Rapid population divergence linked with co-variation between coloration and sexual display in strawberry poison frogs

Evolution

Volumn 65, Issue 5, 2011, Pages 1271-1282

  Rudh, Andreas ^a   Rogell, Björn ^a   Håstad, Olle ^a   Qvarnström, Anna ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Aposematism; Natural selection; Oophaga pumilio; Population differentiation; Sexual selection; Speciation

Indexed keywords

ADAPTATION; APOSEMATISM; COLOR MORPH; COVARIANCE ANALYSIS; FROG; PHENOTYPIC PLASTICITY; REPRODUCTIVE SUCCESS; SEXUAL SELECTION; SPECIATION (BIOLOGY);

ANIMAL; ANIMAL COMMUNICATION; ARTICLE; EVOLUTION; FEMALE; FOOD CHAIN; FROGS AND TOADS; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; MALE; PANAMA; PHYSIOLOGY; SEXUAL BEHAVIOR;

ANIMAL COMMUNICATION; ANIMALS; ANURA; BIOLOGICAL EVOLUTION; FEMALE; FOOD CHAIN; GENETIC VARIATION; MALE; PANAMA; SELECTION, GENETIC; SEXUAL BEHAVIOR, ANIMAL;

DENDROBATES PUMILIO; DENDROBATIDAE; FRAGARIA X ANANASSA;

EID: 79955154512     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2010.01210.x     Document Type: Article

References (83)

