Skip to main content
Book cover

Developmental Instability: Its Origins and Evolutionary Implications pp 169–185Cite as

Shaping intraspecifíc variation: development, ecology and the evolution of morphology and life history variation in tiger salamanders

  • Chapter

Part of the Contemporary Issues in Genetics and Evolution book series (CIGE,volume 2)

Abstract

The tiger salamander, Ambystoma tigrinum, is a geographically widespread, morphologically variable, polytipic species. It is among the most variable species of salamanders in morphology and life history with two larval morphs (typical and cannibal) and three adult morphs (metamorphosed, typical branchiate, cannibal branchiate) that vary in frequency between subspecies and between populations within subspecies. We report morphometric evidence suggesting that branchiate cannibals arose through intraspecifíc change in the onset or timing of development resulting in the wider head and hypertrophied tooth-bearing skull bones characteristic of this phenotype. We also quantified bilateral symmetry of gill raker counts and abnormalities, then evaluated fluctuating asymmetry as a measure of the developmental stability of each morph. There was a significant interaction between fluctuating asymmetry of developmental abnormalities in cannibals and typicals and the locality where they were collected, suggesting that relative stability of each phenotype could vary among populations. While altered timing of developmental events appears to have a role in the evolution and maintenance of morphs, novel phenotypes persist only under favorable ecological conditions. Predictability of the aquatic habitat, genetic variation, kinship, body size, intraspecifíc competition and predation all affect expression and survival of the morphs in A. tigrinum. This taxon provides an excellent model for understanding the diversity and complexity of developmental and ecological variables controlling the evolution and maintenance of novel phenotypes.

Key words

  • fluctuating asymmetry
  • heterochrony
  • intraspecifíc
  • morphology
  • polymorphism

This is a preview of subscription content, access via your institution.

Chapter
GBP   19.95
Price includes VAT (United Kingdom)
  • DOI: 10.1007/978-94-011-0830-0_13
  • Chapter length: 17 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
GBP   143.50
Price includes VAT (United Kingdom)
  • ISBN: 978-94-011-0830-0
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
GBP   179.99
Price includes VAT (United Kingdom)
Hardcover Book
GBP   219.99
Price includes VAT (United Kingdom)
Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alberch, P., S. J. Gould, G. F. Oster & D. B. Wake, 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5: 296–318.

    Google Scholar 

  • Alexander, R. D. & R. S. Bigelow, 1960. Allochronic speciation in field crickets and a new species, Acheta veletis. Evolution 14: 334–346.

    CrossRef  Google Scholar 

  • Baird, D., 1965. Paleozoic lepospondyl amphibians. Amer. Zool. 5: 287–294.

    Google Scholar 

  • Begun, D. J. & J. P. Collins, 1992. Biochemical plasticity in the Arizona tiger salamander (Ambystoma tigrinum nebulosum). J. Heredity 83: 224–227.

    CAS  Google Scholar 

  • Berna, H., 1990. Ecology and life history of the tiger salamander,Ambystoma tigrinum nebulosum Hallowell, on the Kaibab Plateau. M.S. thesis, Arizona State University.

    Google Scholar 

  • Bolt, J. R., 1979. Amphibamus grandiceps as a juvenile dissorophid:evidence and implications, pp. 529–563 in Mazon Creek Fossils, edited by M. H. Nitecki. Academic Pr., NY.

    Google Scholar 

  • Bookstein, F. L., B. Chernoff, R. L. Elder, J. M. Humphries, G. R. Smith & R. E. Strauss, 1985. Morphometrics in Evolutionary Biology. Spec. Publ. no. 15. Acad. Nat. Sci. Phil.

    Google Scholar 

  • Brandon, R. A., 1972. Hybridization between the Mexican salamanders Ambystoma dumerilii and Ambystoma mexicanum under laboratory conditions. Herpetologica 28: 199–207.

    Google Scholar 

  • Brandon, R. A., 1977. Interspecific hybridization among Mexican and United States salamanders of the genus Ambystoma under laboratory conditions. Herpetologica 33: 133–152.

