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Reproductive Biology |
Cornell University, Department of Ecology and Evolutionary Biology, Corson Hall, Ithaca, New York 14853 USA
Received for publication February 8, 2006. Accepted for publication May 26, 2006.
ABSTRACT
Because selfing enables a single individual to reproduce in a new location, the ability to self-fertilize should enhance plants' capacity for colonization. This study examined whether selfing ability correlated with successful migration in three fern species, Dryopteris carthusiana, Dryopteris intermedia, and Polystichum acrostichoides, which vary in their ability to colonize forests on abandoned agricultural lands in central New York, USA. Polystichum acrostichoides is much more frequent in forests that were never cleared for agriculture, D. carthusiana is more frequent in forests that developed on former fields, and D. intermedia is equally frequent in the two forest types. To test the hypothesis that better-colonizing species and post-agricultural forest populations have greater selfing ability, I assessed the sporophyte production of gametophytes grown in isolation and in pairs of varying relatedness. Dryopteris carthusiana had the highest reproductive success and selfing ability and P. acrostichoides the lowest. These results support the hypothesis that selfing may facilitate colonization in these species. They also exemplify the general pattern that polyploid fern species have higher rates of self-fertilization than related diploids, as the allotetraploid D. carthusiana had greater selfing ability than both diploid species.
Key Words: Baker's Law • Dryopteridaceae • genetic load • inbreeding depression • land-use history • New York • polyploidy • self-fertilization
Understanding how life history traits relate to colonizing ability can reveal the processes underlying natural patterns of plant distribution and help to predict species' responses to human introduction, extirpation, and habitat alteration. Because better colonizers are more likely to become invasive, more apt to survive habitat fragmentation, and quicker to recover after restoration, identifying traits that promote plant migration can aid efforts to preserve biological diversity in human-modified habitats. One trait long thought to facilitate colonization is the ability to self-fertilize (Lloyd, 1980
). Darwin (1876)
discussed the suggestion that hermaphroditic and monoecious plants should spread more easily than dioecious species because a single individual could found a reproductive population. On the same principle, Baker (1955
, 1967
) proposed that self-compatibility should facilitate long-distance dispersal, an idea Stebbins (1957)
called "Baker's Law." In fact, self-fertilization would be favored not only in migration across long distances, but in any landscape with frequent local colonization and extinction (Pannell and Barrett, 1998
).
Despite the logical appeal and theoretical support of this hypothesis, however, it remains unclear how often range expansions and establishment events actually depend on selfing. Most of the empirical evidence for Baker's Law comes from large-scale, biogeographic patterns, such as the prevalence of self-compatible species in island floras (Carlquist, 1974
; McMullen, 1987
; Webb and Kelly, 1993
; Anderson et al., 2001
). In many cases, selfing taxa occur at the range margins of outcrossing sister taxa (Solbrig and Rollins, 1977
; Wyatt, 1986
; Barrett and Shore, 1987
; Barrett et al., 1989
; Moeller and Geber, 2005
). These patterns suggest an association between selfing and historical colonization, but few studies have directly measured both selfing ability and colonization success during ongoing migrations. For example, species introductions have allowed for comparisons of selfing abilities among congeners of varying invasiveness (Gerlach and Rice, 2003
) and between established and recently colonized populations (Schueller, 2004
).
Like the spread of invasives, the recolonization of restored habitats by native species provides an ideal opportunity to study the role of selfing in contemporary colonization. Among the most common restored habitats worldwide are forests on abandoned agricultural lands (Williams, 1989
; Ball, 2001
). Even hundreds of years after reforestation, herbaceous forest species vary widely in their ability to recolonize post-agricultural sites (reviewed by Flinn and Vellend, 2005
). While several studies have explored relationships between migration rates and life history traits, especially those associated with dispersal (Matlack, 1994
; Verheyen et al., 2003
), none have examined how plant mating systems may affect the recolonization of post-agricultural forests.
