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Mimicry: Ecology, Evolution, and Development Editorial Mimicry: Ecology, evolution, and development David PFENNIG, Guest Editor Department of Biology, University of North Carolina, Coker Hall, CB#3280, Chapel Hill, NC 27599 USA, [email protected] 1 Introduction 1879), multiple undesirable species (e.g., toxic species) converge on the same warning signal, thereby sharing Mimicry occurs when one species (the “mimic”) the cost of educating predators about their undesirabil- evolves to resemble a second species (the “model”) be- ity. cause of the selective benefits associated with confusing Mimicry is among the most active research areas in a third species (the “receiver”). For example, natural all of evolutionary biology, in part because of the highly selection can favor phenotypic convergence between integrative nature that the study of mimicry necessarily completely unrelated species when an edible species entails. Mimicry involves asking both functional ques- receives the benefit of reduced predation by resembling tions (it involves investigating, for example, the adap- an inedible species that predators avoid. tive significance of more versus less precise resem- Research into mimicry has a rich history that traces blance between models and mimics) and mechanistic back to the beginnings of modern evolutionary biology. ones (it also involves investigating, for example, how In 1862––a scant three years after Darwin had published mimetic phenotypes are produced). Thus, mimicry re- The Origin of Species––Henry Walter Bates (1862), an search draws on diverse fields, many of which are on English explorer and naturalist, first suggested that close the cutting edge of biological research. Indeed, as Bro- resemblances between unrelated species could evolve as die and Brodie (2004, p. 617) note, the study of mimicry an anti-predator adaptation. Upon reading his paper, could be used to illustrate virtually every major concept Darwin immediately wrote to Bates that, “In my opinion in a modern evolutionary biology course. it is one of the most remarkable & admirable papers I This special column of Current Zoology presents a ever read in my life. ... You have most clearly stated and range of original research and review papers, covering solved a wonderful problem” (read the full letter at: the ecology, evolution, and development of mimicry. http://www.darwinproject.ac.uk/entry-3816). Even today, Clearly, a complete discussion of mimicry is beyond the mimicry is widely used as a testament to natural selec- scope of a single journal issue. Nevertheless, these pa- tion’s efficacy in promoting complex adaptation (Cott pers offer a flavor of ongoing work. 1940; Edmunds 1974; Brodie and Brodie 2004; Ruxton Below, I briefly outline some key questions in mim- et al. 2004; Turner 2005; Forbes 2009). icry research before highlighting how the contributions Although many types of mimicry have now been de- of this special column address these questions. scribed, the most familiar type is “protective” or “de- fensive” mimicry. Defensive mimicry occurs when one 2 Key Questions in Mimicry Research species receives protection from predation because of its There are many key questions that researchers of close resemblance to a second, already protected species mimicry currently investigate. Here, I highlight five (for a discussion of other types of mimicry, see questions that have been particularly fruitful areas of Vane-Wright 1976; Vane-Wright 1980; Endler 1981; research. Pasteur 1982; Malcolm 1990; Rainey and Grether 2007). First, what proximate mechanisms underpin mimicry? There are two common forms of defensive mimicry: Specifically, what are the genetic and developmental Batesian and Müllerian mimicry (Wickler 1968; Pasteur mechanisms that produce mimetic phenotypes? An- 1982). With Batesian mimicry (named after H. W. Bates; swering this question is important, because particular see above), an edible species evolves to resemble a proximate mechanisms might facilitate or impede the conspicuous, inedible species, thereby gaining protec- evolution of mimicry. For instance, when models and tion from predation. With Müllerian mimicry (Müller mimics share mechanisms of signal production, mimi- 604 Current Zoology Vol. 58 No. 4 cry may evolve relatively easily, as a small number of that imperfect mimics represents a trade-off between mutations may be needed for the mimic to match the predator-mediated selection favoring mimetic conver- phenotype of its model (Leimar et al., 2012). Despite gence on the one hand and other agents of selection the importance of mechanisms in influencing the ease (such as mate choice) favoring divergence on the other with which mimicry evolves, little is known about how hand (Pfennig and Kikuchi, 2012a). Moreover, there models and mimics