    Google Scholar 

  • Burnaby, T. P., 1966. Growth-invariant discriminant functions and generalized distances. Biometrics 22: 96–110.

    CrossRef  Google Scholar 

  • Cattell, R. B., 1966. The Scree Test for the number of factors. Multivar. Behav. Res. 1: 245–276.

    Google Scholar 

  • Collins, J. P., 1981. Distribution, habitats and life history variation in the tiger salamander, Ambystoma tigrinum, in eastcentral and southeast Arizona. Copeia 1981: 666–675.

    CrossRef  Google Scholar 

  • Collins, J. P. & J. R. Holomuzki, 1984. Intraspecific variation in diet within and between trophic morphs in larval tiger salamanders (Ambystoma tigrinum nebulosum). Canadian Journal of Zoology 62: 168–174.

    CrossRef  Google Scholar 

  • Collins, J. P. & J. E. Cheek, 1983. Effect of food and density on development of typical and cannibalistic salamander larvae in Ambystoma tigrinum nebulosum. Amer. Zool. 23: 77–84.

    Google Scholar 

  • Crump, M. L., 1992. Cannibalism in amphibians, pp. 256–276 in Cannibalism: Ecology and Evolution among Diverse Taxa, edited by M. A. Elgar and B. J. Crespi. Oxford University Press, Oxford, UK.

    Google Scholar 

  • DeMar, R., 1968. The Permian labyrinthodont amphibian Dissorophus multicinctus, and adaptations and phylogeny of the family Dissorophidae. J. Paleontology 42: 1210–1242.

    Google Scholar 

  • DeQueiroz, K., 1985. The ontogenetic method for determining character polarity and its relevance to phylogenetic systematics.Syst. Zool. 34: 280–299.

    CrossRef  Google Scholar 

  • Dobzhansky, Th., 1937. Genetics and the Origin of Species. Columbia Univ. Pr., NY.

    Google Scholar 

  • Duellman, W. E. & L. Treub, 1986. Biology of Amphibians. McGraw-Hill, NY.

    Google Scholar 

  • Edwards, J. L., 1976. Spinal nerves and their bearing on salamander phylogeny. J. Morph. 148: 305–328.

    CrossRef  PubMed  CAS  Google Scholar 

  • Eldredge, N. & S. J. Gould, 1972. Punctuated equilibria: an alternative to phyletic gradualism, pp. 82–115 in Models in Paleobiology, edited by T. J. M. Schopf. Freeman, SF.

    Google Scholar 

  • Emerson, S. B., 1986. Heterochrony and frogs: the relationship of a life history trait to morphological form. Amer. Natur. 127: 167–183.

    CrossRef  Google Scholar 

  • Estes, R., 1981. Teil 2. Gymnophiona, Caudata. Handbuch der Paläoherpetologie. Gustav Fischer Verlag, Stuttgart.

    Google Scholar 

  • Fink, W. L., 1982. The conceptual relationship between ontogeny and phylogeny. Paleobiology 8: 254–264.

    Google Scholar 

  • Ford, E. B., 1965. Genetic Polymorphism. M.I.T. Pr., Cambridge.

    Google Scholar 

  • Gauch, H. G., Jr., 1982. Noise reduction by eigenvector ordination.Ecology 63: 1643–1649.

    CrossRef  Google Scholar 

  • Gehlbach, F. R., 1965. The herpetology of the Zuni Mountains region, northwestern New Mexico. Proc. U. S. Nat. Mus. 116:243–332.

    Google Scholar 

  • Gehlbach, F. R., 1967. Ambystoma tigrinum (Green). Tiger salamander.Catalogue of American Amphibians and Reptiles: 52.1-52.4.

    Google Scholar 

  • Gould, S. J., 1977. Ontogeny and Phylogeny. Belknap Pr., Cambridge.

    Google Scholar 

  • Hecht, M. K., 1957. A case of parallel evolution in salamanders. Proc. Zool. Soc., Calcutta, Mookerjee Memor. 1957: 283–292.

