Skip to main content
Log in

Homologous Versus Antithetic Alternation of Generations and the Origin of Sporophytes

  • Published:
The Botanical Review Aims and scope Submit manuscript

Abstract

The late-nineteenth/early-twentieth century debate over homologous versus antithetic alternation of generations is reviewed. Supporters of both theories, at first, used Coleochaete as a model for the origin of land-plant life cycles. The early debate focused on the morphological interpretation of the sporophyte and on whether vascular cryptogams had bryophyte-like ancestors. The terms of the debate shifted after the discovery that the alternation of morphological generations was accompanied by an alternation of chromosome number. Supporters of homologous alternation now promoted a model in which land plants had been derived from an algal ancestor with an isomorphic alternation of haploid and diploid generations whereas supporters of antithetic alternation favored a model in which land plants were derived from a haploid algal ancestor with zygotic meiosis. Modern evidence that embryophytes are derived from charophycean green algae is more compatible with an updated version of the antithetic theory.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Literature Cited

  • Allen, C. E. 1905. Die Keimung der Zygote bei Coleochaete. Berichte der deutschen botanischen Gesellschaft 23: 285–292.

    Google Scholar 

  • Berkeley, M. J. 1857. Introduction to cryptogamic botany. Bailliere, London.

    Google Scholar 

  • Bierhorst, D. W. 1953. Structure and development of the gametophyte of Psilotum nudum. American Journal of Botany 40: 649–658.

    Article  Google Scholar 

  • Bierhorst, D. W. 1954. The gametangia and embryo of Psilotum nudum. American Journal of Botany 41: 274–281.

    Article  Google Scholar 

  • Bierhorst, D. W. 1969. On Stromatopteris and its ill-defined organs. American Journal of Botany 56: 160–174.

    Article  Google Scholar 

  • Blackwell, W. H. 2003. Two theories of origin of the land-plant sporophyte: which is left standing? Botanical Review 69: 125–148.

    Article  Google Scholar 

  • Bower, F. O. 1887a. On apospory and related phenomena. Transactions of the Linnean Society of London, Second Series 2: 301–326.

    Google Scholar 

  • Bower, F. O. 1887b. On the limits of the use of the terms ‘phyllome’ and ‘caulome.’ A suggestion. Annals of Botany 1: 133–146.

    Google Scholar 

  • Bower, F. O. 1890. On antithetic as distinct from homologous alternation of generations in plants. Annals of Botany 4: 347–370.

    Google Scholar 

  • Bower, F. O. 1898. Opening address to the British Association, Bristol meeting, Section K (Botany). Nature 59: 66–69, 88–91, 112–114.

    Google Scholar 

  • Bower, F. O. 1908. The origin of a land flora. Macmillan, London.

    Google Scholar 

  • Bower, F. O. 1935. Primitive land plants, also known as the archegoniatae. Macmillan, London.

    Google Scholar 

  • Brown, R. C., & B. E. Lemmon. 1997. The quadripolar microtubule system in lower land plants. Journal of Plant Research 110: 93–106.

    Article  Google Scholar 

  • Campbell, D. H. 1903. Antithetic versus homologous alternation. American Naturalist 37: 153–169.

    Article  Google Scholar 

  • Campbell, D. H. 1905. The structure and development of mosses and ferns (Archegoniatae), second edition. MacMillan, New York

  • Celakovsky, L. 1874. Ueber die verschiedenen Formen und die Bedeutung des Generationswechsels der Pflanzen. Sitzungsberichte der königlich böhmischen Gesellschaft der Wissenschaften in Prag 1874: 21–61.

    Google Scholar 

  • Chamberlain, C. J. 1917. Prothallia and sporelings of three New Zealand species of Lycopodium. Botanical Gazette 63: 51–65.

    Article  Google Scholar 

  • Chamisso, A. V. 1819. De animalibus quibusdam e classe Vermium Linnaeana in circumnavigatione terrae. Fasciculus primus. De Salpa. Dümmler, Berlin.

    Google Scholar 

  • Coulter, J. M. 1899. The origin of the leafy sporophyte. Botanical Gazette 28: 46–59.

    Article  Google Scholar 

  • Dassler, C. L., & D. R. Farrar. 1997. Significance of form in fern gametophytes: clonal gemmiferous gametophytes of Callistopteris baueriana (Hymenophyllaceae). International Journal of Plant Sciences 158: 622–639.

