Oecologia

, Volume 168, Issue 1, pp 109–118 | Cite as

Larval growth in polyphenic salamanders: making the best of a bad lot

  • H. H. Whiteman
  • S. A. Wissinger
  • M. Denoël
  • C. J. Mecklin
  • N. M. Gerlanc
  • J. J. Gutrich
Population ecology - Original Paper

Abstract

Polyphenisms are excellent models for studying phenotypic variation, yet few studies have focused on natural populations. Facultative paedomorphosis is a polyphenism in which salamanders either metamorphose or retain their larval morphology and eventually become paedomorphic. Paedomorphosis can result from selection for capitalizing on favorable aquatic habitats (paedomorph advantage), but could also be a default strategy under poor aquatic conditions (best of a bad lot). We tested these alternatives by quantifying how the developmental environment influences the ontogeny of wild Arizona tiger salamanders (Ambystoma tigrinum nebulosum). Most paedomorphs in our study population arose from slow-growing larvae that developed under high density and size-structured conditions (best of a bad lot), although a few faster-growing larvae also became paedomorphic (paedomorph advantage). Males were more likely to become paedomorphs than females and did so under a greater range of body sizes than females, signifying a critical role for gender in this polyphenism. Our results emphasize that the same phenotype can be adaptive under different environmental and genetic contexts and that studies of phenotypic variation should consider multiple mechanisms of morph production.

Keywords

Polyphenism Density dependence Size structure Facultative paedomorphosis Ambystoma tigrinum 

Notes

Acknowledgments

This long-term research could not have been completed without the support and assistance of numerous colleagues, research assistants, funding agencies, and friends. We particularly thank R.D. Howard for his unending and much needed advice, wisdom, revisions, and patience during the initial phases of this project. W. Brown, A. Benson, J. Boynton, E. Olson, J. Doyle, J. Earl, A. Bohonak, S. Horn, G. McCrabb, R. Moorman, J. Marcus, J. McGrady-Steed, K. Buhn, D. Weigel, G. Maruca, M. Hatfield, C. Eden, H. Grieg, R. Schultheis, S. Mattie, D. Dale, M. Mumford, C. Aubee, E. Bruneau, M. Galatowitsch, M. O’Brien, and S. Thomason provided field and intellectual assistance. P. Waser, J. Lucas, N. Buschhaus, J. Young, M. Brown, A. Bohonak, J. Haydock, J. Doyle, K. Landholt, and J. Earl reviewed previous versions of the manuscript. J. Hetfield, L. Ulrich, K. Hammett, R. Trujillo, J. Newstead, and C. Burton provided intense encouragement. I. Billick, B. Barr, S. Donovan, S. Lohr, T. Allison and L. Swift have provided much needed aid and assistance at the RMBL, and W. Gibbons, R. Semlitsch, D. White, G. Kipphut, and R. Fister patiently supported this work. M. Denoël was a Research Associate at the Fonds de la Recherche Scientifique (FRS-FNRS) during this research. This research was funded by a Purdue David Ross Summer Fellowship, a Purdue Research Foundation Fellowship, the American Museum of Natural History (Theodore Roosevelt Fund), Sigma Xi (Grant in Aid), the Rocky Mountain Biological Laboratory (Lee R. G. Snyder Memorial Fund), the American Society of Ichthyologists and Herpetologists (Helen Gaige Fund), the Animal Behavior Society (ABS Research Grant), the Colorado Division of Wildlife, the American Philosophical Society, the Murray State University Center for Institutional Studies and Research (CISR), a CISR Presidential Research Fellowship, a Fulbright Fellowship (MD), the Fonds National de la Recherche Scientifique (FRS-FNRS grants 1.5.011.03, 1.5.120.04, F.4718.06, 1.5.199.07, 1.5.013.08, and 1.5.010.09) and the National Science Foundation (DEB 9122981 and DEB 0109436 to HW; BSR 8958253, DEB 9407856, and DEB 010893 to SAW; EPI 0132295 to G. Kipphut; and UBM 0531865 to R. Fister).

