Watanox Sahashi Outcrossing Rates

1 Some studies employed Gst• Ranges of Fst and Nm are shown only for studies that calculated population pairwise values.

2 For these species one or more pairwise values of Fst were 0, thus calculations of Nm were not possible; the reported mean and maximum extent of the range of Nm do not include information from those pairs of populations.

A mixed-mating system is one wherein neither outcrossing nor inbreeding predominates (e.g., see Lande and Schemske, 1985). Although rare compared to the relative frequencies of either predominantly outcrossing or predominantly inbreeding populations, Holsinger (1991) showed that mixed-mating could be evolutionarily stable when self-fertilization evolves under certain levels of population density. Documented examples of sexual, diploid ferns with mixed-mating systems include Dryopteris expansa (Soltis and Soltis, 1987a), Blechnum spicant (Soltis and Soltis, 1988a), Hemionitis palmata (Ranker, 1992a), Sadleria cyatheoides and S. pallida (Ranker et al., 1996), Sphenomeris chinensis (syn. Odontosoria chinensis; Ranker et al., 2000), Sticherus flabellatus (Keiper and McConchie, 2000), and Adi-antum capillus-veneris (Pryor et al., 2001). Ecologically, these mixed-mating species seem to share the attribute of having at least some populations or individuals that colonize disturbed places and others that grow in seemingly more stable microhabitats (see Ranker et al., 2000). Keiper and McConchie (2000) provided evidence from AFLP data (see Vos et al., 1995) that colonizing populations of Sticherus flabellatus are primarily inbreeding but also that larger, established populations occasionally exhibit outcrossing. Pryor et al. (2001) were the first to employ microsatellites in studying fern population genetics and they discovered evidence of a mixed-mating system in Adiantum capillus-veneris in Great Britain and Ireland.

Holsinger (1987) developed a statistical technique to estimate intragameto-phytic selfing (IGS) rates in homosporous plants based on estimates of genotype frequencies in populations. A number of studies have employed Holsinger's method, including species that essentially span the phylogenetic diversity of ferns and lycophytes (see Chapter 15): Blechnum spicant (Soltis and Soltis, 1988a); Huperzia miyoshiana, Lycopodium annotinum, and L. clavatum (Soltis and Soltis, 1988b); Blechnum spicant, Botrychium virginianum, Dryopteris expansa, Polystichum imbricans, and P. munitum (Soltis et al., 1988a); Equisetum arvense (Soltis et al., 1988b); Pteridium aquilinum (Wolf et al., 1988); Cheilanthes gracillima (Soltis et al., 1989); Gymnocarpium dryopteris ssp. disjunctum (Kirkpatrick et al., 1990); Hemionitis palmata (Ranker, 1992a); Botrychium (Sceptridium) multifidum var. robustum and B. (S.) ternatum (Watano and Sahashi, 1992); five species of Pleopeltis (Hooper and Haufler, 1997); Polystichum otomasui (Maki and Asada, 1998); and Sphenomeris chinensis (Ranker et al., 2000). Soltis and Soltis (1992) presented a summary of IGS estimates of 20 species, including some of those listed in other citations here. Overwhelmingly, these studies have supported the conclusions based on analyses of F-values that most populations of most species are primarily outcrossing and exhibit zero intragametophytic selfing. In the review of IGS rates of 20 species, Soltis and Soltis (1992) found a highly significant correlation between IGS rates and F-values, suggesting that intragametophytic selfing is the primary contributor to the fixation index in the taxa studied, rather than intergameto-phytic selfing.

There are several interesting exceptions to the generality of high outcrossing rates in ferns and these appear to relate to the colonization ability of a species (see below for discussion) or having subterranean gametophytes. All species of Ophioglossaceae are homosporous and have subterranean gametophytes. St. John (1949) and Tryon and Tryon (1982) suggested that the subterranean habit of Ophioglossaceae gametophytes might inhibit outcrossing, because of their potential isolation from other gametophytes. McCauley et al. (1985) employed enzyme electrophoresis to estimate selfing rates in three populations of Botrychium dissec-tum. Their estimate of the inbreeding coefficient, FIS (equivalent to the weighted mean of the fixation index (F) across populations), was 0.951; that is, 95% selfing and only 5% outcrossing. Similar high rates of inbreeding, intragametophytic selfing, and allelic fixation were estimated for Botrychium virginianum (Soltis and Soltis, 1986; Soltis et al., 1988a). Watano and Sahashi (1992) reported inbreeding in Botrychium (Sceptridium) multifidum var. robustum, B. (S.) nipponicum, B. (S.) ternatum, and B. (S.) triangularifolium. Similarly, Hauk and Haufler (1999) provided isozymic evidence that populations of Botrychium lanceolatum and B. simplex are primarily inbreeding. Thus, there is ample support for the hypothesis of St. John (1949) that having subterranean gametophytes facilitates intragameto-phytic selfing.

In one of the few population genetic studies of a heterosporous fern, Vitalis et al. (2002) provided evidence from microsatellites that the water fern Marsilea strigosa reproduces almost entirely via intergametophytic selfing.

