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Predator-based selection and the impact of edge sympatry on components of coral snake mimicry

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A Correction to this article was published on 21 February 2022

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Abstract

Mimicry is a vivid example of how predator-driven selection can impact phenotypic diversity, which itself can be influenced by the presence (sympatry) or absence (allopatry) of a dangerous model. However, the impact of sympatry and allopatry on predation on mimicry systems at fine spatial scales (e.g., edge sympatry, allopatry) is not well understood. We studied mimicry in a montane tropical site in Honduras with an abrupt elevational gradient where coral snakes and mimics exist in close sympatry and allopatry. Specifically, we used clay replicas to test the impact of edge sympatry on (1) overall attack rates, (2) the fitness benefit of mimetic coloration, and (3) predation on specific mimetic signal components. Unlike previous research, we found that mimetic phenotypes received significantly more attacks than cryptic replicas in edge sympatry, suggesting that mimetic phenotypes might not confer a fitness benefit in areas of edge sympatry. Additionally, we documented temporal variation in predator-based selection, as the impacts of allopatry on predatory attacks varied among years. Our results imply that the effect of sympatry and allopatry on predator-based selection in mimicry systems may be more complex than previously thought for species-rich assemblies of coral snakes and their mimics in the montane tropics.

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Data available through Dryad at: https://doi.org/10.5061/dryad.pnvx0k6kv

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References

  • Akcali CK, Kikuchi DW, Pfennig DW (2018) Coevolutionary arms races in Batesian mimicry? A test of the chase-away hypothesis. Biol J Lin Soc 124:668–676

    Article  Google Scholar 

  • Akcali CK, Pfennig DW (2014) Rapid evolution of mimicry following local model extinction. Biol Lett 10:20140304

    Article  PubMed  PubMed Central  Google Scholar 

  • Akcali CK, Pfennig DW (2017) Geographic variation in mimetic precision among different species of coral snake mimics. J Evol Biol 30:1420–1428

    Article  CAS  PubMed  Google Scholar 

  • Alliance AS (2019) Spike-thumb Frog, Plectrohyla dasypus. Amphibian Survival Alliance

  • Arbuckle K, Speed MP (2015) Antipredator defenses predict diversification rates. Proc Natl Acad Sci U S A 112:13597–13602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bateman PW, Fleming PA, Wolfe AK (2017) A different kind of ecological modelling: the use of clay model organisms to explore predator-prey interactions in vertebrates. J Zool 301:251–262

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Brodie E III (1993) Differential avoidance of coral snake banded patterns by free-ranging avian predators in Costa Rica. Evolution 47:227–235

    Article  PubMed  Google Scholar 

  • Brodie III E, Janzen FJ (1995) Experimental studies of coral snake mimicry: generalized avoidance of ringed snake patterns by free-ranging avian predators. Funct Ecol 9:186–190

    Article  Google Scholar 

  • Brown T, Arrivillaga C (2017) Herpetofauna of Cusuco National Park. Operation Wallacea, Honduras

  • Brown TW, Barazowski MB, Lonsdale G (2020) Defensive tail-curling and head-mimicking behavior in a variable coralsnake, Micrurus diastema (Squamata: Elapidae) in Cusuco National Park, Honduras. Int Reptile Conserv Found 27:231–232

    Google Scholar 

  • Charlesworth D, Charlesworth B (1975) Theoretical genetics of batesian mimicry I. Single-Locus Models. J Theor Biol 55:283–303

    Article  CAS  PubMed  Google Scholar 

  • Cox CL, Davis Rabosky AR (2013) Spatial and temporal drivers of phenotypic diversity in polymorphic snakes. Am Nat 182:E40-57

    Article  PubMed  Google Scholar 

  • Davis Rabosky AR, Cox CL, Rabosky DL, Title PO, Holmes IA, Feldman A, McGuire JA (2016) Coral snakes predict the evolution of mimicry across New World snakes. Nat Commun 7:11484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis Rabosky AR, Larson JG, Danforth SM, Moore TY (2020) A quantitative analysis of micrurus coral snakes reveals unexpected variation in stereotyped anti-predator displays within a mimicry system. Integr Org Biol 2:1–13

    Google Scholar 

  • Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton

    Google Scholar 

  • Finkbeiner SD, Salazar PA, Nogales S, Rush CE, Briscoe AD, Hill RI, Kronforst MR, Willmott KR, Mullen SP (2018) Frequency dependence shapes the adaptive landscape of imperfect Batesian mimicry. Proc R Soc B Biol Sci 285:20172786

    Article  Google Scholar 

  • Greene HW, McDiarmid RW (1981) Coral snake mimicry: does it occur? Science 213:1207–1212