    Article  Google Scholar 

  • Farley, J. 1982. Gametes and spores. Ideas about sexual reproduction 1750–1914. Johns Hopkins University Press, Baltimore.

    Google Scholar 

  • Farlow, W. G. 1874. An asexual growth from the prothallus of Pteris cretica. Quarterly Journal of Microscopical Science 14: 266–272.

    Google Scholar 

  • Farmer, J. B., & L. Digby. 1907. Studies in apospory and apogamy in ferns. Annals of Botany 21: 161–191.

    Google Scholar 

  • Föyn, B. 1929. Untersuchungen über die Sexualität und Entwicklung von Algen. IV. Vorläufige Mitteilung über die Sexualität und den Generationswechsel von Cladophora und Ulva. Berichte der Deutschen Botanischen Gesellschaft 47: 495–506.

    Google Scholar 

  • Fritsch, F. E. 1916. The algal ancestry of the higher plants. New Phytologist 15: 233–250.

    Article  Google Scholar 

  • Goebel, K. V. 1926. Wilhelm Hofmeister. The work and life of a nineteenth century botanist. Ray Society, London [H. M. Bower, translator].

    Google Scholar 

  • Graham, L. E. 1985. The origin of the life cycle of land plants. American Scientist 73: 178–186.

    Google Scholar 

  • Graham, L. K. E., & L. W. Wilcox. 2000. The origin of alternation of generations in land plants: a focus on matrotrophy and hexose transport. Philosophical Transactions of the Royal Society of London B 355: 757–766.

    Article  CAS  Google Scholar 

  • Groth-Malonek, M., & V. Knoop. 2005. Bryophytes and other basal land plants: the mitochondrial perspective. Taxon 54: 293–297.

    Google Scholar 

  • Hartmann, M. 1929. Untersuchungen über die Sexualität und Entwicklung von Algen. III. Über die Sexualität und den Generationswechsel von Chaetomorpha und Enteromorpha. Berichte der Deutschen Botanischen Gesellschaft 47: 485–494.

    Google Scholar 

  • Hofmeister, W. 1862. On the germination, development, and fructification of the higher Cryptogamia, and on the fructification of the Coniferæ. Ray Society, London [F. Currey, translator].

    Google Scholar 

  • Holloway, J. E. 1915. Studies in the New Zealand species of the genus Lycopodium: Part I. Transactions and Proceedings of the New Zealand Institute 48: 253–303.

    Google Scholar 

  • Holloway, J. E. 1921. Further studies on the prothallus, embryo, and young sporophyte of Tmesipteris. Transactions and Proceedings of the New Zealand Institute 53: 386–44.

    Google Scholar 

  • Holloway, J. E. 1939. The gametophyte, embryo and young rhizome of Psilotum triquetrum Swartz. Annals of Botany 3: 313–336.

    Google Scholar 

  • Hopkins, A. W., & G. E. McBride. 1976. The life-history of Coleochaete scutata (Chlorophyceae) studied by a Feulgen microspectrophotometric analysis of the DNA cycle. Journal of Phycology 12: 29–35.

    Google Scholar 

  • Jaramillo, M. A., & E. M. Kramer. 2007. The role of developmental genetics in understanding homology and morphological evolution in plants. International Journal of Plant Science 168: 61–72.

    Article  CAS  Google Scholar 

  • Karol, K. G., R. M. McCourt, M. T. Cimino, & C. F. Delwiche. 2001. The closest living relatives of landplants. Science 294: 2351–2353.

    Article  PubMed  CAS  Google Scholar 

  • Kenrick, P. 1994. Alternation of generations in land plants: new phylogenetic and palaeobotanical evidence. Biological Reviews 69: 293–330.

    Article  Google Scholar 

  • Lang, W. H. 1909. A theory of alternation of generations in archegoniate plants based upon the ontogeny. New Phytologist 8: 1–12.

    Article  Google Scholar 

  • Lang, W. H. 1915. Phyletic and causal morphology. Report of the British Association for the Advancement of Science. Transactions of Section K. 701–721.

  • Lang, W. H., F. O. Bower, D. H. Scott, J. B. Farmer, F. W. Oliver, & A. G. Tansley. 1909. Discussion on “Alternation of generations” at the Linnean Society. New Phytologist 8: 104–108.

