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Homospory 2002: an Odyssey of Progress in Pteridophyte Genetics And Articles Homospory 2002: An Odyssey of Progress in Pteridophyte Genetics and Evolutionary Biology Downloaded from CHRISTOPHER H. HAUFLER http://bioscience.oxfordjournals.org/ he homosporous vascular plants, including ferns and Tother graceful, primarily forest-dwelling groups such as FERNS AND OTHER HOMOSPOROUS the ground pines and horsetails, are the extant representatives of ancient lineages that once dominated the land surface. VASCULAR PLANTS HAVE HIGHLY POLY- Although the very well-studied seed plants find their closest PLOID CHROMOSOME NUMBERS, BUT relatives (sister group) among these species (Pryer et al. 2001), called homosporous pteridophytes, genetic aspects of ho- THEY EXPRESS TRAITS FOLLOWING mosporous plants have not been studied extensively. In ad- at University of Kansas Libraries on September 11, 2014 dition to the homosporous species, there are extant het- DIPLOID MODELS AND, ALTHOUGH erosporous pteridophytes—among them the water ferns (Marsileaceae), spike mosses (Selaginellaceae), and quill- CAPABLE OF EXTREME INBREEDING, ARE worts (Isoetaceae)—and extinct heterosporous lineages, PREDOMINANTLY OUTCROSSING which are well represented in the fossil record. But these “evolutionary experiments”in the heterosporous way of life, whose ancestors are homosporous, did not result in the ex- tems and evolutionary potential. All vascular plant life cycles traordinary burst of diversification seen among the seed feature an alternation of genetically different phases: sporo- plants, and they are not the focus of this review. However, there phytes, the diploid portion of the life cycle responsible for the are more than 10,000 homosporous pteridophyte species on production of spores, and gametophytes, the haploid gener- Earth today, and homospory appears to be the foundation on ation that yields gametes. The homosporous pteridophytes which all extant plant groups stand. Thus valuable insights for produce spores that are uniform in size, whereas heterosporous understanding the origin and biodiversity of groups such as species (including seed plants) produce spores of two differ- the flowering plants could be gained from a solid under- ent sizes, microspores and megaspores. This seemingly sim- standing of homosporous lineages. ple difference in spore size extends to the mode of sexual re- Unfortunately, developing and testing hypotheses about the production. Heterosporous species have unisexual genetics and evolution of homosporous pteridophytes has gametophytes—microspores produce exclusively male ga- been a difficult enterprise, because although homosporous metophytes and sperm, while megaspores germinate to ini- plants share many structural features with their much- tiate only female gametophytes and eggs. In contrast, all studied heterosporous siblings, the reproductive biology of spores of homosporous species can become bisexual game- these two groups is quite different. Nonetheless, the last quar- ter century has seen considerable change in our under- standing of pteridophyte evolution and genetics. This re- Christopher H. Haufler (e-mail: [email protected]) is a professor in the view will consider how new discoveries, insights, and Department of Ecology and Evolutionary Biology at the University of hypotheses have modified our perceptions of homosporous Kansas, Lawrence, KS 66045, and president of the American Fern Society. pteridophytes and assess the impact that these changes have He studies the evolution and phylogenetic history of ferns, focusing on the had on understanding basic aspects of plant genetics. narrow boundary between population genetics and macroevolutionary Homosporous pteridophytes possess biological attributes processes; he is especially fascinated by modes and mechanisms of speciation. that complicate a thorough understanding of their genetic sys- © 2002 American Institute of Biological Sciences. December 2002 / Vol. 52 No. 12 • BioScience 1081 Articles tophytes, bearing both eggs and sperm on the same individ- • Gene flow in homosporous species occurs through dis- ual. Such distinctive genetic architecture as well as aspects of persal of spores and sperm, which contrasts markedly life history and ecology can influence patterns and processes with seed and pollen dispersal. of evolution. Only by fully integrating all of these components • In thinking about the movement of genes between indi- can we obtain an accurate picture of the evolutionary potential viduals and populations, it is necessary to consider the of homosporous pteridophytes. The following elements of ho- high dispersal capacity of unicellular spores and to bal- ance this against the limitations imposed by the restrict- mosporous species pertain to genetic analyses: ed habitat requirements