Advertisement

Apomictic Reproduction in the Amazon Molly, Poecilia formosa, and Its Triploid Hybrids

  • Paul J. Monaco
  • Ellen M. Rasch
  • Joseph S. Balsano
Part of the Monographs in Evolutionary Biology book series (MEBI)

Abstract

The Amazon molly, Poecilia formosa, initially described in 1859 by Girard, is the first vertebrate in which unisexuality was recognized (Hubbs and Hubbs, 1932). Poecilia formosa is intermediate in form between two sexual species, Poecilia latipinna (LeSueur) and Poecilia mexicana Steindachner and is thought to have arisen in nature as a hybrid of these species (Hubbs and Hubbs, 1932; Hubbs, 1955, 1964; Abramoff et al., 1968; Prehn and Rasch, 1969; Balsano et al., 1972). Poecilia formosa is not a true thelytokous parthenogen as defined by White (1973); instead, it reproduces by gynogenesis, a mechanism that is sperm dependent. Males of related sexual species provide sperm, which serve only to activate the egg. Functional syngamy does not occur. Thus, developing embryos are derived from diploid ova that contain only maternal chromosomes and each daughter is a genetic copy of its mother (Meyer, 1938; Hubbs and Hubbs, 1946; Kallman, 1962a,b,c; Hubbs, 1964; Rasch et al., 1965; Darnell et al.,1967; Schultz, 1969; Uzzell, 1970; White, 1973). The obligatory dependence on sperm that is a hallmark of gynogenetic reproduction compels P. Formosa to behave in nature as a sexual parasite on closely related, sympatric bisexual species (Hubbs, 1964). Although a variety of poeciliid males can “father” P. formosa in the laboratory (Hubbs and Hubbs, 1946), the survival and success in nature of these all-female forms require their coincident distribution with at least one of the bisexual host species.