4.3 Genetic structure of populations

Population genetic studies of ferns and lycophytes report that genetic variation is structured within and among populations in the same way that it is in other groups of organisms. The apparent primary determinants of genetic structure are various life-history and ecological characteristics such as mating system, population size, dispersal and colonization ability, habitat diversity, and recent demographic history.

Population divergence in ferns and lycophytes has been measured by Wright's standardized variance in allele frequencies, FST (Wright, 1965, 1978; Nei, 1977), and/or Nei's unbiased genetic identity, I (Nei, 1978). Because FST is usually calculated as a weighted average for all alleles at a locus, it is equivalent to GST, the gene diversity among populations (Nei, 1973, 1977; Wright, 1978; Swofford and Selander, 1989) and, thus, studies that employ either of these measures can be compared.

Population-level measures of FST and I for a variety of fern taxa are reported in Table 4.2. Mean population pairwise values were either taken directly from the literature cited or were calculated from the data provided. The grand mean of FST values for 19 taxa was 0.184 (range 0.07 to 0.70), which is intermediate to the mean GST values reported for populations of seed plants with wind dispersal (0.14) and those reported for seed plant taxa with seed dispersal other than wind (range 0.22 to 0.28). Thus, in spite of generally high levels of interpopulational genetic identities (grand mean I = 0.952), species of homosporous ferns can exhibit levels of population genetic structure comparable to that of many species of seed plants.

4.4 Gene flow and divergence

The exchange of genes between populations (so-called gene flow) is a powerful force in evolution. If levels of gene flow are sufficiently low between two populations, they can be expected to diverge genetically as a result of genetic drift, even in the absence of natural selection (Wright, 1931). Specifically, if a proportion m of a population of effective size N is replaced each generation by migrants from another population, the two populations may diverge genetically if Nm < 1.0. Values of Nm > 1.0 (or even 2Nm > 1.0) will tend to maintain genetic homogeneity between populations at selectively neutral loci. Specific predictions can be made about the probability of divergence of populations over time, given various levels of gene flow, when simplifying assumptions are made in theoretical models. Such models assume random mating and no mutation or natural selection (Wright, 1931, 1943, 1951; Slatkin, 1985a, 1985b). Slatkin and Barton (1989), however, demonstrated that even these assumptions could be relaxed. (Hey (2006) provides an insightful review of the literature, suggesting that speciation may occur in the face of gene flow in concert with the action of natural selection.)

Two methods have been commonly used in studies of ferns and lycophytes to estimate values of Nm between populations. One employs the approximate relationship between FST and Nm:

(Wright, 1931,1943,1951; Dobzhansky and Wright, 1941). Slatkin (1985b) devised a method to estimate Nm from the distribution and frequency of rare alleles. Both methods have been employed in the study of ferns, but Slatkin and Barton (1989) suggested that the FST method might actually be preferred over the private-allele method when based on enzyme electrophoretic data.

Table 4.2 summarizes estimates of interpopulational Nm for 24 species of ferns, most of which were estimated using the FST method and all of which used isozymes as genetic markers. The grand mean is 6.13, with a range across taxa of 0.05 to 155.7. Perhaps most notable is that most estimates are well above 1.0, which is consistent with the idea that ferns readily disperse via wind-blown spores.

Aside from dispersal and colonization ability, one of the primary determinants of effective gene flow between populations is mating system. Somewhat surprisingly, across the studies listed in Table 4.2, there is not a significant association between estimates of Nm and F (Spearman's rank correlation, rs = 0.0044, P = 0.49), suggesting that other factors besides mating behavior may have a significant impact on gene flow. The most obvious cases where there does seem to be a causal effect between mating and interpopulational gene flow are found in the inbreeding species Botrychium virginianum and in species that exhibit mixed mating behavior across different populations. In B. virginianum, mean F = 0.962, with some variable loci exhibiting F values of 1.000 (Soltis and Soltis, 1986). The predominance of intragametophytic selfing in this species with subterranean gametophytes could account for the extremely low estimate of gene flow between populations (Nm = 0.41; Soltis et al., 1988a). In mixed-mating Hemionitis palmata, estimates of Nm between pairs of populations ranged from effectively zero (0.02) to well over 1.0 (4.9), presumably because outcrossing populations incorporate genes from new migrants better than inbreeding populations (Ranker, 1992a).

Although some cases of repeated long-range dispersal and interpopulational gene flow in ferns have been hypothesized or documented (see below; Ranker et al., 1994), there is some evidence that gene flow is negatively proportional to distance between populations. Certainly this is what one would predict from the probable leptokurtic dispersal of spores away from the parental plant (e.g., Peck et al., 1990). For example, Ranker et al. (2000) examined isozyme variation in populations of Sphenomeris chinensis on all of the main high islands of the Hawaiian Islands. The mean Nm value between pairs of populations within islands was 13.1 (range 1.9-22.8), whereas the mean across islands of 6.9 (range 2.3-20.9) was significantly less (Mann-Whitney U-test, P = 0.000). Similar patterns of gene flow were observed within and across islands for four species of Hawaiian endemic grammitid ferns (Ranker, 1992b).

