Skip to main content
Log in

Cytogenetics of diploid and triploid salamanders of the Ambystoma jeffersonianum complex

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Analysis of C-band heterochromatin (CBH) and cold-induced secondary constrictions (CICs) indicates that gynogenetic triploidy in the Ambystoma jeffersonianum complex is a cytogenetic consequence of hybridization between the two diploid species, A. jeffersonianum and A. laterale. The key feature in the history of this complex was the apparent proclivity for germ-line chromosome reduplication, and incidental production of chromosomally unreduced ova, allowing the circumvention of meiotic difficulties in diploid hybrid females. Chromosome structure, in terms of CBH and CICs, the mechanism of sex determination (dominant W, female heterogametic), and a recognizable WZ female/ZZ male sex chromosome heteromorphism in the diploid species A. laterale, are cytogenetic factors that allow reconstruction of the probable evolutionary history of the complex. The constitution of the triploid karyotypes suggests that the putative ancestral hybrid diploid females resulted from a mating between female A. jeffersonianum and male A. laterale, and that when such a hybrid female backcrossed to normal males of A. jeffersonianum and A. laterale, both kinds of allotriploids, A. platineum and A. tremblayi respectively, were produced. Karyological differentiation in each triploid species suggests that their origin was relatively recent and virtually simultaneous. It is conceivable that only one such hybrid female gave rise to both kinds of allotriploids in just one or two breeding seasons, and that present geographic distributions are due to persistent post-glaciation migrations of the resulting triploid clones. All offspring from such a back-cross carried a jeffersonianum W-chromosome and hence were female as well as triploid, and probably continued to produce chromosomally unreduced (triploid) ova by the same mechanism that operated in their hybrid mother. Sperm rejection resulting in gynogenesis in the allotriploids can be viewed as a physiological response to “pseudopolyspermy” by the chromosomally unreduced triploid ova. Evidence is presented that one of the triploid species, A. platineum, may produce a high percentage of diploid offspring with karyotypes identical to A. jeffersonianum. Diploids have not been detected among the offspring of A. tremblayi, but tetraploids are occasionally produced.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bogart, J.P.: Evolutionary implications of polyploidy in amphibians and reptiles. In: Polyploidy (W.H. Lewis, ed.), pp. 341–378. New York: Plenum Press 1980

    Google Scholar 

  • Callan, H.G.: Chromosomes and nucleoli of the axolotl, Ambystoma mexicanum. J. Cell. Sci. 1, 85–108 (1966)

    Google Scholar 

  • Clanton, W.: An unusual situation in the salamander Ambystoma jeffersonianum (Green). Occ. Pap. Mus. Zool. Univ. Mich. 290, 1–40 (1934)

    Google Scholar 

  • Conant, R.: A field guide to reptiles and amphibians of eastern and central North America. 2nd ed. Boston: Houghton-Mifflin Co., 1975

    Google Scholar 

  • Cook, F.R., Gorham, S.W.: The occurrence of the triploid form in populations of the blue-spotted salamander, Ambystoma laterale, in New Brunswick. J. New Brunswick Mus. 154–161 (1979)

  • Cueller, O.: On the origin of parthenogenesis in vertebrates; the cytogenetic factors. Amer. Naturalist 108, 625–648 (1974)

    Google Scholar 

  • Cuellar, O.: Cytology of meiosis in the driploid gynogenetic salamander Ambystoma tremblayi. Chromosoma (Berl.) 58, 355–364 (1976)

    Google Scholar 

  • Downs, F.L.: Unisexual Ambystoma from the Bass Islands of Lake Erie. Occ. Pap. Mus. Zool. Univ. Mich. 685, 1–36 (1978)

    Google Scholar 

  • Gilhen, J.: Distribution, natural history and morphology of the blue-spotted salamanders, Ambystoma laterale and A. tremblayi in Nova Scotia. Nova Scotia Mus. Curatorial Report number 22, 1–38 (1974)

    Google Scholar 

  • Graham, R.E.: Environmental effects on deme structure, dynamics and breeding strategy of Ambystoma opacum (Amphibia: Ambystomatidae), with an hypothesis on the probable origin of the marbled salamander life-style. PhD dissertation, Rutgers University (1971)

  • Green, D.M., Bogart, J.P., Anthony, E.H., Genner, D.H.: An interactive, microcomputer-based karyotype analysis system for phylogenetic cytotaxonomy. Comput. Biol. Med. 10, 219–227 (1980)

    Google Scholar 

  • Hadorn, E.: Experimental studies of amphibian development. Berlin, Heidelberg, New York: Springer (1974)

    Google Scholar 

  • Hauschka, T.S., Brunst, V.V.: Sexual dimorphism in the nucleolar autosome of the axolotl (Siredon mexicanum). Hereditas (Lund) 52, 345–356 (1965)

    Google Scholar 

  • Hotta, Y., Stern, H.: DNA scission and repair during pachytene in Lilium. Chromosoma (Berl.) 46, 279–296 (1974)

    Google Scholar 

  • Humphrey, R.R.: Sex determination in ambystomid salamanders: a study of the progeny of females experimentally converted into males. Amer. J. Anat. 76, 33–66 (1945)

    Google Scholar 

  • Humphrey, D.G.: New chromosome number for the order Caudata. Science 128, 304 (1958)

    Google Scholar 

  • John, B., Miklos, G.L.G.: Functional aspects of satellite DNA and heterochromatin. Int. Rev. Cytol. 58, 1–114 (1979)

    Google Scholar 

  • Kezer, J.: Meiosis in salamander spermatocytes. In: The mechanics of inheritance (F.W. Stahl). 2nd ed. Englewood Cliffs, N.J.: Prentice-Hall Inc. (1969)