    Article  CAS  PubMed  Google Scholar 

  • Ham AD, Ihalainen E, Lindström L, Mappes J (2006) Does colour matter? The importance of colour in avoidance learning, memorability and generalisation. Behav Ecol Sociobiol 60:482–491

    Article  Google Scholar 

  • Harper GR Jr, Pfennig DW (2008) Selection overrides gene flow to break down maladaptive mimicry. Nature 451:1103–1106

    Article  CAS  PubMed  Google Scholar 

  • Hengeveld R, Haeck J (1982) The distribution of abundance. I. Measurements. J Biogeogr 9:303–316

    Article  Google Scholar 

  • Heninger R, Watson CM, Cox CL (2020) Relative fitness of decoy coloration is mediated by habitat type. Zoology 142:125820

    Article  PubMed  Google Scholar 

  • Hinman KE, Throop H, Adams KL, Dake AJ, McLauchlan K, McKone JM (1997) Predation by free-ranging birds on partial coral snake mimics: the importance of ring width and color. Soc Stud Evol 51:1011–1014

    Google Scholar 

  • Holmes IA, Grundler MR, Davis Rabosky AR (2017) Predator perspective drives geographic variation in frequency-dependent polymorphism. Am Nat 190:E78–E93

    Article  PubMed  Google Scholar 

  • Hoskins HMJ, Burdekin OJ, Dicks K, Slater KY, McCann NP, Jocque M, Castañeda F, Reid N (2018) Non-volant mammal inventory of Cusuco National Park, north-west Honduras: reporting the presence of Jaguar, Panthera onca (Linnaeus, 1758), and demonstrating the effects of zonal protection on mammalian abundance. Check List 14:877–891

    Article  Google Scholar 

  • Joron M, Mallet JLB (1998) Diversity in mimicry: paradox or paradigm? Trends Ecol Evol 13:461–466

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi DW, Pfennig DW (2010) Predator cognition permits imperfect coral snake mimicry. Am Nat 176:830–834

    Article  PubMed  Google Scholar 

  • Kikuchi DW, Pfennig DW (2013) Imperfect mimicry and the limits of natural selection. Q Rev Biol 88:297

    Article  PubMed  Google Scholar 

  • Kleisner K, Saribay SA (2018) The dual nature of mimicry. Organismal form and beholder’s eye. Biosemiotics 12:79–98

    Article  Google Scholar 

  • Kuchta SR (2005) Experimental support for aposematic coloration in the salamander Ensatina eschscholtzii xanthoptica: implications for mimicry of Pacific Newts. Copeia 2005:265–271

    Article  Google Scholar 

  • Leimar O, Enquist M, Sillen-Tullberg B (1986) Evolutionary stability of aposematic coloration and prey unprofitability: a theoretical analysis. Am Nat 128:469–490

    Article  Google Scholar 

  • Lindstedt C, Eager H, Ihalainen E, Kahilainen A, Stevens M, Mappes J (2011) Direction and strength of selection by predators for the color of the aposematic wood tiger moth. Behav Ecol 22:580–587

    Article  Google Scholar 

  • Lindström L, Alatalo RV, Mappes J (1997) Imperfect Batesian mimicry—the effects of the frequency and the distastefulness of the model. Proc R Soc b Biol Sci 264:149–153

    Article  Google Scholar 

  • Mallet J, Turner J (1997) Biotic drift or the shifting balance — Did forest islands drive the diversity of warningly coloured butterflies? Philos Trans R Soc b Biol Sci 351:262–280

    Google Scholar 

  • Mappes J, Alatalo RV (1997) Batesian Mimicry and Signal Accuracy. Evolution 51:2050–2053

    Article  PubMed  Google Scholar 

  • Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603

    Article  PubMed  Google Scholar 

  • Martin T, Jones S, Hoskins H, McCann N, Batke S, Kelly D, Kolby J, Downing R, Zelaya S, Green S, Lonsdale G, Brown T, Waters S, Rodríguez-Vásquez F, McCravy K, D’Souza M, Crace D, Nunez-Mino J, Haelewaters D, Reid N (2021) (2021) A review of the ecological value of Cusuco National Park: an urgent call for conservation action in a highly threatened Mesoamerican cloud forest. J Mesoamerican Biol 1:6–50

    Google Scholar 

  • Mazerolle MJ (2019) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c)

  • McCranie JR (2011) The snakes of honduras: systematics, distribution, and conservation. Society for the Study Of Amphibians and Reptiles, Thomson-Shore, Michigan

    Google Scholar 

  • Noonan BP, Comeault AA (2009) The role of predator selection on polymorphic aposematic poison frogs. Biol Let 5:51–54

    Article  Google Scholar 

  • Owen RE, Owen ARG (1984) Mathematical paradigms for mimicry: recurrent sampling. J Theor Biol 109:217–247