4.5 Population genetics of dispersal and colonization

Understanding the population genetics of dispersal and colonization has important implications for nearly every field of natural history, including biogeography, ecology, phylogeny, speciation theory, and epidemiology. Because of their presumably highly dispersible, wind-blown spores, ferns and lycophytes should generally have the capacity for long-distance dispersal. Not surprisingly, the extent to which species are effective dispersers depends on a wide range of life-history, adaptive, and genetic characteristics and their interplay with the biotic and physical environments. Clearly, some ferns and lycophytes are capable of dispersing long distances, as evidenced by the fact that they are common elements of the floras of isolated, oceanic islands and that they are often among the first colonizers of open and newly available habitat, especially in the tropics. For example, Schneider et al. (2005) explored the molecular phylogenetic relationships of the Hawaiian endemic clade Diellia (Aspleniaceae) to other members of the family. They estimated that the divergence time of the Diellia lineage from its closest relative coincided with the estimate of a renewal of Hawaiian terrestrial life at ca. 23 Myr ago (Clague, 1996; Price and Clague, 2002), following a 10 Myr lull in the production of new islands, such that essentially all pre-existing terrestrial life on older islands would have gone extinct due to island subsidence. Thus, this lineage of ferns was among the first to colonize the newly produced, mid-oceanic, isolated islands.

What are the genetic attributes of colonizing species of ferns and lycophytes and what are the genetic consequences of colonization? Several studies have shown that isolated, peripheral populations of some fern and lycophyte species, as well as populations of species that habitually colonize new habitats, are capable of intragametophytic selfing and, thus, harbor low levels of genetic load. Such taxa are consistent with ''Baker's Law," which loosely states that self-compatible species should be better colonizers than self-incompatible species (Baker, 1955, 1967; Stebbins, 1957). Among diploids these include Blechnum spicant (Cousens, 1979), Asplenium platyneuron (Crist and Farrar, 1983), Pteris multifida (Watano, 1988), Lygodium microphyllum and L. japonicum (Lott et al., 2003), and Dryopteris carthusiana (Flinn, 2006). Not all colonizing species, however, have this ability. For example, Ranker et al. (1996) discovered that only 0.5% to 5.0% of isolated gametophytes of the lava-flow colonizing species Sadleria cyatheoides were able to produce new sporophytes. They provided evidence from isozymes suggesting that, although this species may have some degree of inbreeding, it is primarily out-crossing. Because polyploids reproduce more successfully via intragametophytic selfing than most diploids, polyploid ferns may be more effective dispersers and colonizers (see Masuyama, 1979; Watano, 1988; Masuyama and Watano, 1990).

4.6 Summary and future prospects

In summary, population genetic studies across a wide range of taxa have revealed several common attributes shared by most species. Most populations and species of homosporous ferns and lycophytes are genetically diploid and are primarily outcrossing. Inbreeding is relatively rare and is primarily restricted to taxa with subterranean gametophytes, but interesting exceptions have been discovered among taxa with epigeal gametophytes. Inbreeding is also common in polyploids. In spite of apparently high levels of interpopulational gene flow, populations can exhibit significant genetic structure that may relate to ecological diversity, isolation-by-distance, history of colonization, mating system, population size, and other factors.

Although the field of population genetics within the context of the study of ferns and lycophytes has made significant progress over the last several decades, this area of inquiry is still in its infancy. Compared to the number of known species of ferns and lycophytes, and especially in light of their importance in tropical ecosystems, relatively few species have been studied. Thus, there is still a pressing need for population genetic studies to provide more substantial evidence concerning patterns and processes of evolution in these important groups of land plants.

Areas of population genetic research that have been little explored, if at all, in ferns and lycophytes include studies of the genetics of reproductive fitness with respect to ecological diversity, the relationship between ploidy, fitness, and genetics, and outbreeding depression (but see Schneller, 1996). Also, although numerous studies have applied DNA-based techniques to molecular systemat-ics, few have applied DNA markers to the study of population level questions. Genomic methods have yet to be applied at the population level to any taxa of ferns or lycophytes. The burgeoning field of ecological genomics holds great potential for understanding the interplay between genetic diversity within and among populations and such important evolutionary processes as adaptation and speciation. Knowledge of population genetic variation and the processes that generate and maintain genetic diversity are critical preludes for understanding the origin of species.


Andersson, I. (1923). The genetics of variegation in a fern. Journal of Genetics, 13, 1-11.

Andersson, I. (1927). Note on some characters in ferns subject to Mendelian inheritance. Hereditas, 9, 157-168.

Andersson-Kottö, I. (1929). A genetical investigation in Scolopendrium vulgare. Hereditas, 12, 109-178.

Andersson-Kottö, I. (1930). Variegation in three species of ferns. Zeitschrift fur induktive Abstammungs-und Vererbungs Lehre, 56, 115-201.

