Summary
Facultative paedomorphosis in salamanders occurs when larvae respond to varying environmental conditions by either metamorphosing into terrestrial metamorphic adults or retaining their larval morphology to become sexually mature paedomorphic adults. Several hypotheses have been proposed for the evolutionary maintenance of this environmentally induced dimorphism, but few data are available to assess them adequately. We studied a montane population of the tiger salamander,Ambystoma tigrinum nebulosum, and measured the adult growth rate and body condition across three growing seasons to assess the relative costs and benefits of each morph. Metamorphic adults grew more than paedomorphic adults in terms of snout—vent length across years and in weight within years. Dietary analyses and foraging experiments revealed some of the proximate factors that may underlie these differential growth patterns. Across all prey, metamorphs had significantly higher biomass and calories per stomach sample than paedomorphs. Metamorphic diets primarily consisted of the fairy shrimpBranchinecta coloradensis, whereas paedomorphic diets contained a variety of benthic and terrestrial invertebrates. Foraging experiments revealed that both morphs are more successful at capturing fairy shrimp relative to other prey types and both show high electivity toward this prey. However, fairy shrimp occurred only in non-permanent ponds and thus are inaccessible to paedomorphs, which can survive only in permanent ponds. Paedomorphs also experience higher levels of intraspecific competition with large larvae in permanent ponds than metamorphs do in non-permanent ponds. Thus, metamorphs obtain a growth advantage over paedomorphs by foraging in non-permanent ponds that contain fairy shrimp and have reduced intraspecific competition. These results suggest that paedomorphs should have decreased fitness relative to metamorphs, primarily because metamorphs can move into the best habitats for growth. The net fitness effect of morph-specific differences in dispersal depend on whether there are trade-offs with other life history traits. Nonetheless, because the relative benefit of metamorph dispersal will change with environmental conditions in permanent ponds and the surrounding habitat, the relative fitness payoff to each morph should track changes in the environment. Thus, facultative paedomorphosis may be maintained in part by variable, environmentally-specific fitness payoffs to each morph.
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References
Albrech, P., Gould, S. J., Oster, G. F. and Wake, D. B. (1979) Size and shape in ontogeny and phylogeny.Paleobiology 5, 296–317.
Arak, A. (1983) Male—male competition and mate choice in anuran amphibians. InMate Choice (P. Bateson, ed.), pp. 181–210. Cambridge University Press, Cambridge.
Behler, J. L. and King, F. W. (1979)The Audubon Society Field Guide to North American Reptiles and Amphibians. Alfred A. Knopf, New York.
Bradshaw, A. D. (1965) Evolutionary significance of phenotypic plasticity in plants.Adv. Genet. 13, 115–55.
Brandon, R. A. and Bremer, D. J. (1966) Neotenic newts,Notophthalmus viridescens louisianensis, in southern Illinois.Herpetologica 22, 213–7.
Caswell, H. (1983) Phenotypic plasticity in life-history traits: demographic effects and evolutionary consequences.Am. Zool. 23, 35–46.
Clutton-Brock, T. H. (1988)Reproductive Success. The University of Chicago Press, Chicago, IL.
Collins, J. P. (1981) Distribution, habitats, and life history variation in the tiger salamander,Ambystoma tigrinum, in east-central and southeast Arizona.Copeia 1981, 666–75.
Collins, J. P. and Cheek, J. E. (1983) Effect of food and density on development of typical and cannibalistic salamander larvae inAmbystoma tigrinum nebulosum.Am. Zool. 23, 77–84.
Collins, J. P., Zerba, K. E. and Sredl, M. J. (1993) Shaping intraspecific variation: development, ecology and the evolution of morphology and life history variation in tiger salamanders.Genetica 89, 167–83.
Crespi, B. J. (1988) Adaptation, compromise, and constraint: the development, morphometrics, and behavioral basis of a fighter-flier polymorphism in maleHoplothrips karnyi (Insecta: Thysanoptera).Behav. Ecol. Sociobiol. 23, 93–104.
Cummins, K. W. and Wuycheck, J. C. (1971) Caloric equivalents for investigations in ecological energetics.Verh. Int. Verein. Limnol. 18, 1–158.
Dodson, S. I. (1970) Complementary feeding niches sustained by size-selective predation.Limnol. Oceanogr. 15, 131–7.
Dominey, W. J. (1980) Female mimicry in male bluegill sunfish — a genetic polymorphism?Nature 284, 546–8.
Dominey, W. J. (1981) Maintenance of female mimicry as a reproductive strategy in bluegill sunfish (Lepomis macrochirus).Environ. Biol. Fish. 6, 59–64.