    Article  Google Scholar 

  • Moseley, M. F., & B. C. Zimmerly. 1949. Psilotum gametophytes matured under greenhouse conditions from self-sown spores. Science 110: 482.

    Article  PubMed  Google Scholar 

  • Oehlkers, F. 1916. Beitrag zur Kenntnis der Kernteilungen bei den Charazeen. Berichte der deutschen botanischen Gesellschaft 34: 223–227.

    Google Scholar 

  • Oltmanns, F. 1898. Die Entwickelung der Sexualorgane bei Coleochaete pulvinata. Flora 85: 1–14.

    Google Scholar 

  • Overton, C. E. 1893. On the reduction of the chromosomes in the nuclei of plants. Annals of Botany 7: 139–143.

    Google Scholar 

  • Pant, D. D., D. D. Nautiyal & D. R. Misra. 1984. Gametophytes of Ophioglossaceae. Phyta Monograph 1: 1–111. Society of Indian Plant Taxonomists, Allahabad.

    Google Scholar 

  • Pincher, H. C. 1937. A genetical interpretation of the alternation of generations. New Phytologist 36: 179–183.

    Article  Google Scholar 

  • Pringsheim, N. 1860. Beiträge zur Morphologie und Systematik der Algen. III. Die Coleochaeteen. Jahrbücher für wissenschaftliche Botanik 2: 1–38.

    Google Scholar 

  • Pringsheim, N. 1876a. Über Sprossung der Moosfrüchte. Monatsberichte der königlich preussischen Akademie der Wissenschaften zu Berlin 1876: 425–429. [‘second edition’ in Jahrbücher für wissenschaftliche Botanik 11: 1–6 (1878)].

  • Pringsheim, N. 1876b. Über den Generationswechsel der Thallophyten und seinen Anschluss an den Generationswechsel der Moose. Monatsberichte der königlich preussischen Akademie der Wissenschaften zu Berlin 1876: 869–911. [‘second edition’ in Jahrbücher für wissenschaftliche Botanik 11: 6–46 (1878)].

  • Pryer, K. M., E. Schuettpelz, P. G. Wolf, H. Schneider, A. R. Smith & R. Cranfill. 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91: 1582–1598.

    Article  CAS  Google Scholar 

  • Qiu, Y. -L., Y. Cho, J. C. Cox, & J. D. Palmer. 1998. The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394: 671–674.

    Article  PubMed  CAS  Google Scholar 

  • Remy, W. 1980. Der Generationswechsel der Archegoniaten Pflanzen im Übergangsfeld von aquatischer zu terrestrischer Lebensweise. Argumenta Palaeobotanica 6: 139–155.

    Google Scholar 

  • Remy, W. & H. Hass. 1991. Gametophyten und Sporophyten im Unterdevon—Fakten und Spekulationen. Argumenta Palaeobotanica 8: 193–223.

    Google Scholar 

  • Remy, W., P. G. Gensel, & H. Hass. 1993. The gametophyte generation of some early Devonian land plants. International Journal of Plant Sciences 154: 35–58.

    Article  Google Scholar 

  • Roe, K. E. 1975. Origin of the alternation of generations in plants: reconsideration of the traditional theories. Biologist 57: 1–13.

    Google Scholar 

  • Samigullin, T. K., S. P. Yacentyuk, G. V. Degtyaryeva, K. M. Valieho-Roman, V. K. Bobrova, I. Capesius, W. F. Martin, A. V. Troitsky, V. R. Filin, & A. S. Antonov. 2002. Paraphyly of bryophytes and close relationship of hornworts and vascular plants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences. Arctoa 11: 31–43.

    Google Scholar 

  • Scott, D. H. 1895. Nathanael Pringsheim. Nature 51: 399–402.

    Article  Google Scholar 

  • Scott, D. H. 1896. Present position of morphological botany. Nature 54: 535–543.

    Article  Google Scholar 

  • Scott, D. H. 1908. Alternation of generations in plants. Nature 79: 1–4.

    Article  Google Scholar 

  • Steenstrup, J. J. S. 1842a. Om Fortplantning og Udvikling gjennem vexlende Generationsrækker, en særegen Form for Opfostringen I de lavere Dyrklasser. Bianco Lunos, Copenhagen.