Keywords

Synaptonemal Complex Meiotic Prophase Triploid Hybrid Primary Oocyte Maturation Division 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abramoff, P., Darnell, R. M., and Balsano, J. S., 1968, Electrophoretic demonstration of the hybrid origin of the gynogenetic teleost P. formosa, Am. Nat. 102: 555–558.CrossRefGoogle Scholar
  2. Anders, A., Anders, F., and Klinke, K., 1973, Regulation of gene expression in the Gordon—Kosswig melanoma system. II. The arrangement of chromatophore determining loci and regulating elements in the sex chromosomes of Xiphophorin fish, Platypoecilus maculatus and Platypoecilus variatus, in: Genetics and Mutagenesis of Fish ( J. H. Schroder, ed.) Springer-Verlag, Berlin, pp. 53–67.CrossRefGoogle Scholar
  3. Anders, F., Chatterjee, K., Schwab, M., Scholl, E., and Anders, A., 1981, Tumor gene expression and interphase chromatin appearance in Xiphophorus, Am. Zool. 21: 535–548.Google Scholar
  4. Balsano, J. S., and Rasch, E. M., 1974, Biochemical and cytogenetic studies of Poecilia from eastern Mexico I. Comparative microelectrophoresis of plasma proteins of seven species, Rev. Biol. Trop. 21: 229–257.Google Scholar
  5. Balsano, J. S., Darnell, R. M., and Abramoff, P., 1972, Electrophoretic evidence of triploidy associated with populations of the gynogenetic teleost Poecilia formosa, Copeia 1972: 292–297.CrossRefGoogle Scholar
  6. Cimino, M. C., 1971, Meiosis in triploid all-female fish (Poeciliopsis, Poeciliidae), Science 175: 1484–1486.CrossRefGoogle Scholar
  7. Cimino, M. C., 1972, Egg production,polyploidization, and evolution in a diploid all female fish of the genus Poeciliopsis, Evolution 26: 294–306.CrossRefGoogle Scholar
  8. Crow, J. F., and Kimura, M., 1965, Evolution in sexual and asexual populations, Am. Nat. 49: 439–450.CrossRefGoogle Scholar
  9. Cuellar, O., 1971, Reproduction and the mechanism of meiotic restitution in the parthenogenetic lizard Cnemidophorus uniparens, J. Morphol. 133: 139–166.CrossRefGoogle Scholar
  10. Cuellar, O., 1974, On the origin of parthenogenesis in vertebrates: The cytological factors, Am. Nat. 108: 625–648.CrossRefGoogle Scholar
  11. Cuellar, O., 1976, Cytology of meiosis in the triploid gynogenetic salamander Ambystoma tremblayi, Chromosoma (Berl.) 58: 355–364.CrossRefGoogle Scholar
  12. Cuellar, O., 1977, Animal parthenogenesis, Science 197: 837–843.PubMedCrossRefGoogle Scholar
  13. Darnell, R. M., Lamb, E., and Abramoff, P., 1967, Matroclinous inheritance and clonal structure of a Mexican population of the gynogenetic fish Poecilia formosa, Evolution 21: 168–178.CrossRefGoogle Scholar
  14. Grell, R. F., 1973, Recombination and DNA replication in the Drosophilia melanogaster oocyte, Genetics 73: 87–103.PubMedGoogle Scholar
  15. Grell, R. F., Oakberg, E. F., and Generoso, E. E., 1980, Synaptonemal complexes of premeiotic interphase in the mouse spermatocyte, Proc. Natl. Acad. Sci. USA 77: 6720–6723.PubMedCrossRefGoogle Scholar
  16. Hubbs, C. L., 1955, Hybridization between fish species in nature, Syst. Zool. 4: 1–20.CrossRefGoogle Scholar
  17. Hubbs, C., 1964, Interactions between a bisexual fish species and its gynogenetic sexual parasite, Bull. Tex. Mem. Mus. 8: 1–72.Google Scholar
  18. Hubbs, C. L., and Hubbs, L. C., 1932, Apparent parthenogenesis in nature, in a form of fish of hybrid origin, Science 76: 628–630.PubMedCrossRefGoogle Scholar
  19. Hubbs, C. L., and Hubbs, L. C., 1946, Experimental breeding of the amazon molly, Aquarium J. 17: 4–6.Google Scholar
  20. Huskins, C. L., 1932, A cytological study of Vilmorin’s unfixable dwarf wheat, J. Genet. 25: 113–124.CrossRefGoogle Scholar
  21. Jacobs, P. A., Angell, R. R., Buchanan, 1. M., Hassold, T. J., Matsayama, A. M., and Manuel, B., 1978, The origin of human triploids, Ann. Hum. Genet. 42: 49–57.CrossRefGoogle Scholar
  22. Kallman, K. D., 1962a, Gynogenesis in the teleost Mollienesis formosa with a discussion of the detection of parthenogenesis in vertebrates by tissue transplantation, J. Genet. 58: 7–21.CrossRefGoogle Scholar
