Article
Free Access
SPECIATION BY POLYPLOIDY IN TREEFROGS: MULTIPLE ORIGINS OF THE TETRAPLOID, HYLA VERSICOLOR
Margaret B. Ptacek,
H. Carl Gerhardt,
Richard D. Sage,
Margaret B. Ptacek
Division of Biological Sciences, University of Missouri, Columbia, Missouri, 65211
Present address: Department of Biological Science, Florida State University, Tallahassee, Florida 32306-2043.Search for more papers by this authorH. Carl Gerhardt
Division of Biological Sciences, University of Missouri, Columbia, Missouri, 65211
Search for more papers by this authorRichard D. Sage
Division of Biological Sciences, University of Missouri, Columbia, Missouri, 65211
Search for more papers by this authorMargaret B. Ptacek,
H. Carl Gerhardt,
Richard D. Sage,
Margaret B. Ptacek
Division of Biological Sciences, University of Missouri, Columbia, Missouri, 65211
Present address: Department of Biological Science, Florida State University, Tallahassee, Florida 32306-2043.Search for more papers by this authorH. Carl Gerhardt
Division of Biological Sciences, University of Missouri, Columbia, Missouri, 65211
Search for more papers by this authorRichard D. Sage
Division of Biological Sciences, University of Missouri, Columbia, Missouri, 65211
Search for more papers by this authorAbstract
Speciation by polyploidy is rare in animals, yet, in vertebrates, there is a disproportionate concentration of polyploid species in anuran amphibians. Sequences from the cytochrome b gene of the mitochondrial DNA (mtDNA) were used to determine phylogenetic relationships among 37 populations of the diploid-tetraploid species pair of gray treefrogs, Hyla chrysoscelis and Hyla versicolor. The diploid species, H. chrysoscelis, consists of an eastern and a western lineage that have 2.3% sequence divergence between them. The tetraploid species, H. versicolor, had at least three separate, independent origins. Two of the tetraploid lineages are more closely related to one or the other of the diploid lineages (0.18%–1.4% sequence divergence) than they are to each other (1.9%–3.4% sequence divergence). The maternal ancestor of the third tetraploid lineage is unknown. The phylogenetic relationships between the two species and among lineages within each species support the hypothesis of multiple origins of the tetraploid lineages.
Literature Cited
- Anderson, S., M. H. L. de Bruijn, A. R. Couison, I. C. Eperon, F. Sanger, and I. G. Young. 1982. Complete sequence of bovine mitochondrial DNA. Journal of Molecular Biology 156: 683–717.
- Avise, J. C. 1986. Mitochondrial DNA and the evolutionary genetics of higher animals. Philosophical Transactions of the Royal Society of London B Biological Sciences 312: 325–342.
- Avise, J. C. 1989. Gene trees and organismal histories: a phylogenetic approach to population biology. Evolution 43: 1192–1208.
- Avise, J. C., and R. A. Lansman. 1983. Polymorphism of mitochondrial DNA in populations of higher animals. Pp. 147–164 in M. Nei and R. K. Koehn, eds. Evolution of genes and proteins. Sinauer, Sunderland, Mass.
- Avise, J. C., and N. C. Saunders. 1984. Hybridization and introgression among species of sunfish (Lepomis): analysis by mitochondrial DNA and allozyme markers. Genetics 108: 237–255.
- Avise, J. C., J. E. Neigel, and J. Arnold. 1984. Demographic influences on mitochondrial DNA lineage survivorship in animal populations. Journal of Molecular Evolution 20: 99–105.
- Bogart, J. P. 1980. Evolutionary implications of polyploidy in amphibians and reptiles. Pp. 341–378 in W. Lewis, ed. Polyploidy: biological relevance. Plenum, New York.
10.1007/978-1-4613-3069-1_18 Google Scholar
- Bogart, J. P., and A. O. Wasserman. 1972. Diploidtetraploid species pairs: a possible clue to evolution by polyploidization in anuran amphibians. Cytogenetics 11: 7–24.
- Brown, W. M., E. M. Prager, A. Wang, and A. C. Wilson. 1982. Mitochondrial DNA sequences of primates: tempo and mode of evolution. Journal of Molecular Evolution 18: 225–239.