Here I use a post-agricultural landscape in central New York to investigate whether selfing ability may contribute to the differential colonization success of three fern species. Ferns and other homosporous plants are particularly interesting in this context because their mating systems potentially include outcrossing, between gametophytes from different sporophytes; intergametophytic selfing, between gametophytes from the same sporophyte, which is analogous to selfing in seed plants; and intragametophytic selfing, between gametes from the same gametophyte, which has no analog in seed plants and yields fully homozygous progeny (Klekowski, 1969
). Though all homosporous plants have the potential to produce bisexual gametophytes, most maintain outcrossing mating systems through several primary mechanisms (Haufler, 1987
; Soltis and Soltis, 1992
). Gametophytes may become unisexual by developing male and female function either exclusively or sequentially. In many species, mature female gametophytes enhance opportunities for outcrossing by releasing antheridiogen, a pheromone that stimulates spore germination and induces maleness in neighboring gametophytes (Näf, 1979
). When gametophytes do undergo intragametophytic selfing, deleterious recessive alleles may hinder the survival of the completely homozygous sporophytes (Klekowski, 1969
). Ferns' great capacity for dispersal via windblown spores presumably facilitates outcrossing by increasing mate availability in many habitats. In order to mate, however, two gametophytes must establish simultaneously within about 5–10 cm of one another, an unlikely event after long-distance dispersal (Peck et al., 1990
; Schneller et al., 1990
; Greer and McCarthy, 1997
). Thus, selfing may be as important to colonization in ferns as in seed plants.
This study focuses on Dryopteris carthusiana (Villars) H. P. Fuchs, Dryopteris intermedia (Muhlenberg ex Willdenow) A. Gray, and Polystichum acrostichoides (Michaux) Schott (Dryopteridaceae), which are wintergreen, herbaceous perennials common in mesic, upland forests and native to eastern North America (Montgomery and Wagner
, 1993; Wagner, 1993
). The range of D. carthusiana also extends throughout Eurasia. Despite a similar capacity for long-distance dispersal via windblown spores (Flinn, 2006
), these three species have contrasting distributions across forests that were never cleared for agriculture (i.e., primary forests) and forests that established on plowed fields 85–100 years ago (i.e., secondary forests, sensu Rackham, 1980
; Peterken, 1981
). In central New York, P. acrostichoides is among the herb species most restricted to primary forests, D. intermedia is equally frequent in the two forest types, and D. carthusiana is more frequent in secondary forests (Singleton et al., 2001
; Flinn, 2006
). I hypothesized that, if selfing facilitated colonization, then species that are more successful colonists should have greater selfing ability than species that are less successful colonists. Thus, I expected D. carthusiana to have greater selfing ability than D. intermedia, and D. intermedia to have greater selfing ability than P. acrostichoides. Another reason to predict a higher tolerance for inbreeding in D. carthusiana is that this species is tetraploid, whereas D. intermedia and P. acrostichoides are diploid (Montgomery and Wagner, 1993; Wagner, 1993
), and the fixed heterozygosity of recent polyploids should reduce inbreeding depression (Stebbins, 1950
; Lande and Schemske, 1985
). In addition, if populations in secondary forests were recently founded through selfing, then plants from secondary forests should have greater selfing ability than plants from primary forests. To test these hypotheses, I conducted an experiment in which I grew gametophytes either in isolation or in pairs, allowing different levels of inbreeding, and compared rates of sporophyte production.
MATERIALS AND METHODS
Study sites
Spores for this experiment came from fern populations in three pairs of adjacent primary and secondary forests, located on mesic uplands in Tompkins County, New York, USA. The secondary forests were abandoned from agriculture 85–100 years ago, according to 1936–1938 aerial photographs. Field evidence showed they had been plowed, eliminating all native vegetation. In central New York, both the Dryopteris species and Polystichum acrostichoides occur in tree and shrub thickets on sites plowed 20–40 years before (Stover and Marks, 1998
). Therefore, fern populations in the oldest secondary forests may have established as many as 80 years ago, whereas populations in primary forests could have continuously occupied the sites for hundreds of years.
Spore collection
To obtain spores, I collected fertile fronds of the three species between 30 June and 11 July 2003. Using transects to stratify samples across 1 ha, I took fronds from 20–30 plants of each species from each forest stand. The fronds were sealed in glassine envelopes and dried in ovens at 35°C for 1 wk to promote spore release.
Gametophyte culture
I sowed the spores on nutrient medium in 60 x 15 mm petri dishes by piercing the glassine envelopes with an insect pin, making holes just large enough to sift out spores without pieces of frond, indusia, or sporangia (D. R. Farrar, Iowa State University, personal communication). The medium contained Parker's macroelements and Thompson's microelements solidified with 1% agar (Klekowski, 1969
). To minimize contamination, I autoclaved the medium at 121°C for 15 min and added the fungicide nystatin at 50 mg/L. The dishes were sealed with Parafilm (American National Can, Chicago, Illinois, USA) and placed in a growth chamber under 14 h light at 26°C and 10 h dark at 16°C.