  23. Kallman, K. D., 1962b, Population genetics of the gynogenetic teleost, Moclienesia formosa, Evolution 16: 497–504.CrossRefGoogle Scholar
  24. Kallman, K. D., 1962c, Population structure of the all female gynogenetic teleost, Molliensia formosa (Girard), Proc. XVI Int. Cong. Zool. 2:170, abstract.Google Scholar
  25. Kallman, K. D., 1964, Homozygosity in a gynogenetic fish, Poecilia formosa, Genetics 50: 260–262.Google Scholar
  26. Kallman, K. D., 1975, The platyfish, Xiphophorus maculatus, in: Handbook of Genetics, Vol. 4 ( R. C. King, ed.), Plenum Press, New York, pp. 81–132.Google Scholar
  27. Kobaysi, H., 1976, A cytological study on the maturation division in the oogenic process of the triploid ginbuna Carassius auratus Iangsdorfii, Jpn. J. Ichthyol. 22: 234–240.Google Scholar
  28. Koch, P., Pijnacker, L. P., and Kreke, J., 1972, DNA reduplication during meiotic prophase in the oocyte of Carausius morosus Br. (Insecta, Cheleutoptera), Chromosoma (Berl.) 36: 313–321.CrossRefGoogle Scholar
  29. Macgregor, H. C., and Uzzell, T. M., 1964, Gynogenesis in salamanders related to Ambystoma jeffersonianum, Science 143: 1043–1045.PubMedCrossRefGoogle Scholar
  30. Maslin, T. P., 1968, Taxonomic problems in parthenogenetic vertebrates, Syst. Zool. 17: 219–231.CrossRefGoogle Scholar
  31. Menzel, B. W., and Darnell, R. M., 1973, Systematics of Poecilia mexicana (Pisces: Poeciliidae) in northern Mexico, Copeia 1973: 225–227.CrossRefGoogle Scholar
  32. Meyer, H., 1938, Investigations concerning the reproductive behavior of Molliensia formosa, J. Genet. 36: 329–366.CrossRefGoogle Scholar
  33. Monaco, P. J., 1982, Reproductive biology of Poecilia formosa and its related species, Ph.D. dissertation, Marquette University.Google Scholar
  34. Monaco, P. J., Rasch, E. M., and Balsano, J. S., 1978, Cytological evidence for temporal differences during the’asynchronous ovarian maturation of bisexual and unisexual fishes of the genus Poecilia, J. Fish Biol. 13: 33–44.CrossRefGoogle Scholar
  35. Monaco, P. J., Rasch, E. M., and Balsano, J. S., 1981a, Nucleoprotein cytochemistry during oogenesis in a unisexual fish, Poecilia formosa, Histochem. J. 13: 747–761.PubMedCrossRefGoogle Scholar
  36. Monaco, P. J., Rasch, E. M., and Balsano, J. S., 1981b, Sperm availability in naturally occurring bisexual—unisexual breeding complexes involving Poecilia mexicana and the gynogenetic teleost Poecilia formosa, Environ. Biol. Fish. 6: 159–166.CrossRefGoogle Scholar
  37. Monaco, P. J., Rasch, E. M., Balsano, J. S., and B. J. Turner, 1982, Muscle protein phenotypes and the probable evolutionary origin of a unisexual fish, Poecilia formosa, and its triploid derivative, J. Exp. Zool. 221: 265–274.CrossRefGoogle Scholar
  38. Moses, M. J., 1968, Synaptinemal complex, Annu. Rev. Genet. 2: 363–412.CrossRefGoogle Scholar
  39. Nur, U., 1979, Gonoid thelytoky in soft scale insects (Coccidae: Homoptera), Chromosoma (Berl.) 72: 89–104.CrossRefGoogle Scholar
  40. Nygren, P., 1954, Apomixis in angiosperms, Bot. Rev. 20: 577–649.CrossRefGoogle Scholar
  41. Pijnacker, L. P., and Koch, P., 1975, Complete and incomplete extra DNA reduplication during spermatogenesis of Carausius morosus Br. (Insecta, Phasmida), Chromosoma (Berl.) 49: 269–278.CrossRefGoogle Scholar
  42. Prehn, L. M., and Rasch, E. M., 1969, Cytogenetic studies of Poecilia (Pisces) I. Chromosome numbers in naturally occurring poeciliied species and their hybrids from eastern Mexico, Can. J. Genet. Cytol. 11: 880–895.PubMedGoogle Scholar
  43. Rasch, E. M., 1968, Use of deoxyribonucleic acid-Feulgen levels as an index of triploidy in naturally occurring interspecific hybrids of poeciliid fishes, J. Histochem. Cytochem. 16:508–509, abstract.Google Scholar
  44. Rasch, E. M., and Balsano, J. S., 1973, Cytogenetic studies of Poecilia (Pisces) III. Persistence of triploid genomes in the unisexual progeny of triploid females associated with Poecilia formosa, Copeia 1973: 810–813.CrossRefGoogle Scholar