References

  1. Aukema B (1995) The adaptive signficance of wing dimorphism in carabid beetles. Res Popul Ecol 37:105–110CrossRefGoogle Scholar
  2. Behler JL, King FW (1979) The Audubon Society field guide to North American reptiles and amphibians. Knopf, New YorkGoogle Scholar
  3. Bizer JR (1978) Growth rates and size at metamorphosis of high elevation populations of Ambystoma tigrinum. Oecologia 34:175–184CrossRefGoogle Scholar
  4. Brunkow PE, Collins JP (1996) Effects of individual variation in size on growth and development of larval salamanders. Ecology 77:1483–1492CrossRefGoogle Scholar
  5. Brunkow PE, Collins JP (1998) Group size structure affects patterns of aggression in larval salamanders. Behav Ecol 9:508–514CrossRefGoogle Scholar
  6. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135PubMedCrossRefGoogle Scholar
  7. Caswell H (1983) Phenotypic plasticity in life-history traits: demographic effects and evolutionary consequences. Am Zool 23:35–46Google Scholar
  8. Church DR, Bailey LL, Wilbur HM, Kendall WL, Hines JE (2007) Iteroparity in the variable environment of the salamander Ambystoma tigrinum. Ecology 88:891–903PubMedCrossRefGoogle Scholar
  9. Collins JP (1981) Distribution, habitats, and life history variation in the tiger salamander, Ambystoma tigrinum, in east-central and southeast Arizona. Copeia 1981:666–675CrossRefGoogle Scholar
  10. Denoël M, Hervant F, Schabetsberger R, Joly P (2002) Short- and long- term advantages of an alternative ontogenetic pathway. Biol J Linn Soc 77:105–112CrossRefGoogle Scholar
  11. Denoël M, Joly P, Whiteman HH (2005) Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biol Rev 80:663–671PubMedCrossRefGoogle Scholar
  12. Denoël M, Whiteman HH, Wissinger SA (2007) Foraging tactics in alternative heterochronic salamander morphs: trophic quality of ponds matters more than water permanency. Freshw Biol 52:1667–1676CrossRefGoogle Scholar
  13. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81PubMedCrossRefGoogle Scholar
  14. Doyle JM, Whiteman HH (2008) Paedomorphosis in Ambystoma talpoideum: effects of initial size variation and density. Oecologia 156:87–94PubMedCrossRefGoogle Scholar
  15. Emlen DJ, Hunt J, Simmons LW (2005) Evolution of sexual dimorphism and male dimorphism in the expression of beetle horns: phylogenetic evidence for modularity, evolutionary lability, and constraint. Am Nat 166:S42–S68PubMedCrossRefGoogle Scholar
  16. Emlen DJ, Corley Lavine L, Ewen-Campen B (2007) On the origin and evolutionary diversification of beetle ‘horns’. Proc Natl Acad Sci USA 104:8661–8668PubMedCrossRefGoogle Scholar
  17. Feder ME, Burggren WW (1992) Environmental physiology of the amphibians. University of Chicago Press, ChicagoGoogle Scholar
  18. Frankino WA, Pfennig DW (2001) Condition-dependent expression of trophic polyphenism: effects of individual size and competitive ability. Evol Ecol Res 3:939–951Google Scholar
  19. Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98PubMedCrossRefGoogle Scholar
  20. Harris RN (1987) Density-dependent paedomorphosis in the salamander Notophthalmus viridescens dorsalis. Ecology 68:705–712CrossRefGoogle Scholar
  21. Harris RN, Semlitsch RD, Wilbur HM, Fauth JE (1990) Local variation in the genetic basis of paedomorphosis in the salamander Ambystoma talpoideum. Evolution 44:1588–1603CrossRefGoogle Scholar
  22. Hazel WN, Smock R, Johnson MD (1990) A polygenic model for the evolution and maintenance of conditional strategies. Proc R Soc Lond B 242:181–187CrossRefGoogle Scholar
  23. Hazel W, Smock R, Lively CM (2004) The ecological genetics of conditional strategies. Am Nat 163:888–900PubMedCrossRefGoogle Scholar
  24. Johnson E, Whiteman HH, Bierzchudek P (2003) Potential of prey size and type to affect foraging asymmetries in tiger salamander larvae (Ambystoma tigrinum nebulosum). Can J Zool 81:1726–1735CrossRefGoogle Scholar
  25. Kikuyama S, Yamamoto K, Kobayashi T, Tonon MC, Galas L, Vaudry H (2005) Hormonal regulation of growth in amphibians. In: Heatwole H (ed) Amphibian biology, endocrinology, vol 6. Surrey Beatty, Chipping Norton, pp 2267–2300Google Scholar
  26. Maret TJ, Collins JP (1997) Ecological origin of morphological diversity: a study of alternative trophic phenotypes in larval salamanders. Evolution 51:898–905CrossRefGoogle Scholar
