Mimicry, Signalling and Coevolution

Ethology COMMENTARY Perspectives and Debates: Mimicry, Signalling and Co-Evolution (Commentary on Wolfgang Wickler – Understanding Mimicry – With special reference to vocal mimicry) Tomas Grim Department of Zoology and Laboratory of Ornithology, Palacky University, Olomouc, Czech Republic Correspondence Abstract Toma´ sˇ Grim, Department of Zoology and Laboratory of Ornithology, Palacky´ In his stimulating discussion, Wolfgang Wickler criticizes fuzzy usage of University, trˇ. 17. listopadu 50, CZ-771 46 term mimicry by drawing attention to its original definition by H. Bates. Olomouc, Czech Republic. Mimicry refers to functional ‘model–mimic–selecting agent’ trinity (with E-mail: [email protected] varying number of species involved) when the selecting agent (i.e. signal receiver) responds similarly to mimic and model to the advantage of the Received: January 16, 2013 mimic. Concurring with Wickler I argue that convergence is neither nec- Initial acceptance: January 16, 2013 essary nor sufficient to support similarity as evidence for mimicry and that Final acceptance: January 19, 2013 it is artificial and unproductive to classify mimicry with respect to ontog- (M. Hauber) eny (innate vs. learned similarity) or model species identity (learning from doi: 10.1111/eth.12067 conspecifics vs. heterospecifics). Using butterfly ‘eye’-spots, I argue that just identifying each of the supposed model, the mimic and the selective agent, and even demonstrating that mimic-model similarity affects the agent’s behaviour, provides no conclusive evidence for mimicry. Even a demonstration that the mimic benefits from receiver response may not provide conclusive evidence for mimicry. Using avian brood parasite–host egg and nestling mimicry, I emphasize that without experimental manip- ulation of the hypothesized mimetic traits, it is impossible to test the mimicry hypothesis robustly. Due to fundamental constraints on human perception, some cases of mimicry may in fact be just a by-product of human inability to perceive relevant differences between animal pheno- types (what is similar for human eye, nose or ear may not be viewed, smelled or heard as similar for relevant animal observers), whereas many cases of real mimicry may escape our attention from the same reason (‘hidden’ mimicry). Surprisingly, the same mimetic phenotype may show completely different effects on selective agents under different ecological circumstances. Finally, relatively dissimilar species may be more mimetic than highly similar model–mimic pairs because mimicry may be more fruitfully understood as a co-evolutionary process rather than a similarity. Terms like ‘mimicry’, ‘mimesis’, ‘mimetism’, ‘mas- particular terms, the science is doomed to fail (imag- querade’, ‘crypsis’ and ‘camouflage’ are often used ine that my understanding of what constitutes an with different or even contradictory meanings in the ‘adaptation’ would not match your opinion; then literature (no specific references needed – this issue citing my work as an evidence for adaptation in your becomes obvious after reading a dozen of randomly work would be meaningless; see Williams 1966). chosen articles or books that use those terms). This At the same time, such debates also cannot, in confuses students and researchers alike. Therefore, principle, be concluded to everyone’s satisfaction discussions about definition of terms, like the because criteria underlying particular definitions are stimulating contribution by Wickler (2013), are essen- inevitably (partly) subjective. Just like a scientific tial – without shared opinions on what we mean by (‘Latin’) genus name may refer to two completely 270 Ethology 119 (2013) 270–277 © 2013 Blackwell Verlag GmbH T. Grim Mimicry, Signalling and Co-Evolution different organisms (Arenaria both flies in the air and The additional argument is that taxonomy is a photosynthesizes on land – depending on whether meaningless factor in assessing mimicry, and this fol- you are a zoologist or a botanist) also a term may lows from two simple patterns: (1) any two biological refer to two completely different meanings; for species show some kind of similarity at least in some example, ‘adaptation’ in evolutionary and behaviour- trait. This directly follows from Darwin’s notion of a al biology is a very different thing from ‘adaptation’ single origin of life followed by ‘descent with modifi- in physiology and neuroscience (or, for that matter, cation’. Therefore; (2) similarity is not discrete; simi- in the literature and film-making). Obviously, a similarity is a phenomenon of continuity. lar phenomenon may work not only between different fields of sciences but also within a particular Proximate vs. Ultimate Perspective branch of science; a behavioural ecologist would favour a functionally based