Abstract
Aposematic (warning) coloration is a highly conspicuous trait that is found throughout the animal kingdom. In several aposematic species, warning signals have been co-opted for use in conspecific communication systems; for example, in the toxic and bright orange Solarte population of the strawberry poison frog (Oophaga [Dendrobates] pumilio), the brightness of male warning coloration serves as a sexual signal by both attracting females and repelling rivals. Here, we investigate correlations between bright male warning coloration and several physiological characteristics (e.g., circulating testosterone and carotenoids and noxious alkaloids in the skin), to gain insights into the mechanisms underlying the signal variation in this population and to inform hypotheses regarding the evolutionary stability of this trait. We find that although measures of male brightness (viewer-dependent or viewer-independent) do not correlate with two classic correlates of sexually selected traits (circulating testosterone and aggregate carotenoids in the skin), male reflectance does show a positive correlation with concentrations of two xanthophyll carotenoids. Total reflectance (a viewer-independent measure of male brightness) also shows a negative relationship with aggregate pumiliotoxin in the skin, which is considered one of the major classes of defensive alkaloids in this species. Because the alkaloids used in this species’ chemical defense are acquired from dietary sources, the magnitude of the reflectance intensity of a male’s warning signal can potentially provide viewers with reliable information regarding territory quality, health, and/or current condition.
Similar content being viewed by others
References
Ahmad S (1992) Biochemical defence of pro-oxidant plant allelochemicals by herbivorous insects. Biochem Syst Ecol 20:269–296
Andersson MB (1994) Sexual selection. Princeton University Press, Princeton
Bagnara JT (1976) Color change. In: Lofts B (ed) Physiology of the Amphibia, vol 3. Academic Press, New York, pp 1–52
Bagnara JT (2003) Enigmas of pterorhodin, a red melanosomal pigment of tree frogs. Pigm Cell Res 16:510–516
Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399
Bezzerides AL, McGraw KJ, Parker RS, Husseini J (2007) Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav Ecol Sociobiol 61:1401–1408
Blount JD, Speed MP, Ruxton GD, Stephens PA (2009) Warning displays may function as honest signals of toxicity. Proc R Soc B 276:871–877
Blount JD, Rowland HM, Drijfhout FP, Endler JA, Inger R, Sloggett JJ, Hurst GDD, Hodgson DJ, Speed MP (2012) How the ladybird got its spots: effects of resource limitation on the honesty of aposematic signals. Funct Ecol 26:334–342
Cooper WE, Greenberg N (1992) Reptilian coloration and behavior. In: Gans C, Crews D (eds) Hormones, brain and behavior. University of Chicago Press, Chicago, pp 299–400
Cortesi F, Cheney KL (2010) Conspicuousness is correlated with toxicity in marine opisthobranchs. J Evol Biol 23:1509–1518
Cote J, Meylan S, Clobert J, Voituron Y (2010) Carotenoid-based coloration, oxidative stress and corticosterone in common lizards. J Exp Biol 213:2116–2124
Crothers LR, Cummings ME (2013) Warning signal brightness variation: sexual selection may work under the radar or natural selection in populations of a polytypic poison frog. Am Nat 181:E116–E124
Crothers LR, Cummings ME (2015) A multifunctional warning signal behaves as an agonistic status signal in a poison frog. Behav Ecol 26:560–568
Crothers L, Gering E, Cummings ME (2011) Aposematic signal variation predicts male-male interactions in a polymorphic poison frog. Evolution 65:599–605
Cummings ME, Crothers LR (2013) Interacting selection diversifies warning signals in a polytypic frog: an examination with the strawberry poison frog. Evol Ecol 27:693–710
Daly JW, Myers CW (1967) Toxicity of Panamanian poison frogs (Dendrobates)—some biological and chemical aspects. Science 156:970–973
Daly JW, Garraffo HM, Spande TF (1999) Alkaloids from amphibian skins. In: Pelletier SW (ed) Alkaloids: chemical and biological perspectives. Elsevier, Oxford, pp 1–147
Daly JW, Kaneko T, Wilham J, Garraffo HM, Spande TF, Espinosa A, Donnelly MA (2002) Bioactive alkaloids of frog skin: combinatorial bioprospecting reveals that pumiliotoxins have an arthropod source. Proc Natl Acad Sci USA 99:13996–14001
Daly JW, Spande TF, Garraffo HM (2005) Alkaloids from amphibian skin: a tabulation of over eight-hundred compounds. J Nat Prod 68:1556–1575
Darst CR, Cummings ME, Cannatella DC (2006) A mechanism for diversity in warning signals: conspicuousness versus toxicity in poison frogs. Proc Natl Acad Sci USA 103:5852–5857