Experimental crosses
After 2 wk, I established crosses by transplanting gametophytes onto fresh medium with a dissecting microscope and a scalpel, placing pairs 1 cm apart. To compare reproductive success at four potential levels of inbreeding, gametophytes grew either in isolation, paired with another gametophyte from the same sporophyte, paired with a gametophyte from a different sporophyte in the same population, or paired with a gametophyte from a sporophyte in a different population at least 2 km away. Pairs were randomly matched within the appropriate pool. Isolated gametophytes could only reproduce through intragametophytic selfing, whereas paired gametophytes could either self-fertilize or outcross. The four inbreeding levels were crossed with the three species and the two forest types in a fully factorial design. Replicating the experiment across three sites and 20 plants per population therefore yielded 1440 crosses involving 2520 gametophytes. I maintained the cultures for 18 mo, watering gametophytes with an eyedropper to facilitate fertilization and examining them monthly for the presence of sporophytes.
Statistical analysis
I assessed the effects of inbreeding level, species, forest history, and their interactions on the likelihood of sporophyte production with maximum-likelihood analysis (PROC CATMOD in SAS; SAS Institute, Cary, North Carolina, USA). An additional factor accounted for site effects. I tested all possible two- and three-way interactions and dropped from the final model those not significant at P < 0.05. This analysis considered only the 953 gametophytes that survived to sexual maturity, at least 1 mo after transplanting. To make maximum use of the available information, the analysis included sporophyte production from each member of pairs.
RESULTS
Gametophytes had modest reproductive success overall. Of gametophytes that survived to sexual maturity, 39% formed sporophytes. The three species had significantly different rates of sporophyte production (Table 1). Across all treatments, Dryopteris carthusiana had the highest reproductive success, with 50% of gametophytes forming sporophytes; Dryopteris intermedia was intermediate, with 31%; and Polystichum acrostichoides had the lowest reproductive success, with 21%.
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DISCUSSION
This experiment revealed differences among species in gametophyte reproductive biology that may have a strong influence on the colonization of post-agricultural forests by these ferns. The most successful colonist, Dryopteris carthusiana, had the greatest reproductive success overall, whereas the least successful colonist, Polystichum acrostichoides, had the lowest. In fact, D. carthusiana gametophytes were over twice as likely to form sporophytes as those of P. acrostichoides. Such consistently higher rates of sporophyte production could speed the colonization process and help explain the species' distributions. In addition, the species' responses to inbreeding were consistent with the hypothesis that selfing ability may facilitate colonization. The potential for self-fertilization was greater in D. carthusiana than in D. intermedia, and in D. intermedia than in P. acrostichoides.
These laboratory results agree with previous characterizations of the species' mating systems based on patterns of genetic variation in natural sporophyte populations. For example, populations of D. carthusiana had significant heterozygote deficiencies at polymorphic loci, suggesting high selfing rates (C. R. Werth, deceased, and C. H. Haufler, University of Kansas, unpublished data cited in Xiang et al., 2000
). In contrast, D. intermedia appears to breed randomly, as indicated by genotype frequencies in accord with Hardy–Weinberg equilibrium (C. R. Werth, deceased, unpublished data cited in Xiang et al., 2000
). Allozyme data demonstrated that P. acrostichoides and five other North American Polystichum species are highly outcrossing (Soltis and Soltis, 1990
). In seven populations across the eastern United States, P. acrostichoides maintained high levels of genetic variation within populations, with inbreeding coefficients ranging from 0.007–0.084 and intragametophtyic selfing rates (estimated from genotype frequencies according to Holsinger, 1987
) ranging from 0–12% (Soltis and Soltis, 1990
; Soltis et al., 1990
). The 11% intragametophytic selfing rate documented here for P. acrostichoides thus falls within the range of selfing rates estimated from natural populations.
