Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes

Genome

Volumn 50, Issue 2, 2007, Pages 119-136

  Bogart, James P ^a   Bi, Ke ^a   Fu, Jinzong ^a   Noble, Daniel W A ^a   Niedzwiecki, John ^b,c  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF CINCINNATI   (United States)

Author keywords

D loop; Intergenic spacer; Kleptogenesis; Microsatellite DNA; Polyploidy; Reproductive mode; Unisexual ambystoma

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA; PRIMER DNA;

ALLELE; AMPHIBIA; ANIMAL; ARTICLE; BIOLOGICAL MODEL; GENETICS; GENOTYPE; HAPLOTYPE; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLOIDY; POLYPLOIDY; SPECIES DIFFERENCE; THEORETICAL MODEL;

ALLELES; ANIMALS; DNA PRIMERS; DNA, MITOCHONDRIAL; GENOTYPE; HAPLOTYPES; MICROSATELLITE REPEATS; MODELS, GENETIC; MODELS, THEORETICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLOIDIES; POLYPLOIDY; SPECIES SPECIFICITY; URODELA;

AMBYSTOMA; AMBYSTOMA BARBOURI; AMBYSTOMATIDAE; EUKARYOTA; SALAMANDROIDEA;

EID: 34249774300     PISSN: 08312796     EISSN: None     Source Type: Journal    
DOI: 10.1139/G06-152     Document Type: Article

References (62)