Dreher CE, Pröhl H (2014) Multiple sexual signals: calls over colors for mate attraction in an aposematic color-diverse poison frog. Front Ecol Evol. doi:10.3389/fevo.2014.00022
Dreher CE, Cummings ME, Pröhl H (2015) An analysis of predator selection to affect aposematic coloration in a poison frog species. PLoS One 10:e0134628. doi:10.1371/journal.pone.0134628
Ducrest A, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510
Emerson SB (2001) Male advertisement calls: behavioral variation and physiological processes. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, DC, pp 36–44
Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622
Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton University Press, Princeton
Goyman W, Landys MM, Wingfield JC (2007) Distinguishing seasonal androgen responses from male-male androgen responsiveness—revisiting the challenge hypothesis. Horm Behav 51:463–476
Grether GF (2000) Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata). Evolution 54:1712–1724
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387
Hegna RH, Saporito RA, Gerow KG, Donnelly MA (2011) Contrasting colors of an aposematic poison frog do not affect predation. Ann Zool Fenn 48:29–38
Hill GE, Johnson JD (2012) The vitamin A-redox hypothesis: a biochemical basis for honest signaling via carotenoid pigmentation. Am Nat 180:E127–E150
Holen OH, Svennungsen TO (2012) Aposematism and the handicap principle. Am Nat 180:629–641
Jiggins CD, Naisbit RE, Coe RL, Mallet J (2001) Reproductive isolation caused by colour pattern mimicry. Nature 411:302–305
Johnstone RA, Norris K (1993) Badges of status and the cost of aggression. Behav Ecol Sociobiol 32:127–134
Kendall MG (1955) Rank correlation methods. Hafner, New York
Kimball RT, Ligon JD (1999) Evolution of avian plumage dichromatism from a proximate perspective. Am Nat 154:182–193
Kime NM, Turner WR, Ryan MJ (2000) The transmission of advertisement calls in Central American frogs. Behav Ecol 11:71–83
Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav Ecol Sociobiol 25:393–401
Lee TJ, Speed MP, Stephens PA (2011) Honest signaling and the uses of prey coloration. Am Nat 178:E1–E9
Lynch KS, Crews D, Ryan MJ, Wilczynski W (2006) Hormonal state influences aspects of female mate choice in the Túngara frog (Physalaemus pustulosus). Horm Behav 49:450–457
Maan ME, Cummings ME (2008) Female preferences for aposematic signal components in a polymorphic poison frog. Evolution 62:2334–2345
Maan ME, Cummings ME (2009) Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog. Proc Natl Acad Sci USA 106:19072–19077
Maan ME, Cummings ME (2012) Poison frog colors are honest signals of toxicity, particularly for bird predators. Am Nat 17:E1–E14
Marler CA, Ryan MJ (1996) Energetic constraints and steroid hormone correlates of male calling behaviour in the túngara frog. J Zool Lond 240:397–409
Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, Oxford
McGraw KJ (2005) The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Anim Behav 69:757–764
McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712
McGraw KJ, Nolan PM, Crino OL (2006) Carotenoid accumulation strategies for becoming a colorful house finch: analyses of plasma and liver pigments in wild molting birds. Funct Ecol 20:678–688
Moore IT, Jessop TS (2003) Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm Behav 43:39–47
Mosconi G, Palermo F, Carotti M, Kikuyama S, Yamamoto K, Polzonetti-Magni AM (2007) Neuroendocrine modulation of stress response in the anuran, Rana esculenta. Amphibia-Reptilia 27:401–408
Müller F (1879) Ituna and Thyridia: a remarkable case of mimicry in butterflies. Trans Entomol Soc Lond 1879:xx–xxix
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 279:257–265
Obika M, Bagnara JT (1964) Pteridines as pigments in amphibians. Science 143:485–487
Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514
Owens IPF, Short RV (1995) Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol Evol 10:44–47
Richards CM (1982) The alteration of chromatophore expression by sex hormones in the Kenyan reed frog, Hyperolius viridiflavus. Gen Comp Endocr 46:59–67
Rudh A, Qvarnström A (2013) Adaptive coloration in amphibians. Semin Cell Dev Biol 24:553–561
Rudh A, Rogel B, Håstad O, Qvarnström A (2011) Rapid population divergence linked with co-variation between coloration and sexual display in strawberry poison frogs. Evolution 65:1271–1282
Rudh A, Breed MF, Qvarnström A (2013) Does aggression and explorative behaviour decrease with lost warning coloration? Biol J Linn Soc 108:116–126