Previous studies of gametophyte ontogeny suggest that sex expression patterns may contribute to the reproductive outcomes observed in this experiment. Growing isolated D. carthusiana gametophytes on agar, Peck (1985)
found that 86% were bisexual, indicating a high potential for self-fertilization. In denser laboratory cultures on soil (1–3 gametophytes cm–2), both D. carthusiana and D. intermedia had mostly female gametophytes, 59–70%, with 17–27% male and 13–14% bisexual (Cousens, 1975
). It is unknown whether D. carthusiana produces or responds to antheridiogen, but sex expression in D. intermedia can be influenced by this pheromone (C. R. Werth, deceased, unpublished data cited in Xiang et al., 2000
). For P. acrostichoides, Greer and McCarthy (1997
, 1999
) reported that isolated gametophytes grown on soil invariably became female and remained unisexual, forming antheridia only on lobes separated from the meristem by necrosis. This pattern of sex expression, mediated by antheridiogen (Näf, 1979
; Greer and McCarthy, 1997
), would provide a mechanism to explain the species' highly outcrossing mating system.
The development of gametophytes in laboratory cultures, especially in isolation and on agar, may differ from growth patterns in denser populations and under field conditions (Rubin and Paolillo, 1983
; Ranker and Houston, 2002
). Likewise, the low overall reproductive success of gametophytes in this experiment, though comparable to rates seen in many other species (Peck et al., 1990
), may reflect the cultural regime. In this case, however, the results of laboratory tests appear consistent with the available information from natural populations.
The species' contrasting mating systems also seem to support theoretical predictions about the evolutionary consequences of polyploidy. Polyploid species are expected to self-fertilize more often than diploids because genome duplication initially mitigates the effects of genetic load (Stebbins, 1950
; Lande and Schemske, 1985
). In the case study presented here, the allotetraploid D. carthusiana had a higher selfing rate than D. intermedia, one of its diploid progenitors (Walker, 1961
), or P. acrostichoides, another closely related diploid. This example thus adds to the growing number of cases in which polyploid fern species tend to self-fertilize more than their diploid relatives (Hedrick, 1987
; Masuyama and Watano, 1990
; Soltis and Soltis, 2000
; Chiou et al., 2002
), though the relationship between polyploidy and inbreeding in seed plants remains much less clear (Husband and Schemske, 1997
; Cook and Soltis, 1999
; Mable, 2004
; B. C. Barringer, Cornell University, unpublished manuscript).
Within species, I found no evidence for an association between the history of populations and their selfing ability. One plausible explanation for this result is that, contrary to the original hypothesis, the foundation of fern populations in post-agricultural forests did not involve elevated rates of self-fertilization. Because the post-agricultural forests in this study were adjacent to continuously forested areas, fern populations may have spread gradually across the land-use boundaries, remaining contiguous with areas of higher plant density that allowed for outcrossing. The proximity to source populations also makes the simultaneous arrival of multiple spores more likely. In fact, I have documented substantial spore banks in the soil of post-agricultural forests adjacent to but not containing sporophyte populations of these species (Flinn, 2006
). Similar situations may be common in the region, as about 90% of the area in secondary forest is contiguous with older stands (Smith et al., 1993
).
Alternatively, even if populations did establish through selfing, they may have grown sufficiently old and large that evidence of founder events involving selfing is no longer detectable. Rather, existing plants' selfing abilities could depend more strongly on mating patterns at current population densities than on a population bottleneck that may have occurred as many as 80 years ago. To obtain sufficient sample sizes for the experiment, I chose sites where all three species had population densities of at least 20 plants ha–1 in each forest stand. The effects of a founder event might be more evident at other sites in the region where population densities remain lower or in more isolated or more recently established populations. If in fact fern populations in forests of different history have similar selfing rates, the genetic consequences of post-agricultural forest colonization may be comparable to those seen for Trillium grandiflorum (Michx.) Salisb. in the same central New York landscape; primary and secondary forest populations did not differ in inbreeding coefficients or observed heterozygosity, though allelic richness and expected heterozygosity were slightly lower in secondary forests (Vellend, 2004
). Describing patterns of genetic variation within and among fern populations would substantially improve our understanding of the role of selfing in the colonization of post-agricultural forests.
Several other studies have related mating systems to colonizing ability in ferns, at either the species or the population level. Based on studies of gametophyte development and reproduction, Holbrook-Walker and Lloyd (1973)
and Lloyd (1974)
suggested that Hawaiian fern species frequently found on newly formed lava flows, though primarily outcrossing, retained a greater ability to self-fertilize than species of late-successional habitats. In two species of Hawaiian Sadleria Kaulf., however, Ranker et al. (1996)
later found that even populations on recent lava flows had genotype frequencies indicative of outcrossing and gametophytes with primarily unisexual development, antheridiogen systems, and very little ability to form sporophytes in isolation. Among three South Asian ferns, Singh and Roy (1977)
found a greater capacity for self-fertilization in the more widely distributed, generalist species. Ranker et al. (2000)
noted that the four fern species for which genetic evidence suggests a mixed mating system occupy both disturbed places and more stable habitats. A high capacity for self-fertilization may also have facilitated the spread of two invasive fern species in Florida (Lott et al., 2003
).