- Brown, W. M., and J. W. Wright. 1983. Evolution of animal mitochondrial DNA. Pp. 62–88 in M. Nei and R. K. Koehn, eds. Evolution of genes and proteins. Sinauer, Sunderland, Mass.
- Carr, S. M., A. J. Brothers, and A. C. Wilson. 1987. Evolutionary inferences from restriction maps of mitochondrial DNA from nine taxa of Xenopus frogs. Evolution 41: 176–188.
- Cash, M. N., and J. P. Bogart. 1987. Cytological differentiation of the diploid-tetraploid species pair of North American treefrogs (Amphibia, Anura, Hylidae). Journal of Herpetology 12: 555–558.
- Dobzhansky, T. 1951. Genetics and the origin of species, 3d ed. Columbia University Press, New York.
- Dobzhansky, T. 1970. Genetics of the evolutionary process. Columbia University Press, New York.
- Faith, D. P. 1991. Cladistic permutation tests for monophyly and nonmonophyly. Systematic Zoology 40: 366–375.
- Faith, D. P., and P. S. Cranston. 1991. Could a cladogram this short have arisen by chance alone? On permutation tests for cladistic structure. Cladistics 7: 1–28.
- Felsenstein, J. 1985. Confidence limits on phylogenies: an analysis using the bootstrap. Evolution 39: 783–791.
- Ferris, S. D., R. D. Sage, C. M. Huang, J. T. Neilsen, U. Ritte, and A. C. Wilson. 1983. Flow of mitochondrial DNA across a species boundary. Proceedings of the National Academy of Sciences, USA 80: 2290–2294.
- Gerhardt, H. C. 1974. Mating call differences between eastern and western populations of the gray treefrog Hyla chrysoscelis. Copeia 1974: 534–536.
10.2307/1442547 Google Scholar
- Gerhardt, H. C., M. B. Ptacek, L. Barnett, and K. G. Torke. 1994. Hybridization between the diploid-tetraploid treefrogs Hyla chrysoscelis and Hyla versicolor. Copeia 1994(1): 51–59.
10.2307/1446670 Google Scholar
- Gyllensten, U., D. Wharton, A. Josefsson, and A. C. Wilson. 1991. Paternal inheritance of mitochondrial DNA in mice. Nature 352: 255–257.
- Hedges, S. B. 1986. An electrophoretic analysis of Holarctic Hylid evolution. Systematic Zoology 35: 1–21.
- Hedges, S. B., J. P. Bogart, and L. R. Maxson. 1992. Ancestry of unisexual salamanders. Nature 356: 708–710.
- Hillis, D. M., A. Larson, S. K. Davis, and E. A. Zimmer. 1990. Nucleic acids III: sequencing. Pp. 339–340 in D. M. Hillis and C. Moritz, eds. Molecular systematics. Sinauer, Sunderland, Mass.
- Howell, N. 1989. Evolutionary conservation of protein regions in the protonmotive cytochrome b and their possible roles in redox catalysis. Journal of Molecular Evolution 29: 157–169.
- Kocher, T. D., W. K. Thomas, A. Meyer, S. V. Edwards, S. Paabo, F. X. Villablanca, and A. C. Wilson. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences, USA 86: 6196–6200.
- Krishan, A. 1975. Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. Journal of Cell Biology 66: 188–193.
- Kuramoto, M. 1990. A list of the chromosome numbers of anuran amphibians. Bulletin of the Fukuoka University of Education 39: 83–127.
- Lamb, T., and J. C. Avise. 1986. Directional introgression of mitochondrial DNA in a hybrid population of tree frogs: the influence of mating behavior. Proceedings of the National Academy of Sciences, USA 83: 2526–2530.
- Maxson, L. E., E. Pepper, and R. D. Maxson. 1977. Immunological resolution of a diploid-tetraploid species complex of tree frogs. Science 197: 1012–1013.
- Miyamoto, M. M., S. M. Tanhauser, and P. J. Laipis. 1989. Systematic relationships in the artiodactyl tribe Bovini (family Bovidae), as determined from mitochondrial DNA sequences. Systematic Zoology 38: 342–349.
- Müller, H. J. 1925. Why polyploidy is rarer in animals than in plants. American Naturalist 59: 346–353.
- Nei, M. 1987. Molecular evolutionary genetics. Columbia University Press, New York.
