Frequency-Dependent Selection by Wild Birds Promotes Polymorphism in Model Salamanders

University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Faculty Publications and Other Works -- Ecology and Evolutionary Biology Ecology and Evolutionary Biology July 2013 Frequency-dependent selection by wild birds promotes polymorphism in model salamanders Benjamin M. Fitzpatrick University of Tennessee - Knoxville, [email protected] Kim Shook University of Tennessee - Knoxville Reuben Izally Farragut High School Follow this and additional works at: https://trace.tennessee.edu/utk_ecolpubs Part of the Ecology and Evolutionary Biology Commons Recommended Citation BMC Ecology 2009, 9:12 doi:10.1186/1472-6785-9-12 This Article is brought to you for free and open access by the Ecology and Evolutionary Biology at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Faculty Publications and Other Works -- Ecology and Evolutionary Biology by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. BMC Ecology BioMed Central Research article Open Access Frequency-dependent selection by wild birds promotes polymorphism in model salamanders Benjamin M Fitzpatrick*1, Kim Shook2,3 and Reuben Izally2,3 Address: 1Ecology & Evolutionary Biology, University of Tennessee, Knoxville TN 37996, USA, 2Pre-collegiate Research Scholars Program, University of Tennessee, Knoxville TN 37996, USA and 3Farragut High School, Knoxville TN 37934, USA Email: Benjamin M Fitzpatrick* - [email protected]; Kim Shook - [email protected]; Reuben Izally - [email protected] * Corresponding author Published: 8 May 2009 Received: 10 February 2009 Accepted: 8 May 2009 BMC Ecology 2009, 9:12 doi:10.1186/1472-6785-9-12 This article is available from: http://www.biomedcentral.com/1472-6785/9/12 © 2009 Fitzpatrick et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Co-occurrence of distinct colour forms is a classic paradox in evolutionary ecology because both selection and drift tend to remove variation from populations. Apostatic selection, the primary hypothesis for maintenance of colour polymorphism in cryptic animals, proposes that visual predators focus on common forms of prey, resulting in higher survival of rare forms. Empirical tests of this frequency-dependent foraging hypothesis are rare, and the link between predator behaviour and maintenance of variation in prey has been difficult to confirm. Here, we show that predatory birds can act as agents of frequency-dependent selection on terrestrial salamanders. Polymorphism for presence/absence of a dorsal stripe is widespread in many salamander species and its maintenance is a long-standing mystery. Results: We used realistic food-bearing model salamanders to test whether selection by wild birds maintains a stripe/no-stripe polymorphism. In experimental manipulations, whichever form was most common was most likely to be attacked by ground-foraging birds, resulting in a survival advantage for the rare form. Conclusion: This experiment demonstrates that frequency-dependent foraging by wild birds can maintain colour polymorphism in cryptic prey. Background common form if it is easier to search for one cryptic prey Maintenance of variation is a classic paradox in evolution type than to simultaneously look for two [4-6]. If preda- because both selection and drift tend to remove variation tors switch their search images to whichever prey is most from populations [1-3]. If one form has an advantage common, the result is frequency-dependent selection (e.g., being more cryptic), it should replace all others. against common prey [4-7]. Empirical tests of this fre- Likewise, random drift alone will eventually result in loss quency-dependent selection hypothesis are rare, and the of all but one form when there are no fitness differences. link between predator behaviour and maintenance of var- Maintenance of a stable polymorphism requires either iation in prey has been difficult to confirm [4,8]. Here, we recurrent mutation, a balance between dispersal and test whether predatory birds can act as agents of fre- divergent selection between populations, or some form of quency-dependent selection on terrestrial salamanders balancing selection within populations [3]. For example, using a manipulative field experiment. predators are expected to form a search image for the most Page 1 of 6 (page number not for citation purposes) BMC Ecology 2009, 9:12 http://www.biomedcentral.com/1472-6785/9/12 Multiple species of small, forest floor-dwelling salamanders exhibit polymorphism for the presence of a dorsal stripe (Fig. 1) and what maintains this polymorphism within populations is a