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Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks,Fairbanks, Alaska 99775-6100
Received for publication August 10, 1998. Accepted for publication March 18, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Alaska • allozymes • Dryas octopetala; • ecotypes • genetic variation • morphology • Rosaceae • subspecies • tundra
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Moran and Hopper, 1983
; Murdy and Brown Carter, 1985
; Shaw and Schneider, 1995
) and has often been used to explain reductions in genetic diversity through founder effect and genetic bottlenecks (e.g., Schwaegerle and Schaal, 1979
; Barrett and Kohn, 1991
; Premoli, Chischilly, and Mitton, 1994
; Young, Boyle, and Brown, 1996
). Natural selection can also lead to allozyme differentation among populations (Grant and Mitton, 1977
; Galen, Shore, and Deyoe, 1991
; Mopper et al., 1991
; Aitken and Libby, 1994
), but has been more widely implicated in divergence of morphological traits during adaptive evolution (e.g., Clausen, Keck, and Hiesey, 1948
; Jain and Bradshaw, 1966
; Antonovics, 1971
). Finally, differentiation of populations is often strongly dependent on biogeographic history (e.g., Raup and Gould, 1974
; Felsenstein, 1985
; Armbruster and Schwaegerle, 1996
). Genetic differences may often reflect historical events and phylogenetic relationships among populations rather than an equilibrium among gene flow, drift, and selection.
Dryas octopetala in interior Alaska offers a unique opportunity to investigate the effects of drift, selection, and gene flow on organization of genes within and among populations. The species can be divided into two subspecies (Hultén, 1959, 1968
), which often occur in adjacent habitats, sometimes separated only by metres. Gene flow between subspecies may occur (McGraw and Antonovics, 1983
), and plants combining features of both species are found infrequently and attributed to hybridization (Hultén, 1968
). Strong natural selection may be responsible for maintaining differences between subspecies; McGraw and Antonovics (1983)
report selection coefficients greater than 0.50 against alien transplants. Genetic drift may also play an important role in the evolution of the species. Hultén (1959)
suggests that during the last glaciation of North America, Alaskan Dryas species were restricted to nonglaciated refugia in central Alaska but achieved widespread distribution following glacial retreat. Both subspecies are now restricted in interior Alaska to patches of alpine habitat. Gene flow among populations may be very low; populations are often isolated by hundreds of kilometres of unsuitable habitat.
In this study we describe the organization of genetic variation within and among Alaskan populations of each subspecies and evaluate the roles of biogeographic history, gene flow, natural selection, and genetic drift in the evolution of this species. We examine genetic variation in morphological traits that may be subject to natural selection as well as variation at enzyme loci that may have little or no adaptive significance. We also assess the potential for gene flow between subspecies by conducting a series of breeding experiments.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) or species (D. octopetala and D. alaskensis; Porsild, 1947
), based on leaf pubescence and the occurrence of scales or glands on the leaves. Gottlieb (1984)
argues that such diagnostic traits are often determined by one or a few genes. These subspecies (as they are treated in this paper) have different suites of morphological and life-history traits, which are genetically determined and which confer selective advantage in their respective habitats (McGraw and Antonovics, 1983
; McGraw, 1985a, b, 1987a, b)
. Subspecies octopetala is adapted to xeric ridge or fellfield habitats and is identified by the presence of "octopetala" scales on the undersides of densely pubescent leaves (Hultén, 1959, 1968
; McGraw and Antonovics, 1983