1. Anderson, R. P., and C. O. Handley 2001. A new species of three-toed sloth (Mammalia: Xenarthra) from Panama, with a review of the genus Bradypus. Proc. Biol. Soc. Washington 114:1-33.
2. Anderson, R. P., and C. O. Handley 2002. Dwarfism in insular sloths: biogeography, selection, and evolutionary rate. Evolution 56:1045-1058.
3. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ
4. Ardren, W. R., and A. R. Kapuscinski 2003. Demographic and genetic estimates of effective population size (N-e) reveals genetic compensation in steelhead trout. Mol. Ecol. 12:35-49.
5. Bagnara, J., J. Taylor, and M. Hadley 1968. The dermal chromatophore unit. J. Cell Biol. 38:67-79.
6. Baugh, J. R., and D. C. Forester 1994. Prior residence effect in the dart-poison frog, dendrobates pumilio. Behaviour 131:207-224.
7. Brown, J. L., M. E. Maan, M. E. Cummings, and K. Summers 2010. Evidence for selection on coloration in a Panamanian poison frog: a coalescent-based approach. J. Biogeogr. 37:891-901.
8. Brust, D. G. 1993. Maternal brood care by dendrobates pumilio-a frog that feeds its young. J. Herpetol. 27:96-98.
9. Coyne, J. A., and H. A. Orr 2004. Speciation. Sinauer Associates, Inc, Sunderland, MA
10. Crawley, M. J. 2007. The R book. John Wiley & Sons Ltd, Chichester
11. Daly, J. W., and C. W. Myers 1967. Toxicity of Panamanian poison frogs (Dendrobates): some biological and chemical aspects. Science 156:970-973.
12. Darwin, C. 1859. On the origin of species by means of natural selection. John Murray, London
13. Eizaguirre, C., T. L. Lenz, A. Traulsen, and M. Milinski 2009. Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. Ecol. Lett. 12:5-12.
14. Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals. Evolution 35:124-138.
15. Forsman, A., and S. Merilaita 1999. Fearful symmetry: pattern size and asymmetry affects aposematic signal efficacy. Evol. Ecol. 13:131-140.
16. Frost, S. K., and S. J. Robinson 1984. Pigment cell differentiation in the fire-bellied toad, bombina orientalis. I. Structural, chemical, and physical aspect of the adult pigment pattern. J. Morphol. 179:229-242.
17. Gavrilets, S. 2004. Fitness landscapes and the origin of species. Princeton Univ. Press, Princeton, NJ
18. Gittleman, J. L., and P. H. Harvey 1980. Why are distasteful prey not cryptic? Nature 286:149-150.
19. Gittleman, J. L., P. H. Harvey, and P. J. Greenwood 1980. The evolution of conspicuous coloration some experiments in bad taste. Anim. Behav. 28:897-899.
20. Graves, B. M., K. A. Stanley, and E. A. Gardner 2005. Correlates of vocal display in a Costa Rican population of Strawberry Poison-Dart Frogs, Dendrobates pumilio. J. Herpetol. 39:101-107.
21. Hagemann, S., and H. Prohl 2007. Mitochondrial paraphyly in a polymorphic poison frog species (Dendrobatidae; D-pumilio). Mol. Phylogenet. Evol. 45:740-747.
22. Hagman, M., and A. Forsman 2003. Correlated evolution of conspicuous coloration and body size in poison frogs (dendrobatidae). Evolution 57:2904-2910.
23. Hagman, M., and A. Forsman 2002. Vision in the peafowl (Aves: Pavo cristatus). J. Exp. Biol. 205:3925-3935.
24. Hart, N. S., and D. M. Hunt 2007. Avian visual pigments: characteristics, spectral tuning, and evolution. Am. Nat. 169:S7-S26.
25. Håstad, O., and A. Ödeen 2008. Different ranking of avian colors predicted by modeling of retinal function in humans and birds. Am. Nat. 171:831-838.
26. Jiggins, C. D., R. E. Naisbit, R. L. Coe, and J. Mallet 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411:302-305.
27. Kaneshiro, K. 1989. The dynamics of sexual selection and founder effects in speciation formation. Pp. 279-296 in L. Giddings, K. Kaneshiro, and W. Anderson, eds. Genetics, speciation and the founder principle. Oxford Univ. Press, Oxford
28. Kotiaho, J., R. V. Alatalo, J. Mappes, S. Parri, and A. Rivero 1998. Male mating success and risk of predation in a wolf spider: a balance between sexual and natural selection? J. Anim. Ecol. 67:287-291.
29. Kuchta, S. R., A. H. Krakauer, and B. Sinervo 2008. Why does the Yellow-eyed ensatina have yellow eyes? Batesian mimicry of Pacific newts (genus Taricha) by the salamander Ensatina eschscholtzii xanthoptica. Evolution 62:984-990.