    Google Scholar 

  • Steenstrup, J. J. S. 1842b. Ueber den Generationswechsel, oder die Fortpflanzung und Entwickelung durch abwechselnde Generationen, eine eigenthümliche Form der Brutpflege in den niederen Thierclassen. Reitzel, Copenhagen [translated into German by C. H. Lorenzen].

    Google Scholar 

  • Steenstrup, J. J. S. 1845. On the alternation of generations; or, The propagation and development of animals through alternate generations: a peculiar form of fostering the young in the lower classes of animals. Ray Society, London [translated from the German version of C. H. Lorenzen by George Busk].

    Google Scholar 

  • Strasburger, E. 1894. The periodic reduction of the number of the chromosomes in the life-history of living organisms. Annals of Botany 8: 281–316.

    Google Scholar 

  • Strasburger, E. 1906. Typische und allotypische Kernteilung. Ergebnisse und Erörterungen. Jahrbücher für wissentschaftliche Botanik 42: 1–71.

    Google Scholar 

  • Tansley, A. G. 1907. Lectures on the evolution of the Filicinean vascular system. New Phytologist 6: 25–35.

    Article  Google Scholar 

  • Tansley, A. G. 1912. Meiosis and alternation of generations. New Phytologist 11: 213–216.

    Article  Google Scholar 

  • Taylor, T. N., H. Kerp, & H. Hass. 2005. Life history biology of early land plants: deciphering the gametophyte phase. Proceedings of the National Academy of Sciences, USA 102: 5892–5897.

    Article  CAS  Google Scholar 

  • Thompson, R. H. 1969. Sexual reproduction in Chaetosphaeridium globosum (Nordst.) Klebahn (Chlorophyceae) and description of a new species to science. Journal of Phycology 5: 285–290.

    Article  Google Scholar 

  • Turmel, M., M. Ehara, C. Otis, & C. Lemieux. 2002. Phylogenetic relationships among streptophytes as inferred from chloroplast small and large subunit rRNA gene sequences. Journal of Phycology 38: 364–375.

    Article  Google Scholar 

  • Treub, M. 1884. Études sur les Lycopodiacées. I. Le prothalle du Lycopodium cernuum L. Annales du Jardin Botanique de Buitenzorg 4: 107–138.

    Google Scholar 

  • Treub, M. 1886a. Études sur les Lycopodiacées. I. Le prothalle du Lycopodium Phlegmaria L. Annales du Jardin Botanique de Buitenzorg 5: 87–114.

    Google Scholar 

  • Treub, M. 1886b. Études sur les Lycopodiacées. II. Le développement de l’embryon chez L. Phlegmaria L. Annales du Jardin Botanique de Buitenzorg 5: 115–139.

    Google Scholar 

  • Turmel, M., C. Otis, & C. Lemieux. 2006. The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Molecular Biology and Evolution 23: 1324–1338.

    Article  PubMed  CAS  Google Scholar 

  • Vines, S. H. 1878. The “pro-embryo” of Chara: an essay in morphology. Journal of Botany (London) 16: 355–363.

    Google Scholar 

  • Wahl, H. A. 1945. Alternation of generations and classification with special reference to the teaching of elementary botany. Torreya 45: 1–32.

    Google Scholar 

  • Wahl, H. A. 1965. Alternation of generations—again. Turtox News 43: 206–209, 248–251.

  • Weismann, A. 1891. On heredity, 1883 (A. E. Shipley, translator). Pp. 67–106 in E. B. Poulton, S. Schönland, and A. E. Shipley [eds.], Essays upon heredity and kindred biological problems, Volume 1, 67–106. Clarendon Press, Oxford.

  • Williams, J. L. 1904. Studies in the Dictyotaceae. I. The cytology of the tetrasporangium and the germinating tetraspore. Annals of Botany 18: 141–160.

    Google Scholar 

Download references

Acknowledgments

The author thanks Richard Bondi, Jan Engelstädter, Lone Frank, Hans Hofmann, Judith Ryan and Richard Thomas for help with translations and the staffs of the Ernst Mayr and Harvard University Herbaria libraries for bibliographic assistance. The manuscript has benefited from the helpful comments of Richard Bondi, Chuck Davis, Jessica Girard, and Dennis Stevenson.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Haig.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haig, D. Homologous Versus Antithetic Alternation of Generations and the Origin of Sporophytes. Bot. Rev 74, 395–418 (2008). https://doi.org/10.1007/s12229-008-9012-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12229-008-9012-x

Keywords

Navigation