While fewer studies have addressed mating-system variation among fern populations, Cousens (1979)
found a higher incidence of bisexuality and a greater ability to self-fertilize in gametophytes from a disjunct population than from the central range of Blechnum spicant (L.) J. Sm. Similarly in Asplenium platyneuron (L.) Oakes, geographically disjunct, solitary plants on recent coal spoils had greater selfing ability than plants from dense populations in the center of the species' range (Crist and Farrar, 1983
). Peck et al. (1990)
contrasted the selfing and colonization abilities of A. platyneuron with Adiantum pedatum L., which had a very low rate of sporophyte formation by isolated gametophytes and had failed to colonize the coal spoils from adjacent populations for 50 years. Together with these studies, the patterns of fern reproductive biology documented here suggest that selfing ability may often be an important component of population establishment following long-distance dispersal.
FOOTNOTES
1 The author would like to thank D. Paolillo, D. Farrar, T. Ranker, and J. Metzgar for advice and encouragement about growing fern gametophytes; S. Gardescu, V. Connolly, and S. Roche for help in watering and transplanting; and P. Marks, M. Geber, and the Geber lab group for input and support. Comments from B. Bedford, H. Sahli, D. Moeller, C. Haufler, and an anonymous reviewer improved the manuscript. This research was supported by the New York State Biodiversity Research Institute, the Andrew W. Mellon Foundation, a Sigma Xi Grant-in-Aid of Research, and a National Science Foundation Graduate Research Fellowship. 
2 Author for correspondence (kmf27{at}cornell.edu
)
LITERATURE CITED
Anderson G. J. Bernardello G. Stuessy T. F. Crawford D. J.. 2001. Breeding system and pollination of selected plants endemic to Juan Fernandez Islands. American Journal of Botany 88: 220-233.
Baker H. G.. 1955. Self-compatibility and establishment after "long-distance" dispersal. Evolution 9: 347-349.[CrossRef][ISI]
Baker H. G.. 1967. Support for Baker's law—as a rule. Evolution 21: 853-856.[CrossRef][ISI]
Ball J. B.. 2001. Global forest resources: history and dynamics. In J. Evans [ed.] The forests handbook, vol. 1 3-22 Blackwell Science, Oxford, UK.
Barrett S. C. Morgan M. T. Husband B. C.. 1989. The dissolution of a complex genetic polymorphism: the evolution of self-fertilization in tristylous Eichhornia paniculata (Pontederiaceae). Evolution 43: 1398-1416.[CrossRef][ISI]
Barrett S. C. Shore J. S.. 1987. Variation and evolution of breeding systems in the Turnera ulmifolia L. complex (Turneraceae). Evolution 41: 340-354.[CrossRef][ISI]
Carlquist S.. 1974. Island biology Columbia University Press, New York, New York, USA.
Chiou W.-L. Farrar D. R. Ranker T. A.. 2002. The mating systems of some epiphytic Polypodiaceae. American Fern Journal 92: 65-79.[CrossRef]
Cook L. M. Soltis P. S.. 1999. Mating systems of diploid and allotetraploid populations of Tragopogon (Asteraceae). I. Natural populations. Heredity 82: 237-244.
Cousens M. I.. 1975. Gametophyte sex expression in some species of Dryopteris. American Fern Journal 65: 39-42.[CrossRef]
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.[CrossRef][ISI]
Crist K. C. Farrar D. R.. 1983. Genetic load and long-distance dispersal in Asplenium platyneuron. Canadian Journal of Botany 61: 1809-1814.[ISI]
Darwin C.. 1876. The effects of cross- and self-fertilization in the vegetable kingdom John Murray, London, England.
Flinn K. M.. 2006. Influences of past agriculture and present environment on plant distributions: population ecology of three fern species in central New York forests Ph.D. dissertation, Cornell University, Ithaca, New York, USA.