30. Limerick, S. 1980. Courtship behaviour and oviposition of the poison-arrow frog Dendrobates pumilio. Herpetologica 36:69-71.
31. Maan, M. E., and M. E. Cummings 2008. Female preferences for aposematic signal components in a polymorphic poison frog. Evolution 62:2334-2345.
32. Maan, M. E., and M. E. Cummings 2009. Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog. Proc. Natl. Acad. Sci. USA 106:19072-19077.
33. Mappes, J., N. Marples, and J. A. Endler 2005. The complex business of survival by aposematism. Trends Ecol. Evol. 20:598-603.
34. Martins, E. P., and T. F. Hansen 1997. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149:646-667.
35. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA
36. Nagel, L., and D. Schluter 1998. Body size, natural selection, and speciation in sticklebacks. Evolution 52:209-218.
37. Noonan, B. P., and A. A. Comeault 2009. The role of predator selection on polymorphic aposematic poison frogs. Biol. Lett. 5:51-54.
38. Nosil, P., L. J. Harmon, and O. Seehausen 2009. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 24:145-156.
39. Ödeen, A., and M. Björklund 2003. Dynamics in the evolution of sexual traits: losses and gains, radiation and convergence in yellow wagtails (Motacilla flava). Mol. Ecol. 12:2113-2130.
40. Orr, M. R., and T. B. Smith 1998. Ecology and speciation. Trends Ecol. Evol. 13:502-506.
41. Osorio, D., A. C. Smith, M. Vorobyev, and H. M. Buchanan-Smith 2004. Detection of fruit and the selection of primate visual pigments for color vision. Am. Nat. 164:696-708.
42. Panhuis, T. M., R. Butlin, M. Zuk, and T. Tregenza 2001. Sexual selection and speciation. Trends Ecol. Evol. 16:364-371.
43. Paradis, E., J. Claude, and K. Strimmer 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
44. Pinheiro, J., D. Bates, S. DebRoy, D. Sakar, and the R Core team 2008. nlme: linear and nonlinear mixed effects models. R package.
45. Poulin, B., G. Lefebvre, R. Ibanez, C. Jaramillo, C. Hernandez, and A. S. Rand 2001. Avian predation upon lizards and frogs in a neotropical forest understorey. J. Trop. Ecol. 17:21-40.
46. Poulton, E. B. 1890. The colours of animals. Their meaning and use. Especially considered in the case of insects. D. Appelton and Company, New York, New York
47. Price, T. 1998. Sexual selection and natural selection in bird speciation. Philos. Trans. R. Soc. Lond. B353:251-260.
48. Pröhl, H. 2005. Territorial behavior in dendrobatid frogs. J. Herpetol. 39:354-365.
49. Pröhl, H., and W. Hödl 1999. Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog, Dendrobates pumilio. Behav. Ecol. Sociobiol. 46:215-220.
50. Pröhl, H., and O. Berke 2001. Spatial distributions of male and female strawberry poison frogs and their relation to female reproductive resources. Oecologia 129:534-542.
51. Przeczek, K., C. Mueller, and S. M. Vamosi 2008. The evolution of aposematism is accompanied by increased diversification. Integr. Zool. 3:149-156.
52. R-Development-Core-Team. 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
53. Reynolds, R. G., and B. M. Fitzpatrick 2007. Assortative mating in poison-dart frogs based on an ecologically important trait. Evolution 61:2253-2259.
54. Rice, W. R., and E. E. Hostert 1993. Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47:1637-1653.
55. Ritchie, M. G. 2007. Sexual selection and speciation. Annu. Rev. Ecol. Evol. Syst. 38:79-102.
56. Rudh, A., B. Rogell, and J. Höglund 2007. Non-gradual variation in colour morphs of the strawberry poison frog Dendrobates pumilio: genetic and geographical isolation suggest a role for selection in maintaining polymorphism. Mol. Ecol. 16:4284-4294.
57. Ruxton, G. D., T. N. Sherratt, and M. P. Speed 2006. Avoiding attack. The evolutionary ecology of crypsis, warning signals & mimicry. Oxford Univ. press, Oxford
58. Santos, J. C., L. A. Coloma, and D. C. Cannatella 2003. Multiple, recurring origins of aposematism and diet specialization in poison frogs. Proc. Natl. Acad. Sci. USA 100:12792-12797.