1. Alves, M.J., Coelho, M.M., and Collares-Pereira, M.J. 2001. Evolution in action through hybridization and polyploidy in an Iberian freshwater fish: a genetic review. Genetica, 111: 375-385. doi:10.1023/A:1013783029921.
2. Avise, J.C., Quattro, J.M., and Vrijenhoek, R.C. 1992. Molecular clones within organismal clones. Evol. Biol. (N.Y.), 26: 225-246.
3. Ballard, J.W.O., and Whitlock, M.C. 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13: 729-744. doi:10.1046/j. 1365-294X.2003.02063.X.
4. Bi, K., and Bogart, J.P. 2006. Identification of intergenomic recombinations in unisexual slamanaders of the genus Ambystoma by genomic in situ hybridization. Cytogenet. Genome Res. 112: 307-312. doi:10.1159/000089885.
5. Bogart, J.P. 1982. Ploidy and genetic diversity in Ontario salamanders of the Ambystoma jeffersonianum complex revealed through and electrophoretic examination of larvae. Can. J. Zool. 60: 848-855.
6. Bogart, J.P. 2003. Genetics and systematics of hybrid species. In Reproductive biology and phylogeny of Urodela. Edited by D.M. Sever, M/s Science, Enfield, New Hampshire. Vol. 1. pp. 109-134.
7. Bogart, J.P., and Klemens, M.W. 1997. Hybrids and genetic interactions of mole salamanders (Ambystoma jeffersonianum and A. laterale) (Amphibia: Caudata) in New York and New England. Am. Mus. Novit. 3218: 1-78.
8. Bogart, J.P., and Licht, L.E. 1986. Reproduction and the origin of polyploids in hybrid salamanders of the genus Ambystoma. Can. J. Genet. Cytol. 28: 605-617.
9. Bogart, J.P., Licht, L.E., Oldham, M.J., and Darbyshire, S.J. 1985. Electrophoretic identification of Ambystoma laterale and Ambystoma texanum as well as their diploid and triploid interspecific hybrids (Amphibia: Caudata) on Pelee Island, Ontario. Can. J. Zool. 63: 340-347.
10. Bogart, J.P., Lowcock, L.A., Zeyl, C.W., and Mable, B.K. 1987. Genome constitution and reproductive biology of the Ambystoma hybrid salamanders on Kelleys Island in Lake Erie. Can. J. Zool. 65: 2188-2201.
11. Bogart, J.P., Elinson, R.P., and Licht, L.E. 1989. Temperature and sperm incorporation in polyploid salamanders. Science (Washington, D.C.), 246: 1032-1034. doi:10.1126/science.2587986.
12. Calkin, P.E., and Feenstra, B.H. 1985. Evolution of the Erie-basin Great Lakes. In Quaternary evolution of the Great Lakes. Edited by P.F. Karrow and P.E. Calkin. Geol. Assoc. Can. Spec. Pap. 30. St. Johns, Newfoundland, pp. 149-170.
13. Canadian Council on Animal Care. 2003. Guidelines on: the care and use of wildlife. CCAC species-specific recommendations on: amphibians and reptiles. Available from http://www.ccac.ca/ en/CCAC_Programs/Guidelines_Policies/GDLINES/ AmphibiansReptiles.htm.
14. Conant, R., and Collins, J.T. 1998. Reptiles and amphibians: eastern and central North America (3rd ed.). Houghton Mifflin, Boston, New York.
15. Dawley, R.M., and Bogart, J.P. 1989. Evolution and ecology of unisexual vertebrates. New York State Mus. Bull. 466, Albany.
16. Dubois, A., and Günther, R. 1982. Klepton and synklepton: Two new evolutionary systematics categories in zoology. Zool. Jb. Syst. 109: 290-305.
17. Duellman, W.E., and Trueb, L. 1986. Biology of amphibians. McGraw Hill, New York.
18. Downs, F.L. 1978. Unisexual Ambystoma from the Bass Islands of Lake Erie. Occ. Pap. Mus. Zool. Univ. Mich. 685: 1-36.
19. Elinson, R.P., Bogart, J.P., Licht, L.E., and Lowcock, L.A. 1992. Gynogenetic mechanisms in polyploid hybrid salamanders. J. Exp. Zool. 264: 93-99. doi:10.1002/jez.1402640114.
20. Frost, D.R., and Hillis, D.M. 1990. Species in concept and practice: herpetological applications. Herpetologica, 46: 87-104.
21. Fu, J., Murphy, R.W., and Darevsky, I.S. 2000. Divergence of the cytochrome b gene in the Lacerta raddei complex and its parthenogenetic daughter species: evidence for recent multiple origins. Copeia, 2000: 432-440. doi:10.1643/0045-8511(2000) 000[0432:DOTCBG]2.0.CO;2.
22. Gómez-Zurita, J., Funk, D.J., and Vogler, A.P. 2006. The evolution of unisexuality in Calligrapha leaf beetles: molecular and ecological insights on multiple origins via interspecific hybridization. Evolution, 60: 328-347. doi:10.1554/05-452.1.
23. Haccou, P., and Schneider, M.V. 2004. Modes of reproduction and the accumulation of deleterious mutations with multiplicative fitness effects. Genetics, 166: 1093-1104. doi:10.1534/genetics. 166.2.1093.
24. Hedges, S.B., Bogart, J.P., and Maxson, L.R. 1992. Ancestry of unisexual salamanders. Nature (London), 356: 708-710. doi:10.1038/356708a0.
25. Highton, R. 1995. Speciation in eastern North American salamanders of the genus Plethodon. Annu. Rev. Ecol. Syst. 26: 579-600. doi:10.1146/annurev.es.26.110195.003051.
26. Highton, R., Maha, G.C., and Maxson, L.R. 1989. Biochemical evolution in the slimy salamanders of the Plethodon glutinosus complex in the eastern United States. Illinois Biol. Monogr. 57: 1-153.
27. Huelsenbeck, J.P., and Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17: 754-755. doi:10.1093/ bioinformatics/17.8.754.
28. Janko, K., Kotlik, P., and Rab, P. 2003. Evolutionary history of asexual hybrid loaches (Cobitis: Teleostei) inferred from phylogenetic analysis of mitochondrial DNA variation. J. Evol. Biol. 16: 1280-1287. doi:10.1046/j.1420-9101.2003.00627.x.
29. Judson, O.P., and Normark, B.B. 1996. Ancient asexual scandals. Trends Ecol. Evol. 11: 41-46.
30. Julian, S.E., King, T.L., and Savage, W.K. 2003. Novel Jefferson salamander, Ambystoma jeffersonianum, microsatellite DNA markers detect population structure and hybrid complexes. Mol. Ecol. Notes, 3: 95-97. doi:10.1046/j.1471-8286.2003.00362.x.