Ryan MJ, Keddy-Hector A (1992) Directional patterns of female mate choice and the role of sensory biases. Am Nat 139:S4–S35
R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-07-0. http://www.R-project.org/
Saks L, McGraw K, Hõrak P (2003) How feather colour reflects its carotenoid content. Funct Ecol 17:555–561
Santos JC, Cannatella DC (2011) Phenotypic integration emerges from aposematism and scale in poison frogs. Proc Natl Acad Sci USA 108:6175–6180
Saporito RA, Donnelly MA, Garraffo HM, Spande TF, Daly JW (2006) Geographic and seasonal variation in alkaloid-based chemical defenses of Dendrobates pumilio from Bocas del Toro, Panama. J Chem Ecol 32:795–814
Saporito RA, Zuercher R, Roberts M, Gerow KG, Donnelly MA (2007a) Experimental evidence for aposematism in the dendrobatid poison frog Oophaga pumilio. Copeia 4:1006–1011
Saporito RA, Donnelly MA, Jain P, Garraffo HM, Spande TF, Daly JW (2007b) Spatial and temporal patterns of alkaloid variation in the poison frog Oophaga pumilio in Costa Rica and Panama over 30 years. Toxicon 50:757–778
Saporito RA, Donnelly MA, Madden AA, Garraffo HM, Spande TF (2010) Sex-related differences in alkaloid chemical defenses of the dendrobatid frog Oophaga pumilio from Cayo Nancy, Bocas del Toro, Panama. J Nat Prod 73:317–321
Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: ‘magic’ but not rare? Trends Ecol Evol 26:389–397
Sinervo B, Miles DB, Frankino WA, Klukowski M, DeNardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38:222–233
Speed MP, Ruxton GD (2007) How bright and how nasty: explaining diversity in warning signal strength. Evolution 61:623–635
Speed MP, Ruxton GD, Blount JD, Stephens PA (2010) Diversification of honest signals in a predator-prey system. Ecol Lett 13:744–753
Speed MP, Ruxton GD, Mappes J, Sherratt TN (2012) Why are defensive toxins so variable? An evolutionary perspective. Biol Rev 87:874–884
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
Summers K, Symula R, Clough M, Cronin T (1999) Visual mate choice in poison frogs. Proc R Soc B 266:2141–2145
Summers K, Speed MP, Blount JD, Stuckert AMM (2015) Are aposematic signals honest? A review. J Evol Biol 28:1583–1599
Ten Eyck GR, ul Haq A (2012) Arginine vasotocin activates aggressive calls during parental care in the Puerto Rican coquí frog, Eleutherodactylus coqui. Neurosci Lett 525:152–156
Wallace AR (1867) Proc Entomol Soc Lond March 4th, IXXX–IXXXi
Weiss SL, Foerster K, Hudon J (2012) Pteridine, not carotenoid, pigments underlie the female-specific orange ornament of striped plateau lizards (Sceloporus virgatus). Comp Biochem Phys B 161:117–123
Whiting MJ, Nagy KA, Bateman PW (2003) Evolution and maintenance of social status signaling badges: experimental manipulations in lizards. In: Fox SF, McCoy JK, Baird TA (eds) Lizard social behavior. Johns Hopkins University Press, Baltimore, pp 47–82
Whiting MJ, Stuart-Fox DM, O’Connor D, Firth D, Bennett NC, Blomberg SP (2006) Ultraviolet signals ultra-aggression in a lizard. Anim Behav 72:353–363
Wilczynski W, Lynch KS, O’Bryant EL (2005) Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology. Horm Behav 38:440–450
Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846
Acknowledgments
This work complied with ANAM SE/A-112-08, SE/A-27-09, SEX/A-58-09, SE/A-30-11 and SE/A-36-12 permits, and UT 07092101 and AUP-2010-00139, Tulane 0382R and STRI 2008-03-12-05-2008 IACUC protocols. We thank Christina Buelow, Victoria Flores, Sara Mason and Anna Deasey for their exceptional field help, and Clyde and Wilson Stephens for the generous use of their property over the years. Special thanks to Hans Hofmann, Daniel Bolnick, Michael Ryan, Kyle Summers, William Wcislo, John Christy, and David Cannatella for their advice on experimental protocols. Finally, we thank two anonymous reviewers and the editors for helpful comments on previous versions of this manuscript. L.C. was supported by a UT EEB grant, NSF DDIG #IOS 1110503, a Smithsonian Tropical Research Institute A. Stanley Rand fellowship, an Animal Behavior Society Barlow Student Research Award, and an American Association of University Women fellowship. L.C. and M.C. were supported by a National Geographic Society Committee for Research and Exploration grant.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Crothers, L., Saporito, R.A., Yeager, J. et al. Warning signal properties covary with toxicity but not testosterone or aggregate carotenoids in a poison frog. Evol Ecol 30, 601–621 (2016). https://doi.org/10.1007/s10682-016-9830-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-016-9830-y