long-standing question [9-15]. Polymorphism is widespread both geographically and phylogenetically, occurring in many species of Plethodon throughout North America in addition to the distantly related Batrachoseps of the Pacific coast of North America [16] and Karsenia of Asia [17]. Thus, it is unlikely that this polymorphism is merely a transitional stage in the evolution of colour pattern. Presence or absence of a dorsal stripe appears to have a simple genetic basis in Plethodon cinereus and is not related to sex [12,18]. What polymorphic salamander species seem to have in common is that they are small, slender, and locally abun- dant. These species often comprise a substantial fraction of the animal biomass in temperate forests and are subject to predation by ground-foraging birds and other predators that search the leaf-litter for small animals [16]. Stud- ies of polymorphic Plethodon cinereus have shown differences between the morphs in behaviour [11,14,15,19], physiology [11,13], and geographic variation in relative abundance [10,20]. However, none directly address how these differences might relate to a mechanism maintaining variation and there is no evi- dence of similar phenotypic correlations in the other polymorphic species. In fact, in P. ventralis, the frequency of the striped form is less at higher elevations [21] whereas the frequency of striped P. cinereus is greater at higher lat- itude and cooler microclimates in general [10,20]. Thus, phenotypic correlations between appearance and physiology are not consistent (also see [13]) and this is not sur- prising given that dorsal colour pattern is unlikely to have a direct function in temperature tolerance or metabolism (Plethodon always avoid sunlight). To explain the maintenance of a similar visual polymorphism across many taxa, we propose that selection acts directly on appearance. The most likely function of dorsal colour pattern is crypsis (Fig. 1), though this is an untested assumption. Though there has been speculation that the red stripe of P. cinereus might be an aposematic signal [19], Brodie and Brodie [22] showed that wild birds prey extensively upon striped P. cinereus, and give no sign ExamplesFigure 1 of polymorphic plethodontid salamanders that the salamanders are unpalatable. Striped P. cinereus Examples of polymorphic plethodontid salamanders. were taken just as often as D. ochrophaeus, which were Each pair of individuals was captured in the same place at the assumed to be cryptic and palatable [22]. A third, com- same time. a, Southern Red-backed Salamanders, Plethodon pletely red form of P. cinereus does appear to be a colour serratus, Great Smoky Mountains National Park (Tennessee, mimic of the toxic Red-spotted Newt eft (Notophthalmus USA). b, Southern Zigzag Salamanders, P. ventralis, Knoxville viridescens), but our focus is on the more widespread (Tennessee, USA). c, California Slender Salamanders, Batra- stripe/no-stripe polymorphism. Polymorphism in cryptic choseps attenuatus, Napa County (California, USA). Page 2 of 6 (page number not for citation purposes) BMC Ecology 2009, 9:12 http://www.biomedcentral.com/1472-6785/9/12 prey populations might be maintained in migration-selection balance if alternative colour forms are adapted to dif- ferent habitats [23], or might be promoted by frequency- dependent predation causing rare form advantage within populations [4,8]. Empirical tests of frequency-dependent foraging on cryptic prey are rare; the best-studied examples involve either colored pellets of dough fed to free-ranging birds [7,24,25]or digital images of moths selected by trained Blue Jays (Cyanocitta cristata) [4,26-28]. These studies demonstrate that birds can generate frequency-dependent selection, that individual Blue Jays learn to focus on abun- dant prey, and that they readily switch focus in response to changes in prey abundance. Apostatic selection by free- ranging wild birds has been shown for small pastries dif- fering in colour [7,25,29], and presence or absence of a stripe [30,31], and also for real Cepaea snail shells differ- ing in banding pattern [32]. However, in other studies, selection changed from negative frequency-dependence (rare form advantage) to positive frequency-dependence (common form advantage) when artificial prey were provided at high densities, showing that rare form advantage is not entirely general and may depend on abundance or aggregation of prey [25,33]. A recent study of Trinidadian guppies implicated frequency-dependent survival in the maintenance of variation in conspicuously colored males

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