    Google Scholar 

  • Holomuzki, J. R. & J. P. Collins, 1987. Trophic dynamics of a top predator, Ambystoma tigrinum nebulosum (Caudata: Ambystomatidae), in a lentic community. Copeia 1987: 949–957.

    CrossRef  Google Scholar 

  • Humphries, J. M., F. L. Bookstein, B. Chernoff, G. R. Smith, R. L. Elder & S. G. Poss, 1981. Multivariate discrimination by shape in relation to size. Syst. Zool. 30: 291–308.

    CrossRef  Google Scholar 

  • Johnson, R. A. & D. W. Wichern, 1982. Applied Multivariate Statistical Analysis. Prentice-Hall, Englewood Cliffs, NJ.

    Google Scholar 

  • Jolicoeur, P., 1963. The multivariate generalization of the allometry equation. Biometrics 19: 497–499.

    CrossRef  Google Scholar 

  • Jones, T. R., J. P. Collins, T. D. Kocher & J. B. Mitton, 1988. Systematic status and distribution of Ambystoma tigrinum stebbinsi Lowe. Copeia: 621–635.

    Google Scholar 

  • Kirkpatrick, M., 1982. Quantum evolution and punctuated equilibria in continuous genetic characters. Amer. Natur. 119: 833–848.

    CrossRef  Google Scholar 

  • Kluge, A., 1984. The relevance of parsimony to phylogenetic inference, pp. 24–38 in Cladistics: Perspectives on the Reconstruction of Evolutionary History, edited by T. Duncan and T. Stuessy. Columbia Univ. Pr., NY.

    Google Scholar 

  • Kluge, A., 1985. Ontogeny and phylogenetic systematics. Cladistics 1: 13–27.

    CrossRef  Google Scholar 

  • Kluge, A. & R. E. Strauss, 1985. Ontogeny and systematics. Ann. Rev. Ecol. Syst. 16: 247–268.

    CrossRef  Google Scholar 

  • Knerer, G. & C. E. Atwood, 1973. Diprionid sawflies: polymorphism and speciation. Science 179: 1090–1099.

    CrossRef  PubMed  CAS  Google Scholar 

  • Lannoo, M. & M. Bachmann, 1984. Aspects of cannibalistic morphs in a population of A. t. tigrinum larvae. Amer. Midl. Natur. 122: 103–109.

    CrossRef  Google Scholar 

  • Lerner, I. M., 1954. Genetic Homeostasis. Dover, N.Y.

    Google Scholar 

  • Loeb, M. L. G., J. P. Collins & T. J. Maret, 1993, in press. The role of prey in controlling expression of a trophic polymorphism in Ambystoma tigrinum nebulosum. Functional Ecology:29 pp. ms.

    Google Scholar 

  • Mather, I., 1955. Polymorphism as an outcome of disruptive selection. Evolution 9: 52–61.

    CrossRef  Google Scholar 

  • Mayr, E., 1942. Systematics and the Origin of Species. Columbia Univ. Pr., NY.

    Google Scholar 

  • Meyer, A., 1987. Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41: 1357–1369.

    CrossRef  Google Scholar 

  • Milligan, B. G., 1986. Punctuated evolution induced by ecological change. Amer. Natur. 127: 522–532.

    CrossRef  Google Scholar 

  • Minckley, W. L., D. A. Hendrickson & C. E. Bond, 1986. Geography of western North American freshwater fishes: description and relationships to intracontinental tectonism, pp. 519–613 in The Zoogeography of North American Freshwater Fishes, edited by C. H. Hocutt & E. O. Wiley. Wiley, NY.

    Google Scholar 

  • Nelson, G., 1978. Ontogeny, phylogeny, paleontology, and the biogenetic law. Syst. Zool. 27: 324–345.

    CrossRef  Google Scholar 

  • Ohlandt, G., 1992. Microgeographic variation in life history of Ambystoma tigrinum nebulosum in Arizona. M.S. thesis, Arizona State University.

    Google Scholar 

  • Palmer, A. R. & C. Strobeck, 1986. Fluctuating asymmetry: measurement, analysis, patterns. Ann. Rev. Ecol. Syst. 17: 391–421.