Andersson-Kottö, I. (1931). The genetics of ferns. Bibliographica Genetica, 8, 269-294.

Aragón, C. E. and Pangua, E. (2003). Gender determination and mating system in the autotetraploid fern Asplenium septentrionale (L.) Hoffm. Botanica Helvetica, 113, 181-193.

Atkinson, L. R. and Stokey, A. G. (1964). Comparative morphology of the gametophyte of homosporous ferns. Phytomorphology, 14, 51-70.

Baker, H. G. (1955). Self-compatibility and establishment after 'long-distance' dispersal. Evolution, 3, 347-349.

Baker, H. G. (1967). Support for Baker's Law - as a rule. Evolution, 4, 853-856.

Chiou, W.-L., Farrar, D. R., and Ranker, T. A. (1998). Gametophyte morphology and reproductive biology in Elaphoglossum Schott. Canadian Journal of Botany, 76, 1967-1977.

Chiou, W.-L., Farrar, D. R., and Ranker, T. A. (2002). The mating systems of some Polypodiaceae species. American Fern Journal, 92, 65-79.

Clague, D. A. (1996). The growth and subsidence of the Hawaiian-Emperor volcanic chain. In The Origin and Evolution of Pacific Island Biotas, New Guinea to Eastern Polynesia: Patterns and Processes, ed. A. Keast and S. E. Miller. Amsterdam: SPB Academic Publishing, pp. 35-50.

Cousens, M. I. (1979). Gametophyte ontogeny, sex expression, and genetic load as measures of population divergence in Blechnum spicant. American Journal of Botany, 66, 116-132.

Cousens, M. I., Lacey, D. G., and Kelly, E. M. (1985). Life history studies of ferns: a consideration of perspective. Proceedings of the Royal Society of Edinburgh, 86B, 371-380.

Crist, K. C. and Farrar, D. R. (1983). Genetic load and long distance dispersal in Asplenium platyneuron. Canadian Journal of Botany, 61, 1809-1814.

Crow J. and Kimura M. (1965). Evolution in sexual and asexual populations. The American Naturalist, 99, 439-450.

Dobzhansky, T. (1970). Genetics of the Evolutionary Process. New York: Columbia University Press.

Dobzhansky, T. and Wright, S. (1941). Genetics of natural populations. V. Relations between mutation rate and accumulation of lethals in populations of Drosophila pseudoobscura. Genetics, 26, 23-51.

Eastwood, A., Cronk, Q.C. B., Vogel, J. C., Hemp, A., and Gibby, M. (2004).

Comparison of molecular and morphological data on St Helena: Elaphoglossum. Plant Systematics and Evolution, 245, 93-106.

Flinn, K. M. (2006). Reproductive biology of three fern species may contribute to differential colonization success in post-agricultural forests. American Journal of Botany, 93, 1289-1294.

Gastony, G. J. and Gottlieb, L. D. (1982). Evidence for genetic heterozygosity in a homosporous fern. American Journal of Botany, 69, 634-637.

Gastony, G. J. and Gottlieb, L. D. (1985). Genetic variation in the homosporous fern Pellaea andromedifolia. American Journal of Botany, 72, 257-267.

Gitzendanner, M. A. and Soltis, P. S. (2000). Patterns of genetic variation in rare and widespread plant congeners. American Journal of Botany, 87, 783-792.

Greer, G. K. (1993). The influence of soil topography and spore-rain density on gender expression in gametophyte populations of the homosporous fern Aspidotis densa. American Fern Journal, 83, 54-59.

Hamrick, J. L. and Godt, M. J. W. (1990). Allozyme diversity in plant species. In Plant Population Genetics, Breeding, and Genetic Resources, ed. A. H. D. Brown, M. T. Clegg, A. L. Kahler, and B. S. Weir. Sunderland, MA: Sinauer, pp. 43-63.

Haufler, C. H. (1985). Enzyme variability and modes of evolution in the fern genus Bommeria. Systematic Botany, 10, 92-104.

Haufler, C. H. (1987). Electrophoresis is modifying our concepts of evolution in homosporous Pteridophytes. American Journal of Botany, 74, 953-966.

Haufler, C. H. (1992). An introduction to fern genetics and breeding systems. In Fern Horticulture: Past, Present and Future Perspectives, ed. J. M. Ide, C. Jermy, and A. M. Paul. Andover: Intercept, pp. 145-155.

Haufler, C. H. (2002). Homospory 2002: an odyssey of progress in pteridophyte genetics and evolutionary biology. Bioscience, 52, 1081-1093.

Haufler, C. H. and Soltis, D. E. (1984). Obligate outcrossing in a homosporous fern: field confirmation of a laboratory prediction. American Journal of Botany, 71, 878-881.

Haufler, C. H. and Soltis, D. E. (1986). Genetic evidence suggests that homosporous ferns with high chromosome numbers are diploid. Proceedings of the National Academy of Sciences of the United States of America, 83, 4389-4393.