59. Saporito, R. A., H. M. Garraffo, M. A. Donnelly, A. L. Edwards, J. T. Longino, and J. W. Daly 2004. Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. Proc. Natl. Acad. Sci. USA 101:8045-8050.
60. Saporito, R. A., M. A. Donnelly, H. M. Garraffo, T. F. Spande, and J. W. Daly 2006. Geographic and seasonal variation in alkaloid-based chemical defenses of Dendrobates pumilio from Bocas del Toro, Panama. J. Chem. Ecol. 32:795-814.
61. Saporito, R. A., M. A. Donnelly, R. A. Norton, H. M. Garraffo, T. F. Spande, and J. W. Daly 2007a. Oribatid mites as a major dietary source for alkaloids in poison frogs. Proc. Natl. Acad. Sci. USA 104:8885-8890.
62. Saporito, R. A., R. Zuercher, M. Roberts, K. G. Gerow, and M. A. Donnelly 2007b. Experimental evidence for aposematism in the dendrobatid poison frog Oophaga pumilio. Copeia 4:1006-1011.
63. Savage, J. M. 2002. The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. Univ. of Chicago Press, Chicago, IL
64. Schaefer, H.-C., M. Vences, and M. Veith 2002. Molecular phylogeny of Malagasy poison frogs, genus Mantella (Anura: Mantellidae): homoplastic evolution of colour pattern in aposematic amphibians. Org. Divers. Evol. 2:97-105.
65. Schluter, D. 2001. Ecology and the origin of species. Trends Ecol. Evol. 16:372-380.
66. Servedio, M. R. 2008. The role of linkage disequilibrium in the evolution of premating isolation. Heredity 102:51-56.
67. Siddiqi, A., T. W. Cronin, E. R. Loew, M. Vorobyev, and K. Summers 2004. Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J. Exp. Biol. 207:2471-2485.
68. Stevens, M., C. J. Hardman, and C. L. Stubbins 2008. Conspicuousness, not eye mimicry, makes "eyespots" effective antipredator signals. Behav. Ecol. 19:525-531.
69. Summers, K., E. Bermingham, L. Weigt, and S. McCafferty 1997. Phenotypic and genetic divergence in three species of dart-poison frogs with contrasting parental behavior. J. Hered. 88:8-13.
70. Summers, K., R. Symula, M. Clough, and T. Cronin 1999. Visual mate choice in poison frogs. Proc. R. Soc. Lond. B 266:2141-2145.
71. Summers, K., T. W. Cronin, and T. Kennedy 2003. Variation in spectral reflectance among populations of Dendrobates pumilio, the strawberry poison frog, in the Bocas del Toro Archipelago, Panama. J. Biogeogr. 30:35-53.
72. Summers, K., T. W. Cronin, and T. Kennedy 2004. Cross-breeding of distinct color morphs of the strawberry poison frog (Dendrobates pumilio) from the Bocas del Toro Archipelago, Panama. J. Herpetol. 38:1-8.
73. Sumner, P., C. A. Arrese, and J. C. Partridge 2005. The ecology of visual pigment tuning in an Australian marsupial: the honey possum Tarsipes rostratus. J. Exp. Biol. 208:1803-1815.
74. Tazzyman, S. J., and Y. Iwasa 2010. Sexual selection can increase the effect of random genetic drift-a quantitative model of polymorphism in O. pumilio, the strawberry poison-dart frog. Evolution 64:1719-1728.
75. v. Campenhausen, M., and K. Kirschfeld 1998. Spectral sensitivity of the accessory optic system of the pigeon. J. Comp. Physiol. A 183:1-6.
76. Vences, M., J. Kosuch, R. Boistel, C. F. B. Haddad, E. La Marca, S. Lotters, and M. Veith 2003. Convergent evolution of aposematic coloration in Neotropical poison frogs: a molecular phylogenetic perspective. Org. Divers. Evol. 3:215-226.
77. Via, S. 1999. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53:1446-1457.
78. Vorobyev, M. 2003. Coloured oil droplets enhance colour discrimination. Proc. R. Soc. Lond. B 270:1255-1261.
79. Vorobyev, M., and D. Osorio 1998. Receptor noise as a determinant of colour thresholds. Proc. R. Soc. Lond. B 265:351-358.
80. Wang, I. J., and H. B. Shaffer 2008. Rapid color evolution in an aposematic species: a phylogenetic analysis of color variation in the strikingly polymorphic strawberry poison-dart frog. Evolution 62:2742-2759.
81. Wang, I. J., and K. Summers 2010. Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison-dart frog. Mol. Ecol. 19:447-458.
82. West-Eberhard, M. J. 1983. Sexual selection, social competition, and speciation. Q. Rev. Biol. 58:155-183.
83. Weygoldt, P. 1980. Complex brood care and reproductive behavior in captive poison-arrow frogs, dendrobates pumilio O. Schmidt. Behav. Ecol. Sociobiol. 7:329-332.