    CrossRef  Google Scholar 

  • Pedersen, S. C., 1991. Dental morphology of the cannibal morph in the tiger salamander, Ambystoma tigrinum. Amphibia-Reptilia 12: 1–14.

    CrossRef  Google Scholar 

  • Pfennig, D. W., M. L. G. Loeb & J. P. Collins, 1991. Pathogens as a factor limiting the spread of cannibalism in tiger salamanders.Oecologia 88: 161–166.

    CrossRef  Google Scholar 

  • Pfennig, D. W. & J. P. Collins, 1993. Kinship affects morphogenesis in cannibalistic salamanders. Nature 362: 836–838.

    CrossRef  PubMed  CAS  Google Scholar 

  • Pfennig, D. W., P. W. Sherman & J. P. Collins, 1993, in press. Kinship and cannibalism in polyphenic salamanders. Behavioral Ecology: 43 pp. ms.

    Google Scholar 

  • Pierce, B. A., J. B. Mitton, L. Jacobson & F. L. Rose, 1983. Head shape and size in cannibal and noncannibal morphs of the tiger salamander from west Texas. Copeia 1983: 1006–1012.

    CrossRef  Google Scholar 

  • Pimentel, R. A., 1979. Morphometrics. Kendall/Hunt, Dubuque.

    Google Scholar 

  • Powers, J. H., 1903. The causes of acceleration and retardation in the metamorphosis of Ambystoma tigrinum: A preliminary report. Amer. Natur. 37: 385–410.

    CrossRef  Google Scholar 

  • Powers, J. H., 1907. Morphological variation and its causes in Ambystoma tigrinum. Stud. Univ. Nebraska 7: 197–274.

    Google Scholar 

  • Regal, P. J., 1966. Feeding specializations and the classification of terrestrial salamanders. Evolution 20: 392–407.

    CrossRef  Google Scholar 

  • Reilly, S. M., G. V. Lauder & J. P. Collins, 1992. Performance consequences of a trophic polymorphism: feeding behavior in typical and cannibal phenotypes of Ambystoma tigrinum. Copeia 1992: 672–679.

    CrossRef  Google Scholar 

  • Reyment, R. A., R. E. Blackith & N. A. Campbell, 1984. Multivariate Morphometrics. 2nd ed. Acad. Pr., NY.

    Google Scholar 

  • Rohlf, F. J. & F. L. Bookstein, 1987. A comment on shearing as a method for ’size correction’. Syst. Zool. 36: 356–367.

    CrossRef  Google Scholar 

  • Rosenzweig, M. L., 1978. Competitive speciation. Biol. J. Linnean Soc. 10: 275–289.

    CrossRef  Google Scholar 

  • Roughgarden, J., 1972. Evolution of niche width. Amer. Natur. 106: 683–713.

    CrossRef  Google Scholar 

  • Sage, R. D. & R. K. Selander, 1975. Trophic radiation through polymorphism in cichlid fishes. Proc. Nat. Acad. Sci. USA 72: 4660–4673.

    CrossRef  Google Scholar 

  • Seger, J., 1985. Intraspecific resource competition as a cause of sympatric speciation, pp. 43–53 in Essays in Honor of John Maynard Smith, edited by P. J. Greenwood, P. H. Harvey & M. Slatkin. Cambridge Univ. Pr., Cambridge.

    Google Scholar 

  • Shaffer, H. B., 1984a. Evolution in a paedomorphic lineage. I. An electrophoretic analysis of the Mexican ambystomatid salamanders. Evolution 38: 1194–1206.

    CrossRef  Google Scholar 

  • Shaffer, H. B., 1984b. Evolution in a paedomorphic lineage. II. Allometry and form in the Mexican ambystomatid salamanders. Evolution 38: 1207–1218.

    CrossRef  Google Scholar 

  • Sokal, R. R. & F. J. Rohlf, 1981. Biometry, 2nd ed. Freeman, SF.

    Google Scholar 

  • Somers, K. M., 1986. Multivariate allometry and removal of size with principal components analysis. Syst. Zool. 35: 359–368.