Haufler, C. H., Windham, M. D., and Ranker, T. A. (1990). Biosystematic analysis of the Cystopteris tennesseensis (Dryopteridaceae) complex. Annals of the Missouri Botanical Garden, 77, 314-329.

Hauk, W. D. and Haufler, C. H. (1999). Isozyme variability among cryptic species of Botrychium subgenus Botrychium (Ophioglossaceae). American Journal of Botany, 86, 614-633.

Hedrick, P. W. (1987). Population genetics of intragametophytic selfing. Evolution, 41, 137-144.

Hey, J. (2006). Recent advances in assessing gene flow between diverging populations and species. Current Opinion in Genetics and Development, 16, 592-596.

Hickok, L. G. (1978a). Homoeologous chromosome pairing: frequency differences in inbred and intraspecific hybrid polyploid ferns. Science, 202, 982-984.

Hickok, L. G. (1978b). Homoeologous chromosome pairing and restricted segregation in the fern Ceratopteris. American Journal of Botany, 65, 516-521.

Holderegger, R. and Schneller, J. J. (1994). Are small isolated populations of Asplenium septentrionale variable? Biological Journal of the Linnean Society, 51, 377-385.

Holsinger, K. E. (1987). Gametophytic self-fertilization in homosporous plants -

development, evaluation, and application of a statistical-method for evaluating its importance. American Journal of Botany, 74, 1173-1183.

Holsinger, K. E. (1990). The population genetics of mating system evolution in homosporous plants. American Fern Journal, 80, 153-160.

Holsinger, K. E. (1991). Mass-action models of plant mating systems: the evolutionary stability of mixed mating systems. The American Naturalist, 138, 606-622.

Hooper, E. A. and Haufler, C. H. (1997). Genetic diversity and breeding system in a group of neotropical epiphytic ferns (Pleopeltis; Polypodiaceae). American Journal of Botany, 84, 1664-1674.

Ishikawa, H., Motomi, I., Watano, Y., and Kurita, S. (2003). Electrophoretic evidence for homoeologous chromosome pairing in the apogamous fern species Dryopteris nipponensis (Dryopteridaceae). Journal of Plant Research, 116, 165-167.

Kang, M., Ye, Q., and Huang, H. (2005). Genetic consequence of restricted habitat and population decline in endangered Isoetes sinensis (Isoetaceae). Annals of Botany, 96, 1265-1274.

Keiper, F. J. and McConchie, R. (2000). An analysis of genetic variation in natural populations of Sticherus flabellatus [R. Br. (St John)] using amplified fragment length polymorphism (AFLP) markers. Molecular Ecology, 9, 571-581.

Kirkpatrick, R. E. B., Soltis, P. S., and Soltis, D. E. (1990). Mating system and distribution of genetic variation in Gymnocarpium dryopteris ssp. disjunctum. American Journal of Botany, 77, 1101-1110.

Klekowski, E. J., Jr. (1969). Reproductive biology of the Pteridophyta. II. Theoretical considerations. Botanical Journal of the Linnean Society, 62, 347-359.

Klekowski, E. J., Jr. (1970a). Populational and genetic studies of a homosporous fern - Osmunda regalis. American Journal of Botany, 57, 1122-1138.

Klekowski, E. J., Jr. (1970b). Reproductive biology of the Pteridophyta. IV. An experimental study of mating systems in Ceratopteris thalictroides (L.) Brongn. Journal of the Linnean Society, Botany, 63, 153-169.

Klekowski, E. J., Jr. (1971). Ferns and genetics. Bioscience, 21, 317-322.

Klekowski, E. J., Jr. (1972a). Genetical features of ferns as contrasted to seed plants. Annals of the Missouri Botanical Garden, 59, 138-151.

Klekowski, E. J., Jr. (1972b). Evidence against genetic self-incompatibility in the homosporous fern Pteridium aquilinum. Evolution, 26, 66-73.

Klekowski, E. J. Jr. (1973). Genetic load in Osmunda regalis populations. American Journal of Botany, 60, 146-154.

Klekowski, E. J., Jr. (1979). The genetics and reproductive biology of ferns. In The

Experimental Biology of Ferns, ed. A. F. Dyer. London: Academic Press, pp. 133-170.

Klekowski, E. J., Jr. (1988). Mutation, Developmental Selection, and Plant Evolution. New York: Columbia University Press.

Klekowski, E. J., Jr. and Baker, H. G. (1966). Evolutionary significance of polyploidy in the Pteridophyta. Science, 153, 305-307.

Lande, R. and Schemske, D. W. (1985). The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution, 39, 24-40.

Lang, W. H. (1923). On the genetic analysis of a heterozygotic plant of Scolopendrium vulgare. Journal of Genetics, 13, 167-175.

Leimu, R., Mutikainen, P., Koricheva, J., and Fischer, M. (2006). How general are positive relationships between plant population size, fitness and genetic variation? Journal of Ecology, 94, 942-952.

Li, J. and Haufler, C. H. (1994). Phylogeny, biogeography, and population biology of Osmunda species: insights from isozymes. American Fern Journal, 85, 105-114.

