Polyploidy, Breeding Systems, and Genetic Differentiation in Homosporous Pteridophytes

Abstract

241 The common name "pteridophyte" has been applied to plants composing four divisions (Bold et aI., 1986): Psilotophyta, Microphyllophyta, Arthrophyta, and Pteridophyta. Most pteridophytes are homosporous, producing one type of spore that germinates to produce a potentially bisexual gametophyte. The homosporous pteridophytes are the whisk ferns, Psilotum and Tmesipteris (Psilotophyta); the lycopods, Lycopodium sensu lato and Phyllo-glossum (class Aglossopsida of the Microphyllophyta); the horsetails and scouring rushes, Equisetum (Arthrophyta); and most families of ferns (Pteridophyta). These are ancient lineages, some of which are regarded as living fossils (Bold et aI., 1986). The lycopods, for example, can be traced back in the fossil record to the lower Devonian. Homosporous pteridophytes are unique among vascular plants in possessing free-living gametophytes that are potentially bisexual. The unusual nature of the life cycle in these plants compared to all heterosporous plants, including seed plants, has important evolutionary implications, including: (1) the two free-living organisms, gametophyte and sporophyte, may often have distinct ecological requirements; (2) both the gametophyte and sporophyte experience separate selective forces; and (3) selfing oli a bisexual gametophyte produces a completely homozygous sporophyte in a single generation. These plants are also unusual in possessing the highest chromosome numbers known for any organisms. Whereas the average gametic chromosome number for angiosperms is n = 15.99, the mean for all homosporous pteridophYtes is n = 55.27 (Klekowski and Baker, 1966). The average haploid number for homosporous ferns (pteridophyta) is 57.05 (Klekowski and Baker, 1966). Using chromosome numbers reported by Love et al. (1977) we have determined that the average chromosome number for lycopods (Aglossopsida, Microphyllophyta) is approximately n = 86. Chromosome numbers for Psilotophyta range from n = 52 to 208 in Psilotum and n = 104 to 208 in Tmesipteris (Love et aI., 1977). All species of Equisetum (Arthrophyta) for which chromosome counts are available have n = 108. For the past two I'decades, the prevalent view of homosporolls pteridophyte biology has been that these plants are fundamentally different from all other vascular plants in both levels of polyploidy and type of breeding system. Klek'owski and Baker (1966) argued that the high chromosome numbers characteristic of homosp())rous pteridophytes reflected very high levels of polyploidy. For example, original base chromosome numbers of x = 9 and 12 have been proposed for Equisetum (Love et aI., 1977; ~ida, 1976), suggesting that extant species are 24-or 18-ploid, respectively. Klekowski and Baker (1966) suggested that high levels of polyploidy were essential for maintaining genetic variation in all lineages of homosporous pteridophytes. The genetic variation stored through polyploidy could then be released as a result of pairing of chromosomes from these additional genomes (homoeologous pairing). Such a genetic mechanism was deemed critical because genetic variation would otherwise be eliminated by the presumed habitual self-fertilization of the bisexual gametophytes of these plants. 241 The common name "pteridophyte" has been applied to plants composing four divisions (Bold et aI., 1986): Psilotophyta, Microphyllophyta, Arthrophyta, and Pteridophyta. Most pteridophytes are homosporous, producing one type of spore that germinates to produce a potentially bisexual gametophyte. The homosporous pteridophytes are the whisk ferns, Psilotum and Tmesipteris (Psilotophyta); the lycopods, Lycopodium sensu lato and Phyllo-glossum (class Aglossopsida of the Microphyllophyta); the horsetails and scouring rushes, Equisetum (Arthrophytaj; and most families of ferns (Pteridophyta). These are ancient lineages, some of which are regarded as living fossils (Bold et aI., 1986). The lycopods, for example, can be traced back in the fossil record to the lower Devonian. Homosporous pteridophytes are unique among vascular plants in possessing free-living gametophytes that are potentially bisexual. The unusual nature of the life cycle in these plants compared to all heterosporous plants, including seed plants, has important evolutionary implications, including: (1) the two free-living organisms, gametophyte and sporophyte, may often have distinct ecological requirements; (2) both the gametophyte and sporophyte experience separate selective forces; and (3) selfing of a bisexual gametophyte produces a completely homozygous sporophyte in a single generation. These plants are also unusual in possessing the highest chromosome numbers known for any organisms. Whereas the average gametic chromosome number for angiosperms is n = 15.99, the mean for all homosporous pteridophytes is n = 55.27 (Klekowski and Baker, 1966). The average haploid number for homosporous ferns (Pteridophyta) is 57.05 (Klekowski and Baker, 1966). Using chromosome numbers reported by Love et al. (1977) we have determined that the average chromosome number for lycopods (Aglossopsida, Microphyllophyta) is approximately n = 86. Chromosome numbers for Psilotophyta range from n = 52 to 208 in Psilotum and n = 104 to 208 in Tmesipteris (Love et aI., 1977). All species of Equisetum (Arthrophyta) for which chromosome counts are available have n = 108. For the past two I'decades, the prevalent view of homosporous pteridophyte biology has been that these plants are fundamentally different from all other vascular plants in both levels of polyploidy and type of breeding system. Klekowski and Baker (1966) argued that the high chromosome numbers characteristic of homosporous pteridophytes reflected very high levels of polyploidy. For example, original base chromosome numbers of x = 9 and 12 have been proposed for Equisetum (Love et aI., 1977; Vida, 1976), suggesting that extant species are 24-or 18-ploid, respectively. Klekowski and Baker (1966) suggested that high levels of polyploidy were essential for maintaining genetic variation in all lineages of homosporous pteridophytes. The genetic variation stored through polyploidy could then be released as a result of pairing of chromosomes from these additional genomes (homoeologous pairing). Such a genetic mechanism was deemed critical because genetic variation would otherwise be eliminated by the presumed habitual self-fertilization of the bisexual gametophytes of these plants.