definition (‘mimicry is Wickler views mimicry from the selective agent’s per- primarily deception, everything else is not important spective. According to him, the origin of similarity for definition of mimicry’), whereas a taxonomist does not matter – it can be but need not be a conver- may privilege a phylogenetically based definition gence. For him, mimicry is primarily a perceptual (‘mimicry is convergence, everything else is not phenomenon. important for definition of mimicry’). Just as the In contrast, in my own area of research (avian brood results may be determined by methods of investiga- parasitism), mimicry is viewed strictly as the most deci- tion (Grim 2005a) or analyses (e.g. Trnka et al. sive evidence for co-evolution between brood parasite 2012), criteria determine definitions. In the end, it is and its host, although there is also the possibility of our own decision how we classify and define natural unilateral ‘advergence’ of the mimic to the model phenomena; the devil lies, among other things, in (Mallet 1999; Hauber & Kilner 2007), that is, ‘sequen- the fact that natural phenomena are mostly continu- tial evolution mimicry’ (Grim 2005b). The origin of ous, whereas definitions and terminological labels similarity is critical for judging it as mimetic similarity; are necessarily categorical (Grim 2005b). mimicry refers solely to cases when similarity evolved Keeping the above-mentioned qualifications in specifically due to discrimination by host of parasite eggs mind, it is still important to discuss what we mean by (Stoddard & Stevens 2012), chicks (Langmore et al. particular terms (e.g. Vane-Wright 1976, 1980). 2011) and adults (Welbergen & Davies 2011). Here, Sometimes it helps to return to original definitions, mimicry is primarily an evolutionary phenomenon. before the terms in question got misused and mud- Thus, some researchers may approach mimicry dled in the literature. This is why W. Wickler went from a primarily proximate (mechanistic, perceptual) back to H. Bates who mixed the functional concept side, whereas others approach the same phenomenon of mimicry with convergent evolutionary process, from a primarily ultimate (natural selection, evolu- thus setting the stage for future confusions. Here, tion) side. Before entering a heated discussion about I am going to provide both specific comments on which of these views is more useful, it is important to W. Wickler’s opinions and additional ruminations on remember that this opinion discrepancy might simply mimicry imbroglios. follow from well-known general research traditions – Being a behavioural ecologist, I agree that it is use- throughout the 20th century, continental ‘German’ ful to keep to the functional definition of mimicry. science was more descriptive and proximate, while The key point, following from the fact that it is the insular ‘English’ and ‘New World’ science was more signal receiver who brings mimicry into existence, is that experimental and ultimate (see, e.g., works of Konrad ‘The natural selecting agent is deceived not because Lorenz vs. Nikolaas Tinbergen). key markings converge but because a stimulus and its This leads in some cases (but not all cases, of course) meaning to the signal perceiver diverge.’ (Wickler to opposing interpretations of similarities we observe 2013). This automatically means that ‘the question of in nature. Whydahs and indigobirds (Vidua spp.) para- analogous versus homologous, and of interspecific sitize African estrildid finches. If an estrild host tries to versus intraspecific, resemblance between model and reject parasitism at the egg stage, it has little chance to mimic is irrelevant for deceptive mimicry to function’ do so – both its and parasite eggs are purely white and (Wickler 2013). Clearly, signal receiver simply similarly sized; thus, there are few reliable signatures responds to particular stimuli irrespective of their ori- that could underlie host discrimination decisions. gin (innate/learned, homologous/convergent, etc.; From the Wicklerian point of view, this is mimicry: see below). Definition and classification of mimicry the selective agent (host) is perceptually confused by should respect this biological reality. the resemblance between its own eggs (model) and Ethology 119 (2013) 270–277 © 2013 Blackwell Verlag GmbH 271 Mimicry, Signalling and Co-Evolution T. Grim parasite eggs (mimic). This forces hosts to accept the Signal is defined as ‘an act or structure that alters egg and benefits the parasite mimic (the latter being a the behaviour of another organism, which evolved necessary condition for mimicry to occur). From the because of that effect and which is effective because brood parasitism researcher’s point of view, this is not the receiver’s response has also evolved’

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