Flinn K. M. Vellend M.. 2005. Recovery of forest plant communities in post-agricultural landscapes. Frontiers in Ecology and the Environment 3: 243-250.[ISI]
Gerlach J. D. Rice K. J.. 2003. Testing life history correlates of invasiveness using congeneric plant species. Ecological Applications 13: 167-179.[CrossRef][ISI]
Greer G. K. McCarthy B. C.. 1997. The antheridiogen neighborhood of Polystichum acrostichoides (Dryopteridaceae) on a native substrate. International Journal of Plant Sciences 158: 764-768.[CrossRef][ISI]
Greer G. K. McCarthy B. C.. 1999. Gametophytic plasticity among four species of ferns with contrasting ecological distributions. International Journal of Plant Sciences 160: 879-886.[CrossRef][ISI][Medline]
Haufler C. H.. 1987. Electrophoresis is modifying our concepts of evolution in homosporous pteridophytes. American Journal of Botany 74: 953-966.[CrossRef][ISI]
Hedrick P. W.. 1987. Genetic load and the mating system in homosporous ferns. Evolution 41: 1282-1289.[CrossRef][ISI]
Holbrook-Walker S. G. Lloyd R. M.. 1973. Reproductive biology and gametophyte morphology of the Hawaiian fern genus Sadleria (Blechnaveae) relative to habitat diversity and propensity for colonization. Botanical Journal of the Linnean Society 67: 157-174.
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.[CrossRef][ISI]
Husband B. C. Schemske D. W.. 1997. The effect of inbreeding in diploid and tetraploid populations of Epilobium angustifolium (Onagraceae): implications for the genetic basis of inbreeding depression. Evolution 51: 737-746.[CrossRef][ISI]
Klekowski E. J. Jr.. 1969. Reproductive biology of the Pteridophyta. III. A study of the Blechnaceae. Botanical Journal of the Linnean Society 62: 361-377.
Lande R. Schemske D. W.. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: 24-40.[CrossRef][ISI]
Lloyd D. G.. 1980. Demographic factors and mating patterns in Angiosperms. In O. T. Solbrig [ed.] Demography and evolution in plant populations 67-88 University of California Press, Berkeley, California, USA.
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.
Lott M. S. Volin J. C. Pemberton R. W. 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.
Mable B. K.. 2004. Polyploidy and self-compatibility: is there an association?. New Phytologist 162: 803-811.[CrossRef][ISI]
Masuyama S. Watano Y.. 1990. Trends for inbreeding in polyploid pteridophytes. Plant Species Biology 5: 13-17.
Matlack G. R.. 1994. Plant species migration in a mixed-history forest landscape in eastern North America. Ecology 75: 1491-1502.[CrossRef][ISI]
McMullen C. K.. 1987. Breeding systems of selected Galapagos Islands angiosperms. American Journal of Botany 74: 1694-1705.[CrossRef][ISI]
Moeller D. A. Geber M. A.. 2005. Ecological context of the evolution of self-pollination in Clarkia xantiana: population size, plant communities, and reproductive assurance. Evolution 59: 786-799.[ISI][Medline]
Montgomery J. D. Wagner W. H. Jr.. 1993. Dryopteris. In Flora of North America Editorial Committee [eds.] Flora of North America north of Mexico, vol. 2 Oxford University Press, New York, New York, USA.
Näf U.. 1979. Antheridiogens and antheridial development. In A. F. Dyer [ed.] The experimental biology of ferns 435-470 Academic Press, London, UK.
Pannell J. R. Barrett S. C. H.. 1998. Baker's Law revisited: reproductive assurance in a metapopulation. Evolution 52: 657-668.[CrossRef][ISI]
Peck C. J.. 1985. Reproductive biology of isolated fern gametophytes. Ph.D. dissertation Iowa State University, Ames, Iowa, USA.
Peck J. H. Peck C. J. Farrar D. R.. 1990. Influences of life history attributes on formation of local and distant fern populations. American Fern Journal 80: 126-142.[CrossRef]
Peterken G. F.. 1981. Woodland conservation and management Chapman and Hall, London, UK.
Rackham O.. 1980. Ancient woodland: its history, vegetation and uses in England E. Arnold, London, UK.
Ranker T. A. Gemill C. E. C. Trapp P. G.. 2000. Microevolutionary patterns and processes of the native Hawaiian colonizing fern Odontosoria chinensis (Lindsaeaceae). Evolution 54: 828-839.[ISI][Medline]
Ranker T. A. Gemill C. E. C. Trapp P. G. Hambleton A. Ha K.. 1996. Population genetics and reproductive biology of lava-flow colonising species of Hawaiian Sadleria (Blechnaceae). In J. M. Camus, M. Gibby, and R. J. Johns [eds.] Pteridology in perspective 581-598 Royal Botanic Gardens, Kew, UK.
Ranker T. A. Houston H. A.. 2002. Is gametophyte sexuality in the laboratory a good predictor of sexuality in nature?. American Fern Journal 92: 112-118.[CrossRef]
Rubin G. Paolillo D. J. Jr.. 1983. Sexual development of Onoclea sensibilis on agar and soil media without the addition of antheridiogen. American Journal of Botany 70: 811-815.[CrossRef][ISI]
Schneller J. J. Haufler C. H. Ranker T. A.. 1990. Antheridiogen and natural gametophyte populations. American Fern Journal 80: 143-152.[CrossRef][ISI]
Schueller S. K.. 2004. Self-pollination in island and mainland populations of the introduced hummingbird-pollinated plant, Nicotiana glauca (Solanaceae). American Journal of Botany 91: 672-681.
Singh V. P. Roy S. K.. 1977. Mating systems and distribution in some tropical ferns. Annals of Botany 41: 1055-1060.
Singleton R. Gardescu S. Marks P. L. Geber M. A.. 2001. Forest herb colonization of postagricultural forests in central New York State, USA. Journal of Ecology 89: 325-338.
Smith B. E. Marks P. L. Gardescu S.. 1993. Two hundred years of forest cover changes in Tompkins County, New York. Bulletin of the Torrey Botanical Club 120: 229-247.[CrossRef][ISI]
Solbrig O. T. Rollins R. C.. 1977. The evolution of autogamy in species of the mustard genus Leavenworthia. Evolution 31: 265-281.[CrossRef][ISI]
Soltis D. E. Soltis P. S.. 1992. The distribution of selfing rates in homosporous ferns. American Journal of Botany 79: 97-100.[CrossRef][ISI]
Soltis P. S. Soltis D. E.. 1990. Genetic variation within and among populations of ferns. American Fern Journal 80: 161-172.[CrossRef][ISI]
Soltis P. S. Soltis D. E.. 2000. The role of genetic and genomic attributes in the success of polyploids. Proceedings of the National Academy of Sciences, USA 97: 7051-7057.
Soltis P. S. Soltis D. E. Wolf P. G.. 1990. Allozymic divergence in North American Polystichum (Dryopteridaceae). Systematic Botany 15: 205-215.[CrossRef][ISI]
Stebbins L. G.. 1950. Variation and evolution in plants Columbia University Press, New York, New York, USA.
Stebbins L. G.. 1957. Self-fertilization and population variability in the higher plants. American Naturalist 91: 337-354.[CrossRef][ISI]
Stover M. E. Marks P. L.. 1998. Successional vegetation on abandoned cultivated and pastured land in Tompkins County, New York. Journal of the Torrey Botanical Society 125: 150-164.[CrossRef][ISI]
Vellend M.. 2004. Parallel effects of land-use history on species diversity and genetic diversity of forest herbs. Ecology 85: 3043-3055.[CrossRef][ISI]
Verheyen K. Honnay O. Motzkin G. Hermy M. Foster D. R.. 2003. Response of forest plant species to land-use change: a life-history trait-based approach. Journal of Ecology 91: 563-577.
Wagner D. H.. 1993. Polystichum. In Flora of North America Editorial Committee [eds.] Flora of North America north of Mexico, vol. 2 Oxford University Press, New York, New York, USA.
Walker S.. 1961. Cytogenetic studies in the Dryopteris spinulosa complex. II. American Journal of Botany 48: 607-614.[CrossRef][ISI]
Webb C. J. Kelly D.. 1993. The reproductive biology of the New Zealand flora. Trends in Ecology and Evolution 8: 442-447.[CrossRef]
Williams M.. 1989. Americans and their forests: a historical geography Cambridge University Press, New York, New York, USA.
Wyatt R.. 1986. Ecology and evolution of self-pollination in Arenaria uniflora (Caryophyllaceae). Journal of Ecology 74: 403-418.[CrossRef][ISI]
Xiang L. Werth C. R. Emery S. N. McCauley D. E.. 2000. Population-specific gender-biased hybridization between Dryopteris intermedia and D. carthusiana: evidence from chloroplast DNA. American Journal of Botany 87: 1175-1180.
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