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No honesty in warning signals across life stages in an aposematic bug

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Abstract

Theory predicts that warning signals should exhibit low variation to increase learning efficiency in predators. Many species, however, exhibit variation in warning colours within species and even within populations. An understudied example of within species variation is that between life stages, where animals change warning colouration throughout ontogeny. Understanding how warning signals change throughout life can help us identify the different ecological pressures that affect the evolution of warning signals. We used the Australasian cotton harlequin bug (Tectocoris diophthalmus) to explore how adults and nymphs differ in their defensive secretions and colouration. We performed spectrophotometric colour measurements and toxicity bioassays. Our results show, overall, no consistent association between colour and toxicity within species. There was no clear pattern for females and nymphs. Adult males, however, present the highest contrast against backgrounds, highest internal contrast, and highest toxicity. There was no association between colour and toxicity within males, nymphs or females. Our results suggest weak signal honesty in warning signals across life stages and sexes, and demonstrate that variation in colour within species is not necessarily linked to changes in toxicity.

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References

  • Abad R, Azhari S, Djozan D, Hejazi M (2012) Compounds in abdominal and metathoracic scent glands of nymphs and adults of Graphosoma lineatum (Linnaeus, 1758) (Het., scutelleridae) under laboratory conditions. Mun Entmol Zool 7:870–880

    Google Scholar 

  • Amézquita A, Ramos Ó, González MC, Rodríguez C, Medina I, Simões PI, Lima AP (2017) Conspicuousness, color resemblance, and toxicity in geographically diverging mimicry: the pan-Amazonian frog Allobates femoralis. Evolution 71:1039–1050

    PubMed  Google Scholar 

  • Arenas LM, Walter D, Stevens M (2015) Signal honesty and predation risk among a closely related group of aposematic species. Sci Rep 5:11021

    CAS  Google Scholar 

  • Aronsson M, Gamberale-Stille G (2008) Domestic chicks primarily attend to colour, not pattern, when learning an aposematic coloration. Anim Behav 75:417–423

    Google Scholar 

  • Aronsson M, Gamberale-Stille G (2009) Importance of internal pattern contrast and contrast against the background in aposematic signals. Behav Ecol 20:1356–1362

    Google Scholar 

  • Barnett JB, Scott-Samuel NE, Cuthill IC (2016) Aposematism: balancing salience and camouflage. Biol Lett 12:20160335

    PubMed  PubMed Central  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1:1–23

    Google Scholar 

  • Blount JD, Speed MP, Ruxton GD, Stephens PA (2008) Warning displays may function as honest signals of toxicity. Proc R Soc B Biol Sci 276:871–877

    Google Scholar 

  • Booth CL (1990) Evolutionary significance of ontogenetic colour change in animals. Biol J Linn Soc 40:125–163

    Google Scholar 

  • Briolat ES, Zagrobelny M, Olsen CE, Blount JD, Stevens M (2018) No evidence of quantitative signal honesty across species of aposematic burnet moths (Lepidoptera: Zygaenidae). J Evolut Biol 32:31–48

    Google Scholar 

  • Briolat ES, Burdfield-Steel ER, Paul SC, Rönkä KH, Seymoure BM, Stankowich T, Stuckert AMM (2019) Diversity in warning coloration: selective paradox or the norm? Biol Rev 94:388–414

    PubMed  Google Scholar 

  • Chouteau M, Angers B (2011) The role of predators in maintaining the geographic organization of aposematic signals. Am Nat 178:810–817

    PubMed  Google Scholar 

  • Chouteau M, Arias M, Joron M (2016) Warning signals are under positive frequency-dependent selection in nature. Proc Natl Acad Sci USA 113:2164–2169

    CAS  PubMed  Google Scholar 

  • Čokl A (2008) Stink bug interaction with host plants during communication. J Insect Physiol 54:1113–1124

    PubMed  Google Scholar 

  • Cortesi F, Cheney K (2010) Conspicuousness is correlated with toxicity in marine opisthobranchs. J Evol Biol 23:1509–1518

    CAS  PubMed  Google Scholar 

  • de Jong PW, Holloway GJ, Brakefield PM, de Vos H (1991) Chemical defence in ladybird beetles (Coccinellidae). II. Amount of reflex fluid, the alkaloid adaline and individual variation in defence in 2-spot ladybirds (Adalia bipunctata). Chemoecology 2:15–19

    Google Scholar 

  • Endler JA (1988) Frequency-dependent predation, crypsis and aposematic coloration. Philos Trans R Soc Lond B 319:505–523

    CAS  Google Scholar 

  • English-Loeb GM, Collier BD (1987) Nonmigratory movement of adult harlequin bugs Murgantia histrionica (Hemiptera: Pentatomidae) as affected by sex, age and host plant quality. Am Midl Nat 118:189–197

    Google Scholar 

  • Fabricant SA, Smith CL (2014) Is the hibiscus harlequin bug aposematic? The importance of testing multiple predators. Ecol Evol 4:113–120

    PubMed  Google Scholar 

  • Fabricant SA, Exnerová A, Ježová D, Štys P (2014) Scared by shiny? The value of iridescence in aposematic signalling of the hibiscus harlequin bug. Anim Behav 90:315–325