    CrossRef  Google Scholar 

  • Soulé, M. E. & J. Cuzin-Roudy, 1982. Allometric variation. 2. Developmental instability of extreme phenotypes. Amer. Natur. 120: 765–786.

    CrossRef  Google Scholar 

  • Stanely, S. M., 1979. Macroevolution. Freeman, SF.

    Google Scholar 

  • Stevens, P. F., 1980. Evolutionary polarity of character states. Ann. Rev. Ecol. Syst. 11: 333–358.

    CrossRef  Google Scholar 

  • Szarski, H., 1957. The origin of the larva and metamorphosis in Amphibia. Amer. Natur. 91: 281–301.

    Google Scholar 

  • Szarski, H., 1962. The origin of the Amphibia. Q. Rev. Biol. 37: 189–241.

    CrossRef  Google Scholar 

  • Thoday, J. M., 1953. Homeostasis in a selection experiment. Heredity 12: 401–415.

    CrossRef  Google Scholar 

  • Tihen, J., 1958. Comments on the osteology and phylogeny of ambystomatid salamanders. Bull. Florida State Mus. 3: 1–51.

    Google Scholar 

  • Vrijenhoek, R. C., 1984. Ecological differentiation among clones: the frozen niche variation model, pp. 217–231 in Population Biology and Evolution, edited by K. Wöhrmann & V. Loeschcke. Springer-Verlag, Berlin.

    CrossRef  Google Scholar 

  • Waddington, C. H., 1957. The Strategy of the Genes. Mac- Millan, NY.

    Google Scholar 

  • West-Eberhard, M. J., 1986. Alternative adaptations, speciation, and phylogeny (a review). Proc. Nat. Acad. Sci. USA 83: 1388–1392.

    CrossRef  PubMed  CAS  Google Scholar 

  • White, M. J. D., 1978. Models of Speciation. Freeman, SF.

    Google Scholar 

  • Wiley, E. O., 1980. Phylogenetic systematics and vicariance biogeography. Syst. Bot. 5: 194–220.

    CrossRef  Google Scholar 

  • Wiley, E. O., 1981. Phylogenetics: The Theory and Practice of Phylogenetic Systematics. Wiley, NY.

    Google Scholar 

  • Wright, S. W., 1968. Evolution and the Genetics of Populations. Vol 1. Genetic and Biometric Foundations. Univ. Chicago Pr., Chicago.

    Google Scholar 

  • Wright, S. W., 1978. Evolution and the Genetics of Populations. Vol 4. Variability within and among Natural Populations. Univ. Chicago Pr., Chicago.

    Google Scholar 

  • Wright, S. W., 1982. Character change, speciation, and the higher taxa. Evolution 36: 427–443.

    CrossRef  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, Arizona State University, Tempe, AZ, 85287-1501, USA

    James P. Collins

  2. Department of Human Genetics, University of Michigan, Ann Arbor, MI, 48109, USA

    Kim E. Zerba

  3. Arizona Game and Fish Department, Nongame Branch, 221 West Greenway Road, Phoenix, AZ, 85023-4312, USA

    Michael J. Sredl

Authors
  1. James P. Collins
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kim E. Zerba
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael J. Sredl
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

    Rights and permissions

    Reprints and Permissions

    Copyright information

    © 1994 Springer Science+Business Media Dordrecht

    About this chapter

    Cite this chapter

    Collins, J.P., Zerba, K.E., Sredl, M.J. (1994). Shaping intraspecifíc variation: development, ecology and the evolution of morphology and life history variation in tiger salamanders. In: Markow, T.A. (eds) Developmental Instability: Its Origins and Evolutionary Implications. Contemporary Issues in Genetics and Evolution, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-0830-0_13

    Download citation

    • DOI: https://doi.org/10.1007/978-94-011-0830-0_13

    • Publisher Name: Springer, Dordrecht

    • Print ISBN: 978-94-010-4357-1

    • Online ISBN: 978-94-011-0830-0

    • eBook Packages: Springer Book Archive