31. King, R.B., Oldham, M.J., Weller, W.F., and Wynn, D. 1996. Historic and current amphibian and reptile distributions in the island region of western Lake Erie. Am. Midl. Nat. 138: 153-173.
32. Kraus, F., and Miyamoto, M.M. 1990. Mitochondrial genotype of a unisexual salamander of hybrid origin is unrelated to either of its nuclear haplotypes. Proc. Natl. Acad. Sci. U.S.A. 87: 2235-2238. doi:10.1073/pnas.87.6.2235.
33. Kraus, F., and Petranka, J.W. 1989. A new sibling species of Ambystoma from the Ohio River drainage. Copeia, 1989: 94-110. doi:10.2307/1445610.
34. Kraus, F., Ducey, P.K., Moler, P., and Miyamoto, M.M. 1991. Two new triparental unisexual Ambystoma from Ohio and Michigan. Herpetologica, 47: 429-439.
35. Lowcock, L.A. 1994. Biotype, genomotype, and genotype: variable effects of polyploidy and hybridity on ecological partitioning in a bisexual-unisexual community of salamanders. Can. J. Zool. 72: 104-117.
36. Lowcock, L.A., and Bogart, J.P. 1989. Electrophoretic evidence for multiple origins of triploid forms in the Ambystoma laterale - jeffersonianum complex. Can. J. Zool. 67: 350-356.
37. Lowcock, L.A., Licht, L.E., and Bogart, J.P. 1987. Nomenclature in hybrid complexes of Ambystoma: no case for the erection of hybrid "species". Syst. Zool. 36: 328-336. doi:10.2307/2413070.
38. Macgregor, H.C., and Uzzell, T.M., Jr. 1964. Gynogenesis in salamanders related to Ambystoma jeffersonianum. Science (Washington, D.C.), 143: 1043-1045. doi:10.1126/science.143.3610. 1043.
39. Mateos, M., and Vrijenhoek, R.C. 2002. Ancient versus reticulate origin of a hemiclonal lineage. Evolution, 56: 985-992. doi:10.1554/0014- 3820(2002)056[0985:AVROOA]2.0.CO;2.
40. Maynard Smith, J. 1978. The evolution of sex. Cambridge University Press, Cambridge, UK.
41. Maynard Smith, J. 1992. Age and the unisexual lineage. Nature (London), 356: 661-662. doi:10.1038/356661a0.
42. McKnight, M.L., and Shaffer, H.B. 1997. Large rapidly evolving intergenic spacers in the mitochondrial DNA of the salamander family Ambystomatidae (Amphibia: Caudata). Mol. Biol. Evol. 14: 1167-1176.
43. Myers, E.M., and Zamudio, K.R. 2004. Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success. Mol. Ecol. 13: 1951-1963. doi:10.1111/j.1365-294X. 2004.02208.x.
44. Niedzwiecki, J. 2005. Evolutionary history and hybridization of two mole salamander sister species from different habitats. Ph.D. thesis, University of Kentucky.
45. Normark, B.B., Judson, O.P., and Moran, N.A. 2003. Genomic signatures of ancient asexual lineages. Biol. J. Linn. Soc. 79: 69-84. doi:10.1046/j.1095-8312.2003.00182.x.
46. Otto, S.P., and Whitton, J. 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34: 401-437. doi:10.1146/annurev. genet.34.1.401.
47. Petranka, J.W. 1998. Salamanders of the United States and Canada. Smithsonian Instution Press. Washington.
48. Robertson, A.V., Ramsden, C., Niedzwiecki, J., Fu, J., and Bogart, J.P. 2006. An unexpected recent ancestor of unisexual Ambystoma. Mol. Ecol. 15: 3339-3351. doi:10.1111/j.1365-294X. 2006.03005.x.
49. Samuels, A.K., Weisrock, D.W., Smith, J.J., France, K.J., Walker, J.A., Putta, S., and Voss, S.R. 2005. Transcriptional and phylogenetic analysis of five complete ambystomatid salamander mitochondrial genomes. Gene, 349: 43-53. doi:10.1016/j.gene. 2004.12.037.
50. Selander, T.C. 1994. Reproduction of unisexual hybrid Ambystoma (Urodela: Ambystomatidae) in the absence of parental species. M.Sc. thesis, Univ. Dayton, Dayton, Ohio.
51. Selkoe, K.A., and Toonen, R.J. 2006. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol. Lett. 9: 615-629. doi:10.1111/j.1461-0248.2006.00889.x.
52. Shaffer, H.B., and McKnight, M.L. 1996. The polytypic species revisited: genetic differentiation and molecular phylogenetics of the tiger salamander Ambystoma tigrinum (Amphibia: Caudata) complex. Evolution, 50: 417-433. doi:10.2307/2410811.
53. Simon, J.C., Delmotte, F., Rispe, C., and Crease, T. 2003. Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol. J. Linn. Soc. 79: 151-163. doi:10.1046/j.1095-8312.2003.00175.x.
54. Spolsky, C.M., Philips, C.A., and Uzzell, T. 1992. Antiquity of clonal salamander lineages revealed by mitochondrial DNA. Nature (London), 356: 706-708. doi:10.1038/356706a0.
55. Swofford, D.L. 2001. PAUP*: Phylogenetic analysis using parsimony and other methods, v. 4.01b10 [computer program]. Sinauer Associates, Sunderland.
56. Taylor, D.J., and Foighil, D.O. 2000. Transglobal comparisons of nuclear and mitochondrial genetic structure in a marine polyploid clam (Lasaea, Lasaeidae). Heredity, 84: 321-330. doi:10.1046/J.1365-2540.2000.00673.x.
57. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. 1994. The CLUSAL X windows interface: flexible strategies for multiple sequence alignment aided by quality anlaysis tools. Nucleic Acids Res. 25: 4876-4882.
58. Uzzell, T.M. 1969. Notes on spermatophore production by salamanders of the Ambystoma jeffersonianum complex. Copeia, 1969: 602-612. doi:10.2307/1441940.
59. Uzzell, T.M., and Goldblatt, S.M. 1967. Serum proteins of salamanders of the Ambystoma jeffersonianum complex. Copeia, 1967: 602-612.
60. Vrijenhoek, R.C., Angus, R.A., and Schultz, R.J. 1977. Variation and heterozygosity in sexual vs. clonally reproducing populations of Poeciliopsis. Evolution, 31: 767-781. doi:10.2307/ 2407438.
61. Williams, G.R. 1975. Sex and Evolution. Princeton University Press, Princeton, N.J.
62. Zamudio, K.R., and Savage, W.K. 2003. Historical isolation, range expansion and secondary contact of two highly divergent mitochondrial lineages in spotted salamanders (Ambystoma maculatum). Evolution, 57: 1631-1652.