Li, J. W. and Haufler, C. H. (1999). Genetic variation, breeding systems, and patterns of diversification in Hawaiian Polypodium (Polypodiaceae). Systematic Botany, 24, 339-355.

Lloyd, R. M. (1974). Mating systems and genetic load in pioneer and non-pioneer Hawaiian Pteridophyta. Botanical Journal of the Linnean Society, 69, 23-35.

Lloyd, R. M. and Warne, T. R. (1978). The absence of genetic load in a morphologically variable sexual species, Ceratopteris thalictroides (Parkeriaceae). Systematic Botany, 3, 20-36.

Lott, M. S., Volin, J. C., Pemberton, R. W., and Austin, D. F. (2003). The reproductive biology of the invasive ferns Lygodium microphyllum and L. japonicum (Schizaeaceae): implications for invasive potential. American Journal of Botany, 90, 1144-1152.

Maki, M. and Asada, Y.-J. (1998). High genetic variability revealed by allozymic loci in the narrow endemic fern Polystichum otomasui (Dryopteridaceae). Heredity, 80, 604-610.

Masuyama, S. (1979). Reproductive biology of the fern Phegopteris decursive-pinnata. I. The dissimilar mating systems of diploids and tetraploids. Botanical Magazine (Tokyo), 92, 275-289.

Masuyama, S. and Watano, Y. (1990). Trends for inbreeding in polyploid pteridophytes. Plant Species Biology, 5, 13-17.

Masuyama, S., Mitui, K., and Nakato, N. (1987). Studies on intraspecific polyploids of the fern Lepisorus thunbergianus. (3) Mating system and the ploidy. Journal of Japanese Botany, 62, 321-331.

McCauley, D. E., Whittier, D. P., and Reilly, L. M. (1985). Inbreeding and the rate of self-fertilization in a grape fern, Botrychium dissectum. American Journal of Botany, 72, 1978-1981.

Muller, H. J. (1950). Our load of mutations. The American Journal of Human Genetics, 2, 111-176.

Nei, M. (1973). Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America, 70, 3321-3323.

Nei, M. (1977). F-statistics and analysis of gene diversity in subdivided populations. Annals of Human Genetics, 41, 225-233.

Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583-590.

Otto, S. P. and Marks, J. C. (1996). Mating systems and the evolutionary transition between haploidy and diploidy. Biological Journal of the Linnean Society, 57, 197-218.

Pangua, E. and Vega, B. (1996). Comparative study of gametophyte development in Cosentinia and Anogramma (Hemionitidaceae) and Cheilanthes (Sinopteridaceae). In Pteridology in Perspective, ed. J. M. Camus, M. Gibby, and R. J. John. Kew: Royal Botanic Gardens, pp. 497-508.

Peck, J. H., Peck, C. J., and Farrar, D. R. (1990). Comparative life history studies and the distribution of pteridophyte populations. American Fern Journal, 80, 126-142.

Pérez-García, B. and Riba, R. (1998). Bibliografía sobre Gametofitos de Helechos y Plantas Afines. Monographs in Systematic Botany from the Missouri Botanical Garden, Vol. 70, ed. V. C. Hollowell. St. Louis, MO: Missouri Botanical Garden Press.

Price, J. P. and Clague, D. A. (2002). How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence. Proceedings of the Royal Society of London Series B, Biological Sciences, 269, 2429-2435.

Pryor, K. V., Young, J. E., Rumsey, F. J., Edwards, K. J., Bruford, M. W., and Rogers, H. J. (2001). Diversity, genetic structure and evidence of outcrossing in British populations of the rock fern Adiantum capillus-veneris using microsatellites. Molecular Ecology, 10, 1881-1894.

Quintanilla, L. G., Pangua, E., Amigo, J., and Pajaron. S. (2005). Comparative study of the sympatric ferns Culcita macrocarpa and Woodwardia radicans: sexual phenotype. Flora, 200, 187-194.

Rabinowitz, D. (1981). Seven forms of rarity. In The Biological Aspects of Rare Plant Conservation, ed. H. Synge. Chichester: Wiley, pp. 205-217.

Ranker, T. A. (1987). Experimental systematics and population biology of the fern genera Hemionitis and Gymnopteris with reference to Bommeria. Unpublished Ph.D. Thesis, University of Kansas, Lawrence, KS.

Ranker, T. A. (1992a). Genetic diversity, mating systems, and interpopulation gene flow in neotropical Hemionitis palmata L. (Adiantaceae). Heredity, 69, 175-183.

Ranker, T. A. (1992b). Genetic diversity of endemic Hawaiian epiphytic ferns: implications for conservation. Selbyana, 13, 131-137.

Ranker, T. A. (1994). Evolution of high genetic variability in the rare Hawaiian fern Adenophorus periens and implications for conservation management. Biological Conservation, 70, 19-24.

Ranker, T. A. and Houston, H. A. (2002). Is gametophyte sexuality in the lab a good predictor of sexuality in nature? Sadleria as a case study. American Fern Journal, 92, 112-118.