Duméril, A. H. A. (1870) Création d'une race blanche d'axolotl à la ménagerie des reptiles du Muséum d'Historie Naturelle, et remarques sur la transformation de ces batraciens.C.R. Acad. Sci., Paris 70, 782–5.
Duméril, A. H. A. (1872) Notes complémentaires sur les axolotls.Mem. Soc. Linn. N. Fr. 2, 248–51.
Eberhard, W. G. (1979) The function of horns inPodischnus agenor (Dynastinae) and other beetles. InSexual Selection and Reproductive Competition in Insects (M. S. Blum and N. A. Blum, eds), pp. 231–58. Academic Press, New York, NY.
Gould, S. J. (1977)Ontogeny and Phylogeny. Harvard University Press, Cambridge, MA.
Grafen, A. (1988) On the uses of data on lifetime reproductive success. InReproductive Success (T. H. Clutton-Brock, ed.), pp. 454–71. The University of Chicago Press, Chicago, IL.
Gross, M. R. (1982) Sneakers, satellites, and parentals: polymorphic mating strategies in North American sunfishes.Z. Tierpsychol. 60, 1–26.
Gross, M. R. (1991) Salmon breeding behavior and life history evolution in changing environments.Ecology 72, 1180–6.
Harris, R. N. (1987) Density-dependent paedomorphosis in the salamanderNotophthalmus viridescens dorsalis.Ecology 68, 705–12.
Harris, R. N., Semlitsch, R. D., Wilbur, H. M. and Fauth, J. E. (1990) Local variation in the genetic basis of paedomorphosis in the salamanderAmbystoma talpoideum.Evolution 44, 1588–603.
Harrison, R. G. (1980) Dispersal polymorphisms in insects.Annu. Rev. Ecol. Syst. 11, 95–118.
Ivlev, V. S. (1961)Experimental Ecology of the Feeding of Fishes. Yale University Press, New Haven, CT.
Jackson, M. E. and Semlitsch, R. D. (1993) Paedomorphosis in the salamanderAmbystoma talpoideum: effects of a fish predator.Ecology 74, 342–50.
Kaplan, R. H. and Salthe, S. N. (1979) The allometry of reproduction: an empirical view in salamanders.Am. Nat. 113, 671–89.
Lauder, G. V. and Shaffer, H. B. (1986) Functional design of the feeding mechanism in lower vertebrates: unidirectional and bidirectional flow-system in the tiger salamander.Zool. J. Linn. Soc. 88, 277–90.
Levins, R. (1968)Evolution in Changing Environments. Princeton University Press, Princeton, NJ.
Lively, C. M. (1986a) Canalization versus developmental conversion in a spatially variable environment.Am. Nat. 128, 561–72.
Lively, C. M. (1986b) Competition, comparative life histories, and maintenance of shell dimorphism in a barnacle.Ecology 67, 858–64.
Lively, C. M. (1986c) Predator-induced shell dimorphism in the acorn barnacleChthamalus anisopoma.Evolution 40, 232–42.
Lloyd, D. G. (1984) Variation strategies of plants in heterogeneous environments.Biol. J. Linn. Soc. 21, 357–85.
McKinney, M. L. and McNamara, K. J. (1991)Heterochrony: The Evolution of Ontogeny. Plenum Press, New York, NY.
Moran, N. A. (1992) The evolutionary maintenance of alternative phenotypes.Am. Nat. 139, 971–89.
Pfennig, D. (1990) The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole.Oecologia 85, 101–7.
Pfennig, D. W. (1992) Polyphenism in spadefoot toad tadpoles as a locally-adjusted evolutionary stable strategy.Evolution 46, 1408–20.
Pfennig, D. W. and Collins, J. P. (1993) Kinship affects morphogenesis in cannibalistic salamanders.Nature 362, 836–8.
Pfennig, D. W., Loeb, M. L. G. and Collins, J. P. (1991) Pathogens as a factor limiting the spread of cannibalism in tiger salamanders.Oecologia 88, 161–6.
Roff, D. A. (1986) The evolution of wing dimorphism in insects.Evolution 40 1009–20.
Roff, D. A. (1994) Habitat persistence and the evolution of wing dimorphism in insects.Am. Nat. 144, 772–98.
Roff, D. A. (In press) The evolution of threshold traits in animals.Q. Rev. Biol.
Roff, D. A. and Fairbairn, D. J. (1993) The evolution of alternative morphologies: fitness and wing morphology in male sand crickets.Evolution 47, 1572–84.
Scheiner, S. M. (1993) Genetics and evolution of phenotypic plasticity.Annu. Rev. Ecol. Syst. 24, 35–68.
Schlichting, C. D. (1986) The evolution of phenotypic plasticity in plants.Annu. Rev. Ecol. Syst. 17, 667–93.
