Variation in Wing Pattern and Palatability in a Female-Limited Polymorphic Mimicry System
Total Page：16
File Type：pdf, Size：1020Kb
UC Davis UC Davis Previously Published Works Title Variation in wing pattern and palatability in a female-limited polymorphic mimicry system. Permalink https://escholarship.org/uc/item/3xn706gr Journal Ecology and evolution, 4(23) ISSN 2045-7758 Authors Long, Elizabeth C Hahn, Thomas P Shapiro, Arthur M Publication Date 2014-12-01 DOI 10.1002/ece3.1308 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Variation in wing pattern and palatability in a female- limited polymorphic mimicry system Elizabeth C. Long1,2,3, Thomas P. Hahn4 & Arthur M. Shapiro1,5 1Center for Population Biology, University of California Davis, Davis, California 2Entomology Section, Natural History Museum of Los Angeles County, Los Angeles, California 3UCLA La Kretz Center for California Conservation Science, Institute of the Environment and Sustainability, University of California, Los Angeles, California 4Department of Neurobiology, Physiology, and Behavior, University of California Davis, Davis, California 5Department of Evolution and Ecology, University of California Davis, Davis, California Keywords Abstract Batesian mimicry, Chlosyne hoffmanni, Chlosyne palla, Euphydryas chalcedona, Checkerspot butterflies in the genera Euphydryas and Chlosyne exhibit pheno- palatability. typic polymorphisms along a well-defined latitudinal and elevational gradient in California. The patterns of phenotypic variation in Euphydryas chalcedona, Correspondence Chlosyne palla, and Chlosyne hoffmanni suggest a mimetic relationship; in addi- Elizabeth Long, UCLA La Kretz Center for tion, the specific patterns of variation in C. palla suggest a female-limited poly- California Conservation Science, Entomology morphic mimicry system (FPM). However, the existence of polymorphic Section, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, models runs counter to predictions of mimicry theory. Palatability trials were Los Angeles, CA 90007. undertaken to assess whether or not the different color morphs of each species Tel: (213) 763-3225; were distasteful or toxic to a generalized avian predator, the European starling Fax: (213) 746-2999; (Sturnus vulgaris). Results indicate that the black morph of E. chalcedona is dis- E-mail: [email protected] tasteful, but not toxic, to predators, while the red morph is palatable. C. hoff- manni and both color morphs of C. palla are palatable to predators. Predators Funding Information that learn to reject black E. chalcedona also reject black C. palla, suggesting that Partial funding for this project was provided the latter is a FPM of the former. C. hoffmanni does not appear to be involved to ECL by the Center for Population Biology, University of California Davis. in this mimetic relationship. Received: 24 September 2014; Revised: 8 October 2014; Accepted: 9 October 2014 Ecology and Evolution 2014; 4(23): 4543– 4552 doi: 10.1002/ece3.1308 Introduction (Huheey 1988; Joron and Mallet 1998). Because a fundamental tenet of Batesian mimicry holds that the Mimicry theory predicts that once a predator guild begins mimic is detrimental to the model, particularly as the to associate a warning signal (aposematism) with a pen- mimic increases in abundance, a model that is able to alty (noxiousness) of the model, individuals that exhibit evolve and establish a new aposematic phenotype, free of the familiar aposematic phenotype will gain protection mimics, would gain a selective advantage (Turner et al. from predation and will experience increased fitness. The- 1984; Huheey 1988; Malcolm 1990; Joron and Mallet ory also predicts that selection will act to reduce variation 1998). Although possible, a predicted increased rate of in the aposematic phenotype of models as individuals that evolution in the mimic versus the model coupled with differ from that phenotype should suffer reduced fitness strong stabilizing selection on the model makes this an due to increased predation (Benson 1972; Harvey et al. unlikely scenario (Joron and Mallet 1998). 