for growth and maturation of • Critical genetic processes (meiosis and fertilization) the gametophytes. occur on separate plants growing in different microhab- itats (figure 1). Gametophytes generally colonize moist, More than 20 years ago, Edward Klekowski (1979), who can open soil in often disturbed microsites, whereas sporo- validly be called the father of modern studies on pteridophyte phytes are typically found in well-established, mature genetics, published a summary and synthesis of the unique sites. features of homosporous pteridophytes. Klekowski, who had Downloaded from • Because a bisexual gametophyte is the product of a sin- been studying these plants for more than a dozen years, ar- gle meiotic event and produces genetically uniform eggs gued convincingly that the features of homosporous vascu- and sperm, biologists have predicted that homosporous lar plants required a modified set of rules to develop hy- pteridophytes are highly inbred and that these popula- potheses about their genetic composition and reproductive tions may have greatly reduced levels of genetic varia- biology. Since 1979, Klekowski’s controversial views have http://bioscience.oxfordjournals.org/ tion. provided the focus for numerous studies and have led to a new • All homosporous pteridophytes have high chromosome set of syntheses about homosporous pteridophyte genetics. numbers, and genetic analyses and assumptions about In the following sections, a picture of homosporous plant evolutionary potential that are regularly applied to oth- genetic systems will be developed by proceeding in an or- er organisms may not be appropriate. ganismal hierarchy: A description of the characteristics of in- dividuals and their genetic makeup provides the basis for a discussion of hypotheses about how these genomic characteristics evolved, which leads to an analysis of how these fea- at University of Kansas Libraries on September 11, 2014 tures influence breeding system interactions or potential interactions between individuals, which ultimately yields a synthesis of popu- lation-level features and evolutionary processes. In this hierarchy, the first question that must be asked is, “What constitutes an indi- vidual?”Because homosporous pteridophytes alternate between two strikingly different and fully independent generations, when one looks at a typical fern sporophyte growing in the woods, one sees only one of two compo- nents of the whole fern individual (figure 1). The sporophyte is the larger, generally peren- nial generation. The diminutive and generally ephemeral gametophytes are found in habi- tats that are usually quite dissimilar from those of the sporophyte. Both generations Figure 1. Homosporous pteridophytes alternate between two entirely indepen- and the processes they contain are critical dent generations. Bisexual gametophytes produce both egg-containing archego- for species survival, but from a genetic per- nia and sperm-producing antheridia. Fertilization occurs when the motile spective, the sporophyte could be considered sperm swim down the necks of the archegonia and unite with the egg, forming the less important generation. Although it is the diploid zygote. Not all gametophytes of homosporous species become bisex- true that meiosis takes place on the sporo- ual, and not all bisexual gametophytes are capable of self-fertilization. The phyte, fertilization occurs when sperms unite single-celled zygote divides mitotically and matures to form the sporophyte. with eggs on the gametophyte. Thus, the On the underside of sporophyte leaves are clusters of sporangia (sori). Meiosis products of the gametophyte actually deter- occurs in the sporangia, producing tetrads of spores that are released into the mine the genetic composition of the sporo- air. Under suitable conditions, the spores germinate and grow by mitotic cell phyte. Through meiosis, the sporophyte can divisions to form the gametophyte. only release recombinations of the compo- 1082 BioScience • December 2002 / Vol. 52 No. 12 Articles nent genomes that were amalgamated through fertilization What if most homosporous plants are polyploid? on the gametophyte. Klekowski (1973) advanced hypotheses that high ploidy lev- As noted above, homosporous species produce gameto- els actually may have been selected to maintain and release ge- phytes that are potentially bisexual, having both eggs and netic variability in homosporous plants. Klekowski reasoned sperms on a single, multicellular, haploid individual that that if bisexual gametophytes of homosporous plants fre- grew by mitosis and differentiation from a unicellular spore. quently fertilized themselves, lineages should rapidly become This condition actually imparts to homosporous species highly homozygous and lose the capacity to store and release greater breeding
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