    Google Scholar 

  • Fabricant SA, Burdfield-Steel ER, Umbers K, Lowe EC, Herberstein ME (2018) Warning signal plasticity in hibiscus harlequin bugs. Evol Ecol 32:489–507

    Google Scholar 

  • Ferrari S, Cribari-Neto F (2004) Beta regression for modelling rates and proportions. J Appl Stat 31:799–815

    Google Scholar 

  • Galarza JA, Nokelainen O, Ashrafi R, Hegna RH, Mappes J (2014) Temporal relationship between genetic and warning signal variation in the aposematic wood tiger moth (Parasemia plantaginis). Mol Ecol 23:4939–4957

    PubMed  Google Scholar 

  • Gelman A, Hill J (2006) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge

    Google Scholar 

  • Giffney RA, Kemp DJ (2014) Does it pay to care?: Exploring the costs and benefits of parental care in the Hibiscus Harlequin Bug Tectocoris diophthalmus (Heteroptera: Scutelleridae). Ethology 120:607–615

    Google Scholar 

  • Grant JB (2007) Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars. J Anim Ecol 76:439–447

    PubMed  Google Scholar 

  • Harmon SM, Mousseau TA (2007) Toxicity of the lovebug Plecia nearctica (Diptera: Bibionidae) in two common indicator organisms, Caenorhabditis elegans and Daphnia pulex. Entomol Generalis/J Gen Appl Entomol 32:311

    Google Scholar 

  • Hartig F (2019) DHARMa: Residual Diagnostics for ## Hierarchical (Multi-Level / Mixed) Regression Models. R package ## version 0.2.6. http://florianhartig.github.io/DHARMa/

  • Hegna RH, Galarza JA, Mappes J (2015) Global phylogeography and geographical variation in warning coloration of the wood tiger moth (Parasemia plantaginis). J Biogeogr 42:1469–1481

    Google Scholar 

  • Heinrich B (1993) How avian predators constrain caterpillar foraging. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints of foraging. Chapman and Hall, New York, pp 224–247

    Google Scholar 

  • Javahery M, Schaefer CW, Lattin JD (2000) Shield bugs (Scutelleridae). Heteroptera of economic importance. CRC Press, Boca Raton, pp 475–503

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lee D-H, Leskey T (2015) Flight behavior of foraging and overwintering brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Bull Entomol Res 105:566–573

    PubMed  PubMed Central  Google Scholar 

  • Lee TJ, Speed MP, Stephens PA (2011) Honest signaling and the uses of prey coloration. Am Nat 178:E1–E9

    PubMed  Google Scholar 

  • Lindstedt C, Schroderus E, Lindström L, Mappes T, Mappes J (2016) Evolutionary constraints of warning signals: a genetic trade-off between the efficacy of larval and adult warning coloration can maintain variation in signal expression. Evolution 70:2562–2572

    CAS  PubMed  Google Scholar 

  • Lindstedt C, Boncoraglio G, Cotter SC, Gilbert JDJ, Kilner RM (2019) Parental care shapes evolution of aposematism and provides lifelong protection against predators. bioRxiv, 644864

  • Lindström L, Alatalo RV, Lyytinen A, Mappes J (2001) Strong antiapostatic selection against novel rare aposematic prey. Proc Natl Acad Sci USA 98:9181–9184

    PubMed  Google Scholar 

  • Magnusson A, Skaug H, Nielsen A, Berg C, Kristensen K, Maechler M, van Bentham K, Bolker B, Brooks M, Brooks MM (2017) Package ‘glmmTMB’. R Package Version 02 0

  • Maia R, Eliason CM, Bitton PP, Doucet SM, Shawkey MD (2013) pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4:906–913

    Google Scholar 

  • Mallet J, Gilbert LE Jr (1995) Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. Biol J Linn Soc 55:159–180

    Google Scholar 

  • Mallet J, Joron M (1999) Evolution of diversity in warning color and mimicry: polymorphisms, shifting balance, and speciation. Annu Rev Ecol Syst 30:201–233

    Google Scholar 

  • McLain DK (1998) Non-genetic benefits of mate choice: fecundity enhancement and sexy sons. Anim Behav 55:1191–1201

    Google Scholar 

  • Medina I, Wang IJ, Salazar C, Amézquita A (2013) Hybridization promotes color polymorphism in the aposematic harlequin poison frog, Oophaga histrionica. Ecol Evol 3:4388–4400

    PubMed  PubMed Central  Google Scholar 

  • Mochida K, Kitada M, Ikeda K, Toda M, Takatani T, Arakawa O (2013) Spatial and temporal instability of local biotic community mediate a form of aposematic defense in newts, consisting of carotenoid-based coloration and tetrodotoxin. J Chem Ecol 39:1186–1192

    CAS  PubMed  Google Scholar 

  • Nokelainen O, Hegna RH, Reudler JH, Lindstedt C, Mappes J (2011) Trade-off between warning signal efficacy and mating success in the wood tiger moth. Proc R Soc B Biol Sci 279:257–265