Semlitsch, R. D. (1985) Reproductive strategy of a facultatively paedomorphic salamanderAmbystoma talpoideum.Oecologia 65, 305–13.
Semlitsch, R. D. (1987) Paedomorphosis inAmbystoma talpoideum: effects of density, food, and pond drying.Ecology 68, 994–1002.
Semlitsch, R. D. and Gibbons, J. W. (1985) Phenotypic variation in metamorphosis and paedomorphosis in the salamanderAmbystoma talpoideum.Ecology 66, 1123–30.
Semlitsch, R. D. and Wilbur, H. M. (1989) Artificial selection for paedomorphosis in the salamanderAmbystoma talpoideum.Evolution 43, 105–12.
Semlitsch, R. D., Harris, R. N. and Wilbur, H. M. (1990) Paedomorphosis inAmbystoma talpoideum: maintenance of population variation and alternative life-history pathways.Evolution 44, 1604–13.
Sexton, O. J. and Bizer, J. R. (1978) Life history patterns ofAmbystoma tigrinum in montane Colorado.Am. Midl. Nat. 99, 101–18.
Shaffer, H. B. (1984) Evolution in a paedomorphic lineage. II. Allometry and form in the Mexican ambystomatid salamanders.Evolution 38, 1207–18.
Smith, H. M. (1989) Discovery of the axolotl and its early history in biological research. InDevelopmental Biology of the Axolotl (J. B. Armstrong and G. M. Malacinski, eds), pp. 3–12. Oxford University Press, New York, NY.
Smith-Gill, S. J. (1983) Developmental plasticity: developmental conversion versus phenotypic modulation.Am. Zool. 23, 47–55.
Snyder, R. C. (1956) Comparative features of the life histories ofAmbystoma gracile (Baird) from populations at low and high altitudes.Copeia 1956, 41–50.
Sokal, R. R. and Rohlf, F. J. (1981)Biometry. W. H. Freeman Press, San Francisco, CA.
Sprules, W. G. (1972) Effects of size-selective predation and food competition on high altitude zooplankton communities.Ecology 53, 375–86.
Sprules, W. G. (1974a) The adaptive significance of paedogenesis in the North American species ofAmbystoma (Amphibia: Caudata): an hypothesis.Can. J. Zool. 52, 393–400.
Sprules, W. G. (1974b) Environmental factors and the incidence of neoteny inAmbystoma gracile (Baird) (Amphibia: Caudata).Can. J. Zool. 52, 1545–52.
Thompson, J. D. (1991) Phenotypic plasticity as a component of evolutionary change.Trends Ecol. Evol. 6, 246–9.
Werner, E. E. (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation.Am. Nat. 128, 319–41.
West-Eberhard, M. J. (1989) Phenotypic plasticity and the origins of diversity.Annu. Rev. Ecol. Syst. 20, 249–78.
Whiteman, H. H. (1994) Evolution of facultative paedomorphosis in salamanders.Q. Rev. Biol. 69, 205–21.
Whiteman, H. H., Wissinger, S. A. and Bohonak, A. J. (1994) Seasonal movement patterns in a subalpine population of the tiger salamander,Ambystoma tigrinum nebulosum.Can. J. Zool. 72, 1780–7.
Wilbur, H. M. (1980) Complex life cycles.Annu. Rev. Ecol. Syst. 11, 67–93.
Wilbur, H. M. (1984) Complex life cycles and community organization in amphibians. InA New Ecology: Novel Approaches to Interactive Systems (P. W. Price, C. N. Slobodchikoff and W. S. Gaud, eds), pp. 195–224. John Wiley and Sons, New York, NY.
Wilbur, H. M. (1990) Coping with chaos: toads in ephemeral ponds.Trends Ecol. Evol. 5, 37.
Wilbur, H. M. and Collins, J. P. (1973) Ecological aspects of amphibian metamorphosis.Science 182, 1305–14.
Wissinger, S. A. and Whiteman, H. H. (1992) Fluctuation in a Rocky Mountain population of salamanders: anthropogenic acidification or natural variation?J. Herpetol. 26, 377–91.
Zerba, K. E. (1989) Individual variation in diet of larval tiger salamanders (Ambystoma tigrinum nebulosum) in Arizona. PhD dissertation, Arizona State University, Flagstaff.
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Whiteman, H.H., Wissinger, S.A. & Brown, W.S. Growth and foraging consequences of facultative paedomorphosis in the tiger salamander,Ambystoma tigrinum nebulosum . Evol Ecol 10, 433–446 (1996). https://doi.org/10.1007/BF01237728
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DOI: https://doi.org/10.1007/BF01237728