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.
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.
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).
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.
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