Ranker, T. A., Floyd, S. K., and Trapp, P. G. (1994). Multiple colonizations of Asplenium adiantum-nigrum onto the Hawaiian Archipelago. Evolution, 48, 1364-1370.

Ranker, T. A., Gemmill, C. E. C., Trapp, P. G., Hambleton, A., and Ha, K. (1996).

Population genetics and reproductive biology of lava-flow colonising species of Hawaiian Sadleria (Blechnaceae). In Pteridology in Perspective, ed. J. M. Camus, M. Gibby, and R. J. John. Kew: Royal Botanic Gardens, pp. 581-598.

Ranker, T. A., Gemmill, C. E. C., and Trapp, P. G. (2000). Microevolutionary patterns and processes of the native Hawaiian colonizing fern Odontosoria chinensis (Lindsaeaceae). Evolution, 54, 828-839.

St. John, E. P. (1949). The evolution of the Ophioglossaceae of the eastern United States. Quarterly Journal of the Florida Academy of Sciences, 12, 207-219.

Schneider, H., Ranker, T. A., Russell, S. J., Cranfill, R., Geiger, J. M. O., Aguraiuja, R., Wood, K. R., Grundmann, M., Kloberdanz, K., and Vogel, J. C. (2005). Origin and diversification of the Hawaiian fern genus Diellia Brack. (Aspleniaceae, Polypodiidae). Proceedings of the Royal Society of London Series B, Biological Sciences, 272, 455-460.

Schneller, J. J. (1979). Biosystematic investigations on the Lady Fern (Athyrium filix-femina). Plant Systematics and Evolution, 132, 255-277.

Schneller, J. J. (1996). Outbreeding depression in the fern Asplenium ruta-muraria L: evidence from enzyme electrophoresis, meiotic irregularities and reduced spore viability. Biological Journal of the Linnean Society, 59, 281-295.

Schneller, J. J. and Holderegger, R. (1996). Genetic variation in small, isolated fern populations. Journal of Vegetation Science, 7, 113-120.

Sciarretta, K. L., Potter Arbuckle, E., Haufler, C. H., and Werth, C. R. (2005). Patterns of genetic variation in southern Appalachian populations of Athyrium filix-femina var. asplenioides (Dryopteridaceae). International Journal of Plant Science, 166, 761-780.

Slatkin, M. (1985a). Gene flow in natural populations. Annual Review of Ecology and Systematics, 16, 393-430.

Slatkin, M. (1985b). Rare alleles as indicators of gene flow. Evolution, 39, 53-65.

Slatkin, M. and Barton, N. H. (1989). A comparison of three indirect methods for estimating average levels of gene flow. Evolution, 43, 1349-1368.

Soltis, D. E., and Soltis, P. S. (1986). Electrophoretic evidence for inbreeding in the fern Botrychium virginianum (Ophioglossaceae). American Journal of Botany, 73, 588-592.

Soltis, D. E., and Soltis, P. S. (1987a). Breeding system of the fern Dryopteris expansa: evidence for mixed-mating. American Journal of Botany, 74, 504-509.

Soltis, D. E., and Soltis, P. S. (1987b). Polyploidy and breeding systems in homosporous Pteridophyta: a reevaluation. The American Naturalist, 130, 219-232.

Soltis, P. S., and Soltis, D. E. (1987c). Population structure and estimates of gene flow in the homosporous fern Polystichum munitum. Evolution, 41, 620-629.

Soltis, P. S. and Soltis, D. E. (1988a). Genetic variation and population structure in the fern Blechnum spicant (Blechnaceae) from western North America. American Journal of Botany, 75, 37-44.

Soltis, P. S. and Soltis, D. E. (1988b). Estimated rates of intragametophytic selfing in lycopods. American Journal of Botany, 75, 248-256.

Soltis, P. S. and Soltis, D. E. (1990a). Genetic variation within and among populations of ferns. American Fern Journal, 80, 161-172.

Soltis, P. S. and Soltis, D. E. (1990b). Evolution of inbreeding and outcrossing in ferns and fern-allies. Plant Species Biology, 5, 1-11.

Soltis, D. E., and Soltis, P. S. (1992). The distribution of selfing rates in homosporous ferns. American Journal of Botany, 79, 97-100.

Soltis, P. S., Soltis D. E., and Holsinger, K. E. (1988a). Estimates of intragametophytic selfing and interpopulational gene flow in homosporous ferns. American Journal of Botany, 75, 1765-1770.

Soltis, P. S., Soltis, D. E., and Noyes, R. D. (1988b). An electrophoretic investigation of intragametophytic selfing in Equisetum arvense. American Journal of Botany, 75, 231-237.

Soltis, P. S., Soltis, D. E., and Ness, B. D. (1989). Population genetic-structure in Cheilanthes gracillima. American Journal of Botany, 76, 1114-1118.

Soltis, P. S., Soltis, D. E., and P. G. Wolf. (1990). Allozymic divergence and species relationships in North American Polystichum (Dryopteridaceae). Systematic Botany,

Stebbins, G. L. (1957). Self fertilization and population variability in the higher plants. The American Naturalist, 91, 337-354.