1982; Endler and Greenwood 1988). An opposing hypoth- In mimics, however, phenotypic polymorphism may esis proposes that models may evolve variability and thus in fact offer a selective advantage. In the case of female- “escape” from the mimic, termed coevolutionary chase limited polymorphic mimicry (FPM), males of the mimic ª 2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 4543 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. FPM in Checkerspot Butterflies E. C. Long et al. species are nonmimetic while females are polymorphic, predator to first test the palatability of three species of with some individuals exhibiting the mimetic, dishonest western checkerspot butterflies: two predominant pheno- aposematic phenotype while others are nonmimetic. Pro- typic forms of E. chalcedona; the mimetic and malelike posed adaptive explanations for this subtype of Batesian forms of C. palla; and C. hoffmanni. We addressed not mimicry include individual-level natural selection, kin only whether or not the butterflies were distasteful to pre- selection, group selection, and sexual selection (Sheppard dators but also whether they were in any way toxic. We 1962; Burns 1966; Wickler 1968; Barrett 1976; Turner then evaluated putative mimetic relationships between the 1978; Wiklund and Jarvi 1982; Stamps and Gon 1983; species and discussed the possible explanations for the Kunte 2009; Allen et al. 2011). observed polymorphisms. Numerous cases of mimicry have been described in butterflies, as have several examples of FPM systems Methods (Bates 1862; Muller 1879; Ford 1936; Van Zandt Brower 1958a,b,c; Clarke and Sheppard 1962; Benson 1972; Bow- Butterfly species ers 1983a; Prudic et al. 2002). The most famous case of FPM mimicry occurs in Papilio dardanus Brown, where The putative model in the study system is Euphydryas the females exhibit at least 14 different phenotypes, mim- chalcedona, the variable checkerspot. This species is wide- icking numerous models (Trimen 1868; Ford 1936; Nijh- spread in the western United States, frequently found in out 2003). However, in most of these described cases, the rocky canyons, and is univoltine with a late spring – early model shows little phenotypic variation, consistent with summer flight season. Some populations are unpalatable the theory. A notable exception occurs in the western to a generalized avian predator (Bowers 1981), supporting United States, where Euphydryas checkerspots, which have the hypothesis that this species acts as a model. The larvae been demonstrated to be unpalatable to generalized avian sequester iridoid glycosides from host plants in at least predators, show considerable phenotypic variation (Bow- part of its range although it does exhibit geographic varia- ers 1981, 1983a,b; Bowers et al. 1985). In particular, the tion in host plant usage; those chemical defenses are variable checkerspot, Euphydryas chalcedona Doubleday, retained in adults (Bowers 1981, 1983a,b, 1986; Bowers true to its name, varies between populations so much that and Puttick 1986; Stermitz et al. 1994). It also displays a a casual observer may have difficulty recognizing individ- great deal of phenotypic variation in wing pattern and uals from populations 1000 m apart in elevation as color throughout its range, with an especially pronounced conspecifics. elevational difference in populations in California’s Sierra A putative FPM relationship exists between E. chalcedo- Nevada Range. Below ~1700 meters, populations are pre- na (as the model) and the northern checkerspot, Chlosyne dominantly black and white with some red accents, while palla Boisduval (as the mimic). Like E. chalcedona, popu- at higher elevations, populations show a strong red-orange lations of C. palla show a great deal of wing pattern vari- background color with black pattern elements (Fig. 1A, ation along a latitudinal and elevational gradient, but Table 1). Phylogenetic evidence indicates that these forms unlike the putative model, only females of the mimic do not represent separate species (Long et al., 2014). vary. The phenotypic distribution of both species is com- The putative mimic of E. chalcedona in this study is plex, and there appears to be a strong correlation between Chlosyne palla, the northern checkerspot. Like the model, the two (Shapiro and Manolis 2007). Other related sym- populations of this species are red-orange at high eleva- patric species, for example Chlosyne hoffmanni Behr, tions in the Sierra, while at lower elevations (and in other strongly resemble some forms of both E. chalcedona and areas where the model is red-orange) males retain the C. palla and could be involved in a complex mimicry red-orange phenotype while females are red-orange, black ring. These relationships have not been previously tested (similar to E. chalcedona), or intermediate between the experimentally and would represent an interesting two (Fig. 1B, Table 1). This species is thus a putative advancement of our knowledge of both the FPM phe- FPM of E. chalcedona. It is difficult to accurately assess nomenon as well as coevolutionary chase promoting poly- female phenotypic ratios in these polymorphic popula- morphism in the model. If confirmed, it would seem to tions due to sampling bias, but the black form appears to be an elegant adaptive explanation for phenotypic vari- be the prevailing female phenotype