  45. Rasch, E. M., and Balsano, J. S., 1974, Biochemical and cytogenetic studies of Poecilia from eastern Mexico II. Frequency, prepetuation, and probable origin of triploid genomes in females associated with Poecilia formosa, Rev. Biol. Trop. 21: 351–381.Google Scholar
  46. Rasch, E. M., Darnell, R. M., Kallman, K. D., and Abramoff, P., 1965, Cytophotometric evidence for triploidy in hybrids of the gynogenetic fish, Poecilia formosa, J. Exp. Zool. 160: 155–170.PubMedCrossRefGoogle Scholar
  47. Rasch, E. M., Prehn, L. M., and Rasch, R. W., 1970, Cytogenetic studies of Poecilia (Pisces) II. Triploidy and DNA levels in naturally occuring populations associated with the gynogenetic teleost) Poecilia formosa (Girard), Chromosoma (Berl.) 31: 18–40.CrossRefGoogle Scholar
  48. Rasch, E. M., Monaco, P. J., and Balsano, J. S., 1978, Identification of a new form of triploid hybrid fish by DNA-Feulgen cytophotometry, J. Histochem. Cytochem. 26:218, abstract.Google Scholar
  49. Rasch, E. M., Monaco, P. J., and Balsano, J. S., 1982, Cytophotometric and autoradio-graphic evidence for functional apomixis in a unisexual fish Poecilia formosa and its related triploid unisexuals, Histochemistry 73: 515–533.PubMedCrossRefGoogle Scholar
  50. Rosen, D. E., and Bailey, R. M., 1963, The poeciliid fishes (Cyprinodontiformes), their structure, zoogeography, and systematics, Bull. Am. Mus. Nat. Hist. 126: 1–176.Google Scholar
  51. Schultz, R. J., 1969, Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates, Am. Nat. 103: 605–619.CrossRefGoogle Scholar
  52. Schultz, R. J., 1980, Role of polyploidy in the evolution of fishes, in: Polyploidy: Biological Relevance ( W. H. Lewis, ed.), Plenum Press, New York, pp. 313–340.Google Scholar
  53. Schultz, R. J., and Kallman, K. D., 1968, Triploid hybrids between the all female teleost Poecilia formosa and Poecilia sphenops, Nature 219: 280.CrossRefGoogle Scholar
  54. Strommen, C. A., Rasch, E. M., and Balsano, J. S., 1975a, Cytogenetic studies of Poecilia (Pisces) IV. Epithelial cell biopses to identify triploid females associated with Poecilia formosa, Copeia 1975: 568–572.CrossRefGoogle Scholar
  55. Strommen, C. A., Rasch, E. M., and Balsano, J. S., I975b, Cytogenetic studies of Poecilia (Pisces) V. Cytophotometric evidence for the production of fertile offspring by triploids related to Poecilia formosa, J. Fish Biol. 7: 1–10.Google Scholar
  56. Swanson, C. P., Merz, T., and Young, W. S., 1967, Cytogenetics, Prentice-Hall, Englewood Cliffs, New Jersey.Google Scholar
  57. Turner, B. J., 1982, The evolutionary genetics of a unisexual fish, Poecilia formosa, in: Mechanisms of Speciation, A. R. Liss, New York, pp. 265–305.Google Scholar
  58. Turner, B. J., Balsano, J. S., Monaco, P. J., and Rasch, E. M., 1983, Clonal diversity and evolutionary dynamics in a diploid—tripolid breeding complex of unisexual fishes (Poe-cilia), Evolution, 37 (4): 798–809.CrossRefGoogle Scholar
  59. Uzzell, T. M., 1970, Meiotic mechanisms of naturally occurring unisexual vertebrates, Am. Nat. 104: 433–445.CrossRefGoogle Scholar
  60. White, M. J. D., 1973, Animal Cytology and Evolution, Cambridge University Press, London.Google Scholar
  61. White, M. J. D., Contreras, Cheney, J., and Webb, G. C., 1977, Cytogenetics of the parthenogenetic grasshopper Warramaba (formerly Moraba) virgo and its bisexual relatives II. Hybridization studies, Chromosoma (Berl.) 61: 127–148.CrossRefGoogle Scholar
  62. Yamamoto, T., 1975, The medaka, Oryzias latipes, and the guppy, Lebistes reticularis, in: Handbook of Genetics, Vol. 4 ( R. C. King, ed.), Plenum Press, New York, pp. 133–149.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Paul J. Monaco
    • 1
  • Ellen M. Rasch
    • 1
  • Joseph S. Balsano
    • 2
  1. 1.Department of Biophysics, Quillen-Dishner College of MedicineEast Tennessee State UniversityJohnson CityUSA
  2. 2.Biomedical Research InstituteUniversity of Wisconsin-ParksideKenoshaUSA

Personalised recommendations