  27. McPeek MA, Holt RD (1992) The evolution of dispersal in spatially and temporally varying environments. Am Nat 140:1010–1027CrossRefGoogle Scholar
  28. Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of phenotypic plasticity in wild populations. J Evol Biol 20:831–844PubMedCrossRefGoogle Scholar
  29. Persson L, Byström P, Wahlström E (2000) Cannibalism and competition in Eurasian perch: population dynamics of an ontogenetic omnivore. Ecology 81:1058–1071CrossRefGoogle Scholar
  30. Persson L, Claessen D, de Roos AM, Byström P, Sjögren S, Svanbäck R, Westman E (2004) Cannibalism in a size-structured population: energy extraction and control. Ecol Monogr 74:135–157CrossRefGoogle Scholar
  31. Pfennig DW (1992) Polyphenism in spadefoot toad tadpoles as a locally-adjusted evolutionarily stable strategy. Evolution 46:1408–1420CrossRefGoogle Scholar
  32. Pfennig DW, McGee M (2010) Resource polyphenism increases species richness: a test of the hypotheses. Phil Trans R Soc Lond B 365:577–591CrossRefGoogle Scholar
  33. Pfennig DW, Rice AM, Martin RA (2007) Field and experimental evidence for competition’s role in phenotypic divergence. Evolution 61:257–271PubMedCrossRefGoogle Scholar
  34. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting C, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467PubMedCrossRefGoogle Scholar
  35. Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture-recapture experiments. Wildl Monogr 107:1–97Google Scholar
  36. Relyea RA (2002) Costs of phenotypic plasticity. Am Nat 159:272–282PubMedCrossRefGoogle Scholar
  37. Roff DA (1986) The evolution of wing dimorphisms in insects. Evolution 40:1009–1020CrossRefGoogle Scholar
  38. Roff DA (1994) Why is there so much genetic variation for wing dimorphism? Res Popul Ecol 36:145–150CrossRefGoogle Scholar
  39. Roff DA (1996) The evolution of threshold traits in animals. Q Rev Biol 71:3–35CrossRefGoogle Scholar
  40. Roff DA, Fairbairn DJ (1993) The evolution of alternative morphologies: fitness and wing morphology in male sand crickets. Evolution 47:1572–1584CrossRefGoogle Scholar
  41. Roff DA, Mostowy S, Fairbairn DJ (2002) The evolution of trade-offs: testing predictions on response to selection and environmental variation. Evolution 56:84–95PubMedGoogle Scholar
  42. Roff DA, Crnokrak P, Fairbairn DJ (2003) The evolution of trade-offs: geographic variation in call duration and flight ability in the sand cricket, Gryllus firmus. J Evol Biol 16:744–753PubMedCrossRefGoogle Scholar
  43. Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Syst 24:35–68CrossRefGoogle Scholar
  44. Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693CrossRefGoogle Scholar
  45. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, SunderlandGoogle Scholar
  46. Semlitsch RD (1985) Reproductive strategy of a facultatively paedomorphic salamander Ambystoma talpoideum. Oecologia 65:305–313CrossRefGoogle Scholar
  47. Sexton OJ, Bizer JR (1978) Life history patterns of Ambystoma tigrinum in montane Colorado. Am Midl Nat 99:101–118CrossRefGoogle Scholar
  48. Smith CK (1990) Effects of variation in body size on intraspecific competition among larval salamanders. Ecology 71:1777–1788CrossRefGoogle Scholar
  49. Smith-Gill SJ (1983) Developmental plasticity: developmental conversion versus phenotypic modulation. Am Zool 23:47–55Google Scholar
  50. Stearns SC (1992) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  51. Stiffler DF (2005) Endocrine control of water and electrolyte balance in amphibians. In: Heatwole H (ed) Amphibian biology, endocrinology, vol 6. Surrey Beatty, Chipping Norton, Australia, pp 2301–2326Google Scholar
  52. Thompson JD (1991) Phenotypic plasticity as a component of evolutionary change. Trends Ecol Evol 6:246–249PubMedCrossRefGoogle Scholar
  53. Tomkins JL, Hazel W (2007) The status of the conditional evolutionarily stable strategy. Trends Ecol Evol 22:522–528PubMedCrossRefGoogle Scholar
  54. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
  55. Van Buskirk J, Smith DC (1991) Density-dependent population regulation in a salamander. Ecology 72:1747–1756CrossRefGoogle Scholar
  56. Via S (2001) Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol Evol 16:381–390PubMedCrossRefGoogle Scholar
  57. Via S, Gromulkiewicz R, de Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217PubMedCrossRefGoogle Scholar