Stokey, A. G. and Atkinson, L. R. (1958). The gametophyte of the Grammitidaceae. Phytomorphology, 8, 391-403.

Su, Y., Wang, T., Zheng, B., Jiang, Y., Chen, G., and Gu, H. (2004). Population genetic structure and phylogeographical pattern of a relict tree fern, Alsophila spinulosa (Cyatheaceae), inferred from cpDNA atpB-rbcL intergenic spacers. Theoretical and Applied Genetics, 109, 1459-1467.

Suter, M., Schneller, J. J., and Vogel, J. C. (2000). Investigations into the genetic variation, population structure, and breeding systems of the fern Asplenium trichomanes subsp. quadrivalens. International Journal of Plant Science, 161, 233-244.

Swofford, D. L. and Selander, R. B. (1989). BIOSYS-1. A computer program for the analysis of allelic variation in population genetics and biochemical systematics, Release 1.7. Urbana, IL: Illinois Natural History Survey.

Tryon, R. M. and Tryon, A. F. (1982). Ferns and Allied Plants. New York: Springer-Verlag.

Vitalis, R., Riba, M., Colas, B., Grillas, P., and Olivieri, I. (2002). Multilocus genetic structure at contrasted spatial scales of the endangered water fern Marsilea strigosa Willd. (Marsileaceae, Pteridophyta). American Journal of Botany, 89, 1142-1155.

Vogel, J. C., Rumsey, F. J., Russell, S. J., Cox, C. J., Holmes, J. S., Bujnoch, W., Starks, C., Barrett, J. A., and Gibby, M. (1999). Genetic structure, reproductive biology and ecology of isolated populations of Asplenium csikii (Aspleniaceae, Pteridophyta). Heredity, 83, 604-612.

Vos, P., Hogers, R., Bleeker, M., Reijans, M., Vandelee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M., and Zabeau, M. (1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research, 23, 4407-4414.

Wallace, B. (1970). Genetic Load - Its Biological and Conceptual Aspects. Englewood Cliffs, NJ: Prentice-Hall.

Watano, Y. (1988). High levels of genetic divergence among populations in a weedy fern, Pteris multifida Poir. Plant Species Biology, 3, 109-115.

Watano, Y., and Masuyama, S. (1991). Inbreeding in natural populations of the annual polyploid fern Ceratopteris thalictroides (Parkeriaceae). Systematic Botany,

Watano, Y., and Sahashi, N. (1992). Predominant inbreeding and its genetic consequences in a homosporous fern genus, Sceptridium (Ophioglossaceae). Systematic Botany, 17, 486-502.

Werth, C. R. and Cousens, M. I. (1990). Summary: the contributions of population studies on ferns. American Fern Journal, 80, 183-190.

Werth, C. R., Guttman, S. I., and Eshbaugh, W. H. (1985). Electrophoretic evidence of reticulate evolution in the Appalachian Asplenium complex. Systematic Botany, 10, 184-192.

Wolf, P. G., Haufler, C. H., and Sheffield, E. (1988). Electrophoretic variation and mating system of the clonal weed Pteridium aquilinum (L.) Kuhn (Bracken). Evolution, 42, 1350-1355.

Wolf, P. G., Sheffield, E., and Haufler, C. H. (1990). Genetic attributes of bracken as revealed by enzyme electrophoresis. In Bracken Biology and Management, ed. J. A. Thomson and R. T. Smith. Hawthorn, Victoria: Australian Institute of Agriculture and Science, Occasional Paper Number 40, pp. 71-78.

Wolf, P. G., Sheffield, E., and Haufler, C. H. (1991). Estimates of gene flow, genetic substructure and population heterogeneity in bracken (Pteridium aquilinum). Biological Journal of the Linnean Society, 42, 407-423.

Wright, S. (1931). Evolution in Mendelian populations. Genetics, 16, 97-159.

Wright, S. (1943). Isolation by distance. Genetics, 28, 114-138.

Wright, S. (1951). The genetical structure of populations. Annals of Eugenics, 15, 323-354.

Wright, S. (1965). The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution, 19, 395-420.

Wright, S. (1969). Evolution and the Genetics of Populations, Vol. 2, The Theory of Gene Frequencies. Chicago, IL: University of Chicago Press.

Wright, S. (1978). Evolution and the genetics of populations, Vol. 4, Variability within and among natural populations. Chicago, IL: University of Chicago Press.

Was this article helpful?

0 0
10 Ways To Fight Off Cancer

10 Ways To Fight Off Cancer

Learning About 10 Ways Fight Off Cancer Can Have Amazing Benefits For Your Life The Best Tips On How To Keep This Killer At Bay Discovering that you or a loved one has cancer can be utterly terrifying. All the same, once you comprehend the causes of cancer and learn how to reverse those causes, you or your loved one may have more than a fighting chance of beating out cancer.

Get My Free Ebook

Post a comment