10.1111/j.1365-294X.2006.02908.x Google Scholar
- Orr, H. A. 1990. “Why polyploidy is rarer in animals than in plants” revisited. American Naturalist 136: 759–770.
- Pamilo, P., and M. Nei. 1988. Relationships between gene trees and species trees. Molecular Biology and Evolution 5: 568–583.
- Ralin, D. B. 1977. Evolutionary aspects of mating call variation in a diploid-tetraploid species complex of treefrogs (Anura). Evolution 31: 721–736.
- Ralin, D. B., M. A. Romano, and C. W. Kilpatrick. 1983. The tetraploid treefrog Hyla versicolor: evidence for a single origin from the diploid H. chrysoscelis. Herpetologica 39: 212–225.
- Romano, M. A., D. B. Ralin, S. I. Guttman, and J. H. Skillings. 1987. Parallel electromorph variation in the diploid-tetraploid gray treefrog complex, Hyla chrysoscelis and Hyla versicolor. American Naturalist 130: 864–878.
- Sage, R. D., W. R. Atchley, and E. Capanna. 1993. House mice as models in systematic biology. Systematic Biology 42: 523–561.
- Saiki, R. K., S. Scharfm, F. Faloona, K. B. Mullis, G. T. Horn, H. A. Erlich, and N. Arheim. 1985. Enzymatic amplification of B-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230: 1350–1354.
- Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2d ed. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
10.1111/j.1095-8312.1996.tb01434.x Google Scholar
- Schmid, M., I. Nanda, C. Steinlein, K. Kausch, and T. Haaf. 1991. Sex-determining mechanisms and sex chromosomes in Amphibia. Pp. 393–430 in D. S. Green and S. K. Sessions, eds. Amphibian cytogenetics and evolution. Academic Press, San Diego.
10.1016/B978-0-12-297880-7.50020-2 Google Scholar
- Spolsky, C., and T. Uzzell. 1984. Natural interspecies transfer of mitochondrial DNA in amphibians. Proceedings of the National Academy of Sciences, USA. 81: 5802–5805.
- Spolsky, C., and T. Uzzell. 1980. Polyploidy in plants: unsolved problems and prospects. Pp. 495–520 in W. Lewis, ed. Polyploidy: biological relevance. Plenum, New York.
10.1007/978-1-4613-3069-1_26 Google Scholar
- Swofford, D. L. 1989. PAUP: phylogenetic analysis using parsimony (version 3.0s). Illinois Natural History Survey, Champaign, Ill.
- Templeton, A. R. 1983. Convergent evolution and nonparametric inferences from restriction data and DNA sequences. Pp. 151–179 in B. S. Weir, ed. Statistical analysis of DNA sequence data. Marcel Dekker, New York.
- Tymowska, J. 1991. Polyploidy and cytogenetic variation in frogs of the genus Xenopus. Pp. 259–297 in D. S. Green and S. K. Sessions, eds. Amphibian cytogenetics and evolution. Academic Press, San Diego.
10.1016/B978-0-12-297880-7.50016-0 Google Scholar
- Wasserman, A. O. 1970. Polyploidy in the common tree toad, Hyla versicolor Le Conte. Science 167: 385–386.
- White, M. J. D. 1954. Animal cytology and evolution, 2d ed. Cambridge University Press, Cambridge.
- White, M. J. D. 1978. Modes of speciation. W. H. Freeman, San Francisco.
- Wiley, J. E. 1983. Chromosome polymorphism in Hyla chrysoscelis. Copeia 1983: 273–275.
- Wiley, J. E., M. L. Little, M. A. Romano, D. A. Blount, and G. R. Cline. 1989. Polymorphism in the location of the 18s and 28s rRNA genes on the chromosomes of the diploid tetraploid treefrogs Hyla chrysoscelis and H. versicolor. Chromosoma 97: 481–487.
- Wright, J. W., C. Spolsky, and W. M. Brown. 1983. The origin of the parthenogenetic lizard Cnemidophorus laredoensis inferred from mitochondrial DNA analysis. Herpetologica 39: 410–416.
- Yoneyama, Y. 1987. The nucleotide sequences of the heavy and light strand replication origins of the Rana catesbeiana mitochondrial genome. Nippon Ika Daigaku Zasshi 54: 429–440.