    Google Scholar 

  • Kezer, J., León, P., Sessions, S.K.: Struktural differentiation of the meiotic and mitotic chromosomes of the salamander, Ambystoma macrodactylum. Chromosoma (Berl.) 81, 177–197 (1980)

    Google Scholar 

  • Kiester, A.R. Nagylaki, T., Shaffer, B.: Population dynamics of species with gynogenetic sibling species. Theoret. Pop. Biol. 19, 358–369 (1981)

    Google Scholar 

  • Koch, P., Pijnacker, L.P., Kreke, J.: DNA reduplication during meiotic prophase in the oocytes of Carausius, morosus Br. (Insecta, Cheleutoptera). Chromosoma (Berl.) 36, 313–321 (1972)

    Google Scholar 

  • Levan, A., Fredga, D., Sandberg, A.A.: Nomenclature for centromeric position on chromosomes. Hereditas (Lund) 52, 201–220 (1964)

    Google Scholar 

  • Lewin, B.: Gene expression, vol. 2, eucaryotic chromosomes. 2nd ed. John Wiley and Sons, New York, Chichester, Krisbane, Toronto (1980)

    Google Scholar 

  • Macgregor, H.C.: The role of lampbrush chromosomes in the formation of nucleoli in amphibian oocytes. Quart. J. Micr. Sci. 106, 215–228 (1965)

    Google Scholar 

  • Macgregor, H.C., Uzzell, T.M., Jr.: Gynogenesis in salamanders related to Ambystoma jeffersonianum. Science 143, 1032–1046 (1964)

    Google Scholar 

  • Mancino, G., Ragghianti, M., Bucci-Innocenti, S.: Experimental hybridization within the genus Triturus (Urodele: Salamandridae). I. Spermatogenesis of F1 species hybrids, Triturus cristatus carnifex x T. vulgaris meridionalis. Chromosoma (Berl.) 69, 27–46 (1978)

    Google Scholar 

  • Minton, S.A., Jr.: Salamanders of the Ambystoma jeffersonianum complex in Indiana. Herpetologica 10, 173–179 (1954)

    Google Scholar 

  • Morescalchi, A.: Chromosome evolution in the caudate amphibia. Evol. Biol. 8, 339–387 (1975)

    Google Scholar 

  • Noble, G.K., Brady, M.K.: Observations on the life history of the marbled salamander, Ambystoma opacum Gravenhorst. Zoologica 8, 89–132 (1933)

    Google Scholar 

  • Ohno, S.: Evolution by gene duplication. Berlin, Heidelberg, New York: Springer (1970)

    Google Scholar 

  • Piersol, W.H.: Spawn and larva of Ambystoma jeffersonianum. Am. Nat. 44, 732–738 (1910)

    Google Scholar 

  • Piersol, W.H.: Pathological polyspermy in eggs of Ambystoma jeffersonianum. Trans. Roy. Can. Inst. 17, 57–74 (1929)

    Google Scholar 

  • Schmid, M., Olert, J., Klett, C.: Chromosome banding in amphibia. III. Sex chromosomes in Triturus. Chromosoma (Berl.) 71, 29–55 (1979)

    Google Scholar 

  • Uzzell, T.M., Jr.: Natural triploidy in salamanders related to Ambystoma jeffersonianum. Science 139, 113–115 (1963)

    Google Scholar 

  • Uzzell, T.M., Jr.: Relations of the diploid and triploid species of the Ambystoma jeffersonianum complex (Amphibia, Caudata) Copeia 2, 257–300 (1964)

    Google Scholar 

  • Uzzell, T.M., Jr.: Ambystoma jeffersonianum. In: Catalogue of American amphibians and reptiles. American Society of Ichthyologists and Herpetologists. p. 47 (1967 a)

  • Uzzell, T.M., Jr.: Ambystoma laterale. In: Catalogue of American amphibians and reptiles. American Society of Ichthyologists and Herpetologists, p. 48 (1967 b)

  • Uzzell, T.M., Jr.: Ambystoma platineum. In: Catalogue of American amphibians and reptiles. American Society of Ichthyologists and Herpetologists. p. 49 (1967 c)

  • Uzzell, T.M., Jr.: Ambystoma tremblayi. In: Catalogue of American amphibians and reptiles. American Society of Ichthyologists and Herpetologists. p. 50 (1967 d)

  • Uzzell, T.M., Jr., Goldblatt, S.M.: Serum proteins of salamanders of the Ambystoma jeffersonianum complex, and the origin of the triploid species of this group. Evolution 21, 345–354 (1967)

    Google Scholar 

  • Walker, P.M.B.: ‘Repetitive’ DNA in higher organisms. Progr. biophys. molec. Biol. 23, 145–190 (1971)

    Google Scholar 

  • White, M.J.D.: Animal cytology and evolution, 3rd ed. Cambridge: Cambridge Univ. Press, (1973)

    Google Scholar 

  • White, R., Pasztor, L.M., Hu, F.: Mouse satellite DNA in noncentromeric heterochromatin of cultured cells. Chromosoma (Berl.) 50, 275–282 (1975)

    Google Scholar 

  • Woodard, J., Swift, H.: The DNA content of cold treated chromosomes. Exptl. Cell Res. 34, 131–137 (1964)

    Google Scholar 

  • Yunis, J.J., Yasmineh, W.G.: Heterochromatin, satellite DNA, and cell function. Science 174, 1200–1209 (1971)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Dedicated to my mentor and valued friend, James Kezer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sessions, S.K. Cytogenetics of diploid and triploid salamanders of the Ambystoma jeffersonianum complex. Chromosoma 84, 599–621 (1982). https://doi.org/10.1007/BF00286329

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00286329

Keywords

Navigation