    Google Scholar 

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

    PubMed  Google Scholar 

  • Poulton EB (1890) The colours of animals: their meaning and use, especially considered in the case of insects. D. Appleton, New York

    Google Scholar 

  • Prudic KL, Noge K, Becerra JX (2008) Adults and nymphs do not smell the same: the different defensive compounds of the giant mesquite bug (Thasus neocalifornicus: Coreidae). J Chem Ecol 34:734

    CAS  PubMed  Google Scholar 

  • Rojas B, Endler JA (2013) Sexual dimorphism and intra-populational colour pattern variation in the aposematic frog Dendrobates tinctorius. Evol Ecol 27:739–753

    Google Scholar 

  • Rönkä K, Mappes J, Michalis C, Kiviö R, Salokannas J, Rojas B (2018) Can multiple-model mimicry explain warning signal polymorphism in the wood tiger moth, Arctia plantaginis (Lepidoptera: Erebidae)? Biol J Linn Soc 124:237–260

    Google Scholar 

  • Sanchez E, Pröhl H, Lüddecke T, Schulz S, Steinfartz S, Vences M (2019) The conspicuous postmetamorphic coloration of fire salamanders, but not their toxicity, is affected by larval background albedo. J Exp Zool Part B Mol Dev Evolut 332:26–35

    Google Scholar 

  • Song S, Kim S, Kwon SW, Lee S-I, Jablonski PG (2018) Defense sequestration associated with narrowing of diet and ontogenetic change to aposematic colours in the spotted lanternfly. Sci Rep 8:16831

    PubMed  PubMed Central  Google Scholar 

  • Speed MP, Ruxton GD, Blount JD, Stephens PA (2010) Diversification of honest signals in a predator–prey system. Ecol Lett 13:744–753

    PubMed  Google Scholar 

  • Staddon B, Thorne M, Knight D (1987) The scent glands and their chemicals in the aposematic cotton harlequin bug, Tectocoris-Diophthalmus (Heteroptera, Scutelleridae). Aust J Zool 35:227–234

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Stuckert AM, Venegas PJ, Summers K (2014) Experimental evidence for predator learning and Müllerian mimicry in Peruvian poison frogs (Ranitomeya, Dendrobatidae). Evol Ecol 28:413–426

    Google Scholar 

  • Stuckert AM, Saporito RA, Summers K (2018) An empirical test indicates only qualitatively honest aposematic signaling within a population of vertebrates. J Herpetol 52:201–208

    Google Scholar 

  • Summers K, Clough ME (2001) The evolution of coloration and toxicity in the poison frog family (Dendrobatidae). Proc Natl Acad Sci USA 98:6227–6232

    CAS  PubMed  Google Scholar 

  • Summers K, Speed M, Blount J, Stuckert A (2015) Are aposematic signals honest? A review. J Evol Biol 28:1583–1599

    CAS  PubMed  Google Scholar 

  • Sword GA (1999) Density-dependent warning coloration. Nature 397:217

    CAS  Google Scholar 

  • Twomey E, Vestergaard JS, Summers K (2014) Reproductive isolation related to mimetic divergence in the poison frog Ranitomeya imitator. Nat Commun 5:4749

    CAS  PubMed  Google Scholar 

  • Wang IJ, Shaffer HB (2008) Rapid color evolution in an aposematic species: a phylogenetic analysis of color variation in the strikingly polymorphic strawberry poison-dart frog. Evol Int J Org Evol 62:2742–2759

    CAS  Google Scholar 

  • Wink M, Grimm C, Koschmieder C, Sporer F, Bergeot O (2000) Sequestration of phorbolesters by the aposematically coloured bug Pachycoris klugii (Heteroptera: Scutelleridae) feeding on Jatropha curcas (Euphorbiaceae). Chemoecology 10:179–184

    CAS  Google Scholar 

  • Winters AE, Stevens M, Mitchell C, Blomberg SP, Blount JD (2014) Maternal effects and warning signal honesty in eggs and offspring of an aposematic ladybird beetle. Funct Ecol 28:1187–1196

    Google Scholar 

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Acknowledgements

We would like to thank University of Melbourne for funding awarded to I.M. and the British Ecological Society for funding awarded to I.M and M.L.H. We would also like to thank Constanza León, Daniela Perez, Lina María Arenas, Devi Stuart-Fox, Scott Fabricant, Emily Burdfield-Steel, Phillip Lincoln Erm and Ben Phillips for help with information on the bug, advice on experimental design, access to Daphnia, and help with toxicity assays.

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  1. School of BioSciences, University of Melbourne, BioSciences 4, Parkville, VIC, 3010, Australia

    Iliana Medina

  2. Division of Ecology and Evolution, Australian National University, Canberra, ACT, 0200, Australia

    Thomas Wallenius & Megan Head

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  1. Iliana Medina
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  2. Thomas Wallenius
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Correspondence to Iliana Medina.

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Medina, I., Wallenius, T. & Head, M. No honesty in warning signals across life stages in an aposematic bug. Evol Ecol 34, 59–72 (2020). https://doi.org/10.1007/s10682-019-10025-0

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