    Article  Google Scholar 

  • Paluh DJ, Hantak MM, Saporito RA (2014) A test of aposematism in the dendrobatid poison frogoophaga pumilio: the importance of movement in clay model experiments. J Herpetol 48:249–254

    Article  Google Scholar 

  • Pfennig DW (2016) Evolutionary biology: to mimicry and back again. Nature 534:184–185

    Article  CAS  PubMed  Google Scholar 

  • Pfennig DW, Harcombe WR, Pfennig KS (2001) Frequency-dependent Batesian mimicry. Nature 410:323

    Article  CAS  PubMed  Google Scholar 

  • Pfennig DW, Harper GR, Brumo AF, Harcombe WR, Pfennig KS (2007) Population differences in predation on Batesian mimics in allopatry with their model: selection against mimics is strongest when they are common. Behav Ecol Sociobiol 61:505–511

    Article  Google Scholar 

  • Pfennig DW, Mullen SP (2010) Mimics without models: causes and consequences of allopatry in Batesian mimicry complexes. Proc R Soc b Biol Sci 277:2577–2585

    Article  Google Scholar 

  • Pough FH (1988) Mimicry of vertebrates: are the rules different? Am Nat 131:S67–S102

    Article  Google Scholar 

  • Quicke DLJ (2017) Mimicry, crypsis, masquerade and other adaptive resemblances. Wiley Blackwell, Hoboken, NJ

    Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Ries L, Mullen SP (2008) A rare model limits the distribution of its more common mimic: a twist on frequency-dependent Batesian mimicry. Evolution 62:1798–1803

    Article  PubMed  Google Scholar 

  • Ruxton G, Allen W, Sherratt NT, Speed M (2004) Avoiding attack: the evolutionary ecology of crypsis, aposematism, and mimicry. Oxford University Press, New York

    Book  Google Scholar 

  • Savage JM, Slowinski JB (1992) The colouration of the venomous coral snakes (family Elapidae) and their mimics (families Aniliidae and Colubridae). Biol J Lin Soc 45:235–254

    Article  Google Scholar 

  • Smith NG (1969) Avian Predation of Coral Snakes. Copeia 1969:402–404

    Article  Google Scholar 

  • Smith SM (1975) Innate recognition of coral snake pattern by a possible avian predator. Science 187:759

    Article  CAS  PubMed  Google Scholar 

  • Smith SM (1977) Coral-snake pattern recognition and stimulus generalisation by naive great kiskadees (Aves: Tyrannidae). Nature 265:535–536

    Article  Google Scholar 

  • Stevens M, Ruxton GD (2012) Linking the evolution and form of warning coloration in nature. Proc R Soc b Biol Sci 279:417–426

    Article  Google Scholar 

  • Titcomb G, Kikuchi D, Pfennig D (2014) More than mimicry? Evaluating scope for flicker-fusion as a defensive strategy in coral snake mimics. Curr Zool 60:123–130

    Article  Google Scholar 

  • Townsend JH, Wilson LD (2008) The amphibians & reptiles of cusuco National Park, Honduras. Salt Lake City, Utah: Bibliomania!

  • Yamauchi A (1993) A population dynamic model of Batesian mimicry. Res Popul Ecol 35:295–315

    Article  Google Scholar 

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Acknowledgements

We thank Mairéad Corr, Maddy Blunt, Georgina Davey, Hunter McCall, Rodrigo Morales, Harry-Pym Davis, and Chris Phipps for field assistance. Declan Crace and Tom Martin were instrumental in the design and implementation of this research. We thank the Department of Biology and Graduate Student Organization at Georgia Southern University and Operation Wallacea for supporting this project. Our sincere gratitude is extended to Lance McBrayer, Adam Rosso, Albert Chung, and Scott Meyer for advice during this project.

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This work was supported by Operation Wallacea and Georgia Southern University.

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LW participated in the design of the study, collected field data, carried out statistical analyses, and drafted the manuscript; GL participated in the design of the study, aided in field work, and revised the manuscript; JDC participated in the design of the study, collected field data, and revised the manuscript; EH aided in statistical analyses and critically revised the manuscript, CC conceived of the study, designed the study, coordinated the study, and critically revised the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed therein.

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Correspondence to Lauren Wilson.

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The original version of this article was revised: The texts “Data will be deposited at Dryad upon acceptance” under Data availability section was updated as “Data available through Dryad at: doi:10.5061/dryad.pnvx0k6kv”.

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Wilson, L., Lonsdale, G., Curlis, J.D. et al. Predator-based selection and the impact of edge sympatry on components of coral snake mimicry. Evol Ecol 36, 135–149 (2022). https://doi.org/10.1007/s10682-021-10143-8

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