  58. Wakano JY, Whiteman HH (2008) Evolution of polyphenism: the role of density and relative body size in morph determination. Evol Ecol Res 10:1157–1172Google Scholar
  59. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size- structured populations. Annu Rev Ecol Syst 15:393–425CrossRefGoogle Scholar
  60. West-Eberhard MJ (1986) Alternative adaptations, speciation, and phylogeny (a review). Proc Natl Acad Sci USA 83:1388–1392PubMedCrossRefGoogle Scholar
  61. West-Eberhard MJ (1989) Phenotypic plasticity and the evolution of diversity. Annu Rev Ecol Syst 20:249–278CrossRefGoogle Scholar
  62. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New YorkGoogle Scholar
  63. West-Eberhard MJ (2005) Developmental plasticity and the origin of species differences. Proc Nat Acad Sci USA 102:6543–6549PubMedCrossRefGoogle Scholar
  64. Whiteman HH (1994) Evolution of facultative paedomorphosis in salamanders. Q Rev Biol 69:205–221CrossRefGoogle Scholar
  65. Whiteman HH (1997) Maintenance of polymorphism promoted by sex-specific fitness payoffs. Evolution 51:2039–2044CrossRefGoogle Scholar
  66. Whiteman HH, Semlitsch RD (2005) Asymmetric reproductive isolation among polymorphic salamanders. Biol J Linn Soc 86:265–281CrossRefGoogle Scholar
  67. Whiteman HH, Wissinger SA (2005) Amphibian population cycles and long-term data sets. In: Lannoo ML (ed) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, pp 177–184Google Scholar
  68. Whiteman HH, Wissinger SA, Bohonak AJ (1995) Seasonal movement patterns in a subalpine population of the tiger salamander, Ambystoma tigrinum nebulosum. Can J Zool 72:1780–1787CrossRefGoogle Scholar
  69. Whiteman HH, Wissinger SA, Brown WS (1996) Growth and foraging consequences of facultative paedomorphosis in the tiger salamander, Ambystoma tigrinum nebulosum. Evol Ecol 10:433–446CrossRefGoogle Scholar
  70. Whiteman HH, Sheen JP, Johnson E, VanDeusen A, Cargille RT, Sacco T (2003) Heterospecific prey and trophic polyphenism in larval tiger salamanders. Copeia 2003:56–67CrossRefGoogle Scholar
  71. Whiteman HH, Krenz JD, Semlitsch RD (2006) Intermorph breeding and the potential for reproductive isolation in polymorphic mole salamanders (Ambystoma talpoideum). Behav Ecol Sociobiol 60:52–61CrossRefGoogle Scholar
  72. Winne CT, Ryan TJ (2001) Aspects of sex-specific differences in the expression of an alternative life cycle in the salamander Ambystoma talpoideum. Copeia 2001:143–149CrossRefGoogle Scholar
  73. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93CrossRefGoogle Scholar
  74. Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314PubMedCrossRefGoogle Scholar
  75. Wissinger SA (1989) Seasonal variation in the intensity of competition and intraguild predation among dragonfly larvae. Ecology 70:1017–1027CrossRefGoogle Scholar
  76. Wissinger SA, Whiteman HH (1992) Fluctuation in a Rocky Mountain population of salamanders: anthropogenic acidification or natural variation? J Herpetol 26:377–391CrossRefGoogle Scholar
  77. Wissinger SA, Bohonak AJ, Whiteman HH, Brown WS (1999) Subalpine wetlands in Colorado: habitat permanence, salamander predation and invertebrate communities. In: Bazter DP, Wissinger SA (eds) Invertebrates in freshwater wetlands of North America: ecology and management. Wiley, New York, pp 757–790Google Scholar
  78. Wissinger SA, Whiteman HH, Denoël M, Mumford ML, Aubee CB (2010) Consumptive and non-consumptive effects of cannibalism in fluctuating age-structured populations. Ecology 91:549–559PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • H. H. Whiteman
    • 1
    • 6
  • S. A. Wissinger
    • 2
    • 6
  • M. Denoël
    • 3
    • 6
  • C. J. Mecklin
    • 4
  • N. M. Gerlanc
    • 1
    • 6
  • J. J. Gutrich
    • 5
    • 6
  1. 1.Department of Biological Sciences and Watershed Studies InstituteMurray State UniversityMurrayUSA
  2. 2.Biology and Environmental Science DepartmentsAllegheny CollegeMeadvilleUSA
  3. 3.Laboratory of Fish and Amphibian Ethology, Behavioural Biology Unit, Department of Environmental SciencesUniversity of LiègeLiègeBelgium
  4. 4.Department of Mathematics and Statistics and Watershed Studies InstituteMurray State UniversityMurrayUSA
  5. 5.Department of Environmental StudiesSouthern Oregon UniversityAshlandUSA
  6. 6.Rocky Mountain Biological LaboratoryCrested ButteUSA

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