produce their phenotypes [with the may be little selective benefit to refine mimetic resem- possible exception of recent research involving mimetic blance beyond a certain point, if (for example) the butterflies in the genus Heliconius (Reed et al., 2011)]. model/co-mimic is common or especially noxious Second, what role does receiver “psychology” play in (Schmidt, 1958; Duncan and Sheppard, 1963; Sherratt, the evolution of mimicry? Receivers (e.g., predators, in 2002; Harper and Pfennig, 2007), or if the mimic is the case of defensive mimicry) are the agents that gen- likely to be especially unprofitable to predators (Sherratt, erate the selective pressures that drive the evolution of 2002). For instance, because larger prey are generally mimicry. Thus, understanding how receivers detect and more profitable for predators, there should be greater respond to signals produced by mimics is crucial for selection pressure on larger individuals in a population illuminating the evolution of mimicry. For instance, for to become better mimics than on their smaller counter- effective mimicry to evolve, how important is it for parts, a prediction recently confirmed in hoverflies predators to perceive signals emanating from mimics (Penney et al., 2012). and models simultaneously versus consecutively? Fifth, what is mimicry’s role in speciation and diver- Third, how does Müllerian mimicry generate poly- sification? As with other forms of strong ecologically morphism among mimics? Longstanding theory based selection, mimicry has long been regarded as a (reviewed in Sherratt 2008), along with field empirical factor that can contribute to speciation and adaptive tests (Kapan, 2001), demonstrate that Müllerian mimi- radiation. For instance, because mimicry is often ex- cry should favor co-mimics that share the same signal, pected to generate strong frequency dependent selection, thereby precluding the origin and maintenance of poly- it should tend to act as a strong agent that selects against morphism in these mimetic signals. Yet, considerable hybrid individuals; that is, it should select against those polymorphism has been found in many Müllerian mimi- individuals that possess phenotypes that are intermedi- cry complexes (reviewed in Joron and Mallet 1998), ate between cryptic and mimetic phenotypes. In this including in millipedes (Marek and Bond, 2009), octopi way, mimicry may contribute to the formation and (Norman et al., 2001), butterflies (Nijhout, 2003; Kunte, maintenance of species barriers (Mallet and Barton, 2009), fish (Alexandrou et al., 2011), frogs (Darst and 1989; Mallet and Joron, 1999; Jiggins et al., 2001; Cummings, 2006), and snakes (Brodie and Brodie, Naisbit et al., 2001; Jiggins, 2008; Chamberlain et al., 2004). These observations have led researchers to pro- 2009; Pfennig and Mullen, 2010). pose various hypotheses for why such polymorphism In sum, as the above questions make clear, studies of may arise, such as the possibility that spatial or temporal mimicry address topics as diverse as how novel, com- variation may exist in the magnitude and direction of plex traits arise; how animals make complex decisions; selection favoring mimicry (Joron and Iwasa, 2005; and how new species originate and diversify. The papers Maan and Cummings, 2008). Alternatively, polymor- in this issue of Current Zoology touch on these ques- phism may arise as a consequence of population subdi- tions. vision through the operation of shifting balance forces 3 Contributions to the Special Column (Mallet and Joron, 1999). Fourth, why is mimicry frequently imprecise? Al- This special column consists of six papers, three of though mimicry is widely used to exemplify natural which are review papers and three of which are original selection’s power in promoting adaptation, it has never- research papers. In the first of the review papers, Pfen- theless become increasingly clear that mimicry is fre- nig and Kikuchi (2012a) discuss the evidence for a quently imprecise (Edmunds, 2000; Sherratt, 2002; novel hypothesis on the evolution of imperfect mimicry. Pfennig and Kikuchi, 2012b). Thus, why are imperfect Specifically, they suggest that imperfect mimicry poten- mimics not further improved by natural selection? Al- tially represents an evolutionary compromise between though a number of hypotheses have been proposed to predator-mediated selection favoring mimetic conver- explain the evolution of imprecise mimicry (reviewed in gence on the one hand and competitively mediated se- Pfennig and Kikuchi 2012a), one leading hypothesis is lection favoring divergence on the other hand (whether David PFENNIG, Guest Editor: Mimicry: Ecology, evolution, and development 605 this competition arises over access to resources or mechanisms as does its model, suggesting that precise
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