics to avoid attack (Wickler 1968; Ruxton evolution in appearance among models and mimics (Prum et al. 2004). Commonly, interspecific mimicry functions as 2014). This process will lead to codivergence in appearance a form of communication to a third, nonmodel species, such of both species from their ancestral phenotypes. Further- as a predator. In recent articles, we have proposed a form of more, if geographic isolation or speciation occurs among interspecific social dominance mimicry (ISDM) in which a populations of sympatric models and mimics, then ISDM subordinate species evolves to mimic the visual appearance may foster coevolutionary radiation among multiple popu- of a dominant species in order to fare better in interactions lations or species within model and mimic clades. Prum with the dominant species (Prum and Samuelson 2012; Prum (2014) proposed multiple examples of this coevolutionary phenomenon, including the yelping model and croaking mi- fi * Corresponding author; e-mail: [email protected]. metic clades of Ramphastos toucans (Ramphastidae; g. 1) Am. Nat. 2016. Vol. 187, pp. 753–764. q 2016 by The University of Chicago. and others. 0003-0147/2016/18706-56293$15.00. All rights reserved. Second, Prum (2014) proposed that an intermediate-sized DOI: 10.1086/686093 mimic of a larger, dominant model species may be con- 754 The American Naturalist A B C D Figure 1: Examples of coevolutionary radiation between mimic and model clades of Ramphastos toucans (Ramphastidae). Larger model species from the yelping clade are on the left, and smaller mimic species from the croaking clade are on the right. A, B, Chestnut-mandibled toucan Ramphastos swainsoni model (A) and choco toucan Ramphastos brevis mimic (B). C, D, Red-billed toucan Ramphastos tucanus tucanus model (C) and channel-billed toucan Ramphastos vitellinus culminatus mimic (D). Mimic species are 55%–58% of the body mass of their sympatric models (Prum 2014). Photo credits: A–C, Nick Athanas (Prum 2014); D, Flickr users Roy and Danielle (CC BY 2.0; https:// creativecommons.org/licenses/by/2.0/). strained from evading mimicry by a third, even smaller, so- vergence in plumage among nine or more species from five cially subordinate species because the intermediate-sized genera of the kiskadee-type flycatchers (Tyrannidae; fig. 2). mimic may be under simultaneous natural selection to main- Recently, Benz et al. (2015) established a new and unex- tain the deceptive similarity to their larger, dominant model pected mimicry complex in Neotropical woodpeckers. In species. Because of this evolutionary constraint, mimics may southeastern South America live three species of black, be especially vulnerable candidates for deceptive social mim- white, and red woodpeckers—the robust woodpecker (Cam- icry by even smaller species. Accordingly, ISDM may create pephilus robustus), the lineated woodpecker (Dryocopus line- mimetic convergence among multiple sympatric species in atus), and the helmeted woodpecker (Dryocopus galeatus). a guild of ecological competitors. The result would be the co- Benz and colleagues discovered that the species galeatus is evolutionary entrainment of multiple species into a quasi- not related to other Dryocopus but is embedded within the Müllerian mimicry complex of species with a broad range Neotropical woodpecker genus Celeus (i.e., it is Celeus ga- of body sizes. Prum (2014) proposed several dramatic exam- leatus). Although Prum (2014) proposed a Ramphastos-like ples of mimicry complexes, for example, the rampant con- mimicry radiation between model Campephilus and mimic Mimicry Cycles, Traps, and Chains 755 A B ference competition. We identify the evolutionary condi- tions for the existence and stability of (1) antagonistic co- evolutionary mimicry cycles in appearance between model and mimic species, (2) mimicry chains in which three or more species are coevolutionarily entrained to evolve a sin- gle common appearance despite their interspecific differ- ences in costs and benefits, and (3) mimicry traps in which a subdominant mimic species is evolutionarily constrained from evading mimicry by a third, subordinate mimic species. We conclude with a discussion of how to test the assump- C D tions and predictions of these ISDM models in the wild. When introducing the idea of ISDM, Prum and Sam- uelson (2012) studied the contest for resources in the dom- inant species as a hawk/dove game while assuming that members of the subordinate species split the resource equally in any encounter. Here, we simplify the analysis by assuming that members of the dominant species also simply split the re- source equally. E F A Two-Species Community without Mimicry Our point of departure is a study of an ecological and evolu- tionary interaction between two species, a dominant spe- cies 1 and a subordinate species 2, that engage in direct inter- ference competition for codistributed ecological resources. Pairs of individuals engage in interactions that determine how a resource is to be split between them. The fitness out- comes of such an interaction depend on whether both in- dividuals are from species 1, both are from species 2, or Figure 2: Examples of a mimicry complex among Neotropical kiskadee- one is from each species, and they are given in table 1. Var- fi type flycatchers (Tyrannidae). A, Boat-billed flycatcher Megarhynchus iables z1 and z2 are the background tnesses of the two spe- pitangua (73 g). B, Great kiskadee Pitangus sulphuratus (61 g). C,Rusty- cies. Background fitnessreferstothefitness implications margined flycatcher Myiozetetes cayannensis (25.9 g). D, Social fly- of all activities other than interactions with the other spe- catcher Myiozetetes similis (28 g). E, Lesser kiskadee Philohydor lictor fl cies. When two individuals of species 1 interact, they split (25.5 g). F, White-throated ycatcher Phelpsia inornata (29.4 g). Photo fi credits: A, http://www.1000birds.com/reports_CR_Boat-billed-Flycatcher theresource in question, which confers an additional tness 1 .htm, by Nick Kontonicolas/www.1000birds.com; B, Nick Anthanas of x1 0 on each of them. When two individuals of species 2 (Prum 2014); C, q T. J. Ulrich/VIREO; D, q G. Lasley/VIREO; E, interact, they also split the resource, which confers an addi- q G. Bartley/VIREO; F, q T. Friedel/VIREO. fi 1 tional tness of x2 0 on each of them. Species 1 is socially dominant. Hence, when an individual of species 1 encoun- ters an individual of species 2, the former takes all of the re- fi source, resulting in a tness increment of 2x1 for the individ- Dryocopus species, Benz and colleagues discovered that these ual of species 1 and a fitness increment of 0 for the individual southeastern South American species constitute a new ex- of species 2.
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