). Subspecies alaskensis is adapted to wet tundra and snowbed depressions and is distinguished by the presence of glandular structures on the underside of glabrous leaves (Hultén, 1959, 1968
; McGraw and Antonovics, 1983
). Subspecies alaskensis is endemic to western Yukon and central Alaska and may have arisen during the Pleistocene from the circumpolar species Dryas. o. ssp. octopetala (Hultén, 1959
). In interior Alaska both subspecies grow in alpine tundra geographically isolated from other tundra areas by unsuitable lowland habitat. The fellfield habitat of ssp. octopetala and snowbed depression habitat of ssp. alaskensis are often closely adjacent (Miller, 1982
; McGraw and Antonovics, 1983
); thus, these subspecies may grow only a few metres apart. To our knowledge ssp. alaskensis only occurs adjacent to ssp. octopetala, but ssp. octopetala often occurs without an adjacent population of ssp. alaskensis. Flowers are obligately entomophilous on Wrangell Island (Tikhmenev, 1985
) and are apparently obligate outcrossers in Alaska, as there is no evidence for apomixis, auto-fertility, or self-fertility (McGraw and Antonovics, 1983
). The flowers are visited primarily by Diptera (Elkington, 1971
; McGraw and Antonovics, 1983
). The species is diploid with 2n = 18 (Federov, 1969
; Elkington, 1971
; Löve and Löve, 1975
; Krogulevich and Rostovtseva, 1984)
. Seeds are wind dispersed (Elkington, 1971
), though it is unlikely that wind often carries achenes between isolated tundra areas (Elkington, 1971
; McGraw and Antonovics, 1983
). The subspecies are interfertile (McGraw and Antonovics, 1983
), and morphologically intermediate plants (presumed hybrids) are observed in habitat intermediate between fellfield and snowbed (Hultén, 1968
). Previous studies have not reported whether putative hybrids are fertile or sterile.
Plant material
Achenes of D. o. ssp. octopetala and ssp. alaskensis were collected from nine locations in interior Alaska (Fig. 1). Six of these locations (Eagle Summit, McCallum Creek, Mount Fairplay, Paxson Mountain, Polychrome Ridge, and Twelvemile Summit) host adjacent populations of ssp. octopetala and alaskensis. Three locations (Lime Mine, Murphy Dome, Wickersham Dome) contain only ssp. octopetala. The four northern populations occur in the White Mountains; Mount Fairplay is part of the Yukon-Tanana Uplands. The remaining four southern populations occur in the Alaska Range. Mountain ranges are isolated by regions of coniferous forest (Viereck et al., 1992
, p. 9).
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100 plants of each subspecies, collecting one leaf and one entire infructescence (achenecetum), representing one open-pollinated maternal family. Acheneceta were collected at least 2 m apart to reduce the possibility of collecting more than one achenecetum per genet. Subspecies designations were confirmed in the laboratory: presence of glands on the undersides of leaves indicates ssp. alaskensis, whereas the presence of "octopetala" scales indicates ssp. octopetala (Hultén, 1968
). Samples for which neither glands nor scales, or both glands and scales, were present (<1%) were not used. Acheneceta were stored at -17°C until needed for electrophoresis or greenhouse experiments.
Electrophoresis
Achenes were placed on wet paper towels under constant illumination to effect germination. Only one seedling from each maternal family was chosen for electrophoresis when the first two true leaves developed at 4–6 wk. Whole seedlings were homogenized in 30–50 µL of extraction buffer. A tris-citrate buffer described by Cheliak and Pitel (1984)
was used to grind samples for isocitrate dehydrogenase (IDH) visualization. Wendel and Weeden's (1989)
tris-HCl grinding buffer number 3 for "tissues with high levels of interfering substances" was used for other enzymes. Whole-plant extracts were loaded into sample wells for cellulose acetate gels (Super Z-12 applicator kit, Helena Laboratories, Beaumont, Texas) or absorbed onto 0.3 x 1.5 cm filter paper wicks for starch gels.
IDH was resolved on 76 x 76 mm cellulose acetate gel plates (Titan III Zip Zone, Helena Laboratories, Beaumont, Texas) in the tris-borate-EDTA pH 8.6 electrode buffer number 10 of Soltis et al. (1983)
, using the techniques and enzyme staining recipe outlined by Hebert and Beaton (1989)
. Gels were run at 200 VDC for 20 min at 4°C. Glyceraldehyde-3-phosphate dehydrogenase, NAD-dependent form ([NAD]G3PDH) and NADP-dependent form ([NADP]G3PDH), glucose-6-phosphate dehydrogenase (G6PDH), malate dehydrogenase (MDH), phosphogluconate dehydrogenase (PGD), and shikimate dehydrogenase (SKD) were resolved on 12% starch gels using the tris-citrate pH 7.0 gel and electrode buffer system of Meizel and Markert (1967)
as described in Wendel and Weeden (1989)
. Gels were run at 50 mA for 6 h at 4°C. Protocols for enzyme staining and techniques for gel preparation, loading, and slicing followed Wendel and Weeden (1989)
. Cellulose acetate and starch gels were scored when bands showed clearly, usually within 0.5 h of staining. For those enzyme systems with more than one presumed locus present on a gel, the most anodal locus was designated as number 1. Alleles at a locus were designated f for the fastest moving (most anodal migration), m for medium, or s for slowest moving (most cathodal position).
Allele frequencies
For each population (subspecies within a location), genotype frequencies were inferred from counts of electrophoretic phenotypes. A, the mean number of alleles per locus calculated across all nine resolved loci, P, the percentage of loci that exhibited more than one allele, HO, average heterozygosity based on direct counts, and HE, the average proportion of heterozygotes based upon Hardy-Weinberg expectations, were calculated (BIOSYS step VARIAB; Swofford and Selander, 1981
). These statistics were calculated once for each population in the study and again for each subspecies, with samples pooled without regard for collection location.
Genetic differences between subspecies and among populations were examined by four types of analyses. First, heterogeneity of allele frequencies was examined using a contingency table analysis and 
2 test (BIOSYS step Swofford and Selander, 1981
). Second, genetic structure was described for means across polymorphic loci using the inbreeding coefficients (F statistics) of Wright (1978;
BIOSYS step FSTAT; Swofford and Selander, 1981
). Third, Roger's (1972)
genetic distance (D) was calculated for all pairs of populations (BIOSYS step SIMDIS; Swofford and Selander, 1981
). Fourth, an exact randomization test was performed to determine whether allelic differences between adjacent populations of ssp. octopetala and ssp. alaskensis are less (or greater) than allelic differences between geographically isolated populations of these two subspecies. We measured heterogeneity between adjacent populations using 2 (Workman and Niswander, 1970
), which, unlike other distance measures, is sensitive to sample size. Mean 2 of the six pairs was used to summarize overall heterogeneity among adjacent populations of the two subspecies. Then, ssp. alaskensis populations (e.g., 1, 2, ... 6) were paired with ssp. octopetala populations (e.g., A, B, ... F) in all possible (6! = 720) combinations (e.g., 1A 2B 3C ... 6F, 1B 2A 3C ... 6F, 1C 2A 3B ... 6F, and so forth). For each of the 720 pairings, mean 2 was calculated.
Greenhouse study
A subset of the populations assayed for allozyme variation was examined for morphological variation (Fig. 1). Twenty-five maternal families were randomly selected from ssp. alaskensis populations at Polychrome Ridge and Twelvemile Summit and from ssp. octopetala populations at Eagle Summit, Murphy Dome, Polychrome Ridge, and Twelvemile Summit. Eight achenes from each of these 150 families were randomly placed in seed trays and germinated at room temperature under constant illumination. Seedlings were potted in standard potting mix within 24 h of germination and randomly assigned positions on the greenhouse bench. Seedlings were watered as needed and fertilized weekly with a 20:20:20 NPK solution. After 31 wk, 436 surviving individuals were scored for two characters used to discriminate subspecies: presence of glands and presence of scales. Seven quantitative traits not used as taxonomic discriminators were measured: height of plant from soil surface to highest point; maximum rosette diameter; number of teeth per centimetre on the margin of largest leaf; length of largest leaf blade; maximum width of largest leaf with revolute margins in natural configuration; maximum width of largest leaf with revolute margins flattened and spread; and width between deepest incisions on the margin of largest leaf. Presence or absence of scent was assessed for each plant in a double-blind test.
Morphometric analyses
Each quantitative variable was examined for normality and homogeneity of variance. Plant height, plant diameter, and number of teeth on leaf margins were log transformed. Leaf dimensions were square-root transformed. Statistical testing of differences between subspecies and among populations was performed using mixed-model analysis of variance (PROC MIXED; SAS, 1997
). Subspecies and populations nested within subspecies were treated as fixed effects; family was treated as a random effect nested within population. As a descriptive tool, we used Model II nested analysis of variance (PROC NESTED; SAS, 1990
) to partition phenotypic variance between subspecies, among populations within subspecies, among families within populations, and within families. Canonical discriminant analysis (PROC CANDISC; SAS, 1990
) was performed on standardized measurements to determine which suite of morphological traits maximizes the multivariate distance among populations. A matrix of generalized-squared distances between population centroids (D2) was created (PROC DISCRIM; SAS, 1990
).
Breeding studies
To determine the potential for gene flow between subspecies of D. octopetala, we generated hybrid plants and backcrossed these hybrids with plants of both subspecies. Hybrid seed was produced in the field by transferring pollen from flowers of ssp. octopetala to bagged flowers of ssp. alaskensis and from flowers of alaskensis to bagged flowers of ssp. ocotopetala. We collected hybrid seed and seed produced by open pollination of both subspecies and grew the seed in a greenhouse for several months. We performed all possible crosses (including self-pollinations) among the following: (1) plants produced by open pollination of ssp. octopetala in the field, (2) plants produced by open pollination of ssp. alaskensis in the field, (3) hybrid plants with ssp. octopetala maternal parents, and (4) hybrid plants with ssp. alaskensis maternal parents.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Morphological variation
Mixed-model analysis of variance showed highly significant differences (P < 0.0001) between subspecies in all traits measured except leaf width at incisions. Trait means differed between subspecies by as much as 50% (Table 3). Significant differences among populations were observed for six traits (P < 0.05) but not for number of incisions per centimetre (P > 0.8). Because plants were raised in a randomized design we attribute these phenotyic differences to genetic differences between subspecies and among populations.
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Application of a random-effects model to these data provides a description of the relative magnitude of each statistical effect (Table 3). Most of the variance in traits was observed within populations, but of that portion of the variance not observed within populations, most occurred between subspecies rather than among populations.
Canonical discriminate analysis determines the linear combination of morphological characters that best distinguishes populations. The first canonical axis (CAN1) separated populations of tall plants with long, deeply incised leaves from populations of short plants with short, shallowly incised leaves (Table 4). Most of the variance in CAN1 lay between subspecies (Table 3) even though CAN1 was calculated to maximize distance among populations.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Ritchie and Cwynar, 1982
) and suggest a unique history of drift, gene flow, and natural selection in this species.
Allozyme diversity
The overall amount of allozyme variation found in Dryas octopetala in interior Alaska is very low compared with amounts reported for plant species with similar life-history characteristics. Although we were limited to nine interpretable loci (most studies examine 12–20 loci; Hamrick and Godt, 1990
), both subspecies of D. octopetala have fewer alleles per locus, less than one-half the proportion of polymorphic loci, and less than one-half the expected heterozygosity reported as the average for long-lived woody perennials, narrowly distributed species, boreal-temperate plants, animal-pollinated or wind-dispersed species (see Hamrick and Godt, 1990
). The probability of selecting two or fewer polymorphic loci in a random sample of nine loci from a species with 50% polymorphic loci is 0.10, indicating that there is a reasonable chance our low estimate of genetic variation in D. octopetala is an artifact of the few loci sampled. Nevertheless, low genetic variability in this species is entirely consistent with Hultén's (1959)
proposal that Alaskan Dryas species survived the last glaciation isolated from other Dryas populations in the nonglaciated refugia of central Alaska, a period of possibly small population size and high genetic drift. Alternatively, low genetic variation may be a characteristic of the Rosaceae (e.g., Neviusia alabamensis—Freiley, 1994
; Geum radiatum—Godt, Johnson, and Hamrick, 1996
, Cercocarpus traskiae—Rieseberg and Gerber, 1995
), a family for which few allozyme data are available (see Hamrick, Linhart, and Mitton, 1979
; Loveless and Hamrick, 1984
).
The distribution of allozymes across study sites indicates surprisingly little differentiation among populations of this species. Although we found statistically significant heterogeneity in allele frequencies among populations, values of FST in this study fall among the lowest to be found in a review of 124 plant species (Loveless and Hamrick, 1984
). Several processes may account for the surprisingly low differentiation observed. Divergence of populations by genetic drift may be slow because of the large size of populations and because individual genotypes may persist for more than 100 yr (Kihlman, 1890
[cited in Porsild, 1947
]). Gene flow among populations would counter divergence, but the possibility of significant gene flow between collection sites seems remote; collection sites were distributed among three isolated mountain ranges and separated by large distances. Alternatively, low differentiation among populations within subspecies may reflect relatively recent origins. Pollen records (Ritchie and Cwynar, 1982
) indicate that following the last glaciation the range of Alaskan Dryas species expanded from glacial refugia in central Alaska and achieved a widespread continuous distribution (Hultén, 1959
) 12 000–9000 yr BP. More recently, in response to climate amelioration, trees and shrubs invaded lowland areas, and Alaskan Dryas became isolated in alpine areas (Ritchie and Cwynar, 1982
). Finally, balancing selection at allozyme loci also could counter the diversifying effects of genetic drift (Berger, 1975
; Hedrick, 1986
).
The similarity at allozyme loci between subspecies contrasts with the pattern of genetic differentiation often found between ecotypes and between morphologically distinct subspecies. Previous studies generally have found clear differences at allozyme loci that parallel phenotypic differences among taxa (e.g., Grant and Mitton, 1977
; Crawford, 1985
; Galen, Shore, and Deyoe, 1991
; Hedrén, 1996
). Furthermore, Mopper et al. (1991)
suggest that such genetic differences can arise in response to selection in a relatively brief period of time. Exceptions to the general pattern are seen among subspecies where divergence was recent and rapid (Crawford, 1985
), where gene flow countered by selection for adaptive traits swamps differences at allozyme loci (Aitken and Libby, 1994
), or where no distinct subspecies/ecotypes are present (i.e., surveys of geographic variation within species). In these cases, morphologically distinct taxa often display few if any differences at allozyme loci.
We found no evidence of gene flow between subspecies of D. octopetala. F statistics revealed differences between subspecies comparable to differences among populations isolated by hundreds of kilometres of unsuitable habitat, and a randomization test indicated no significant similarity in allele frequencies between adjacent populations of ssp. octopetala and ssp. alaskensis. This result suggests strong reproductive isolation between subspecies and is consistent with two observations: (1) McGraw and Antonovics (1983)
found that although subspecies at Eagle Summit are interfertile, differences in time of flowering reduces the frequency of cross-pollination between subspecies to <1%, and (2) at sites where subspecies co-occur we found <1% of flowering plants combined traits used to distinguish subspecies. These results support studies that treat subspecies as distinct taxa. Conflicting with this interpretation are reports of the widespread occurrence of putative hybrids (Hultén, 1959, 1968
; McGraw, 1987a
). Indeed, among field-collected seed we found significant numbers of plants (14%) from families that combine the traits (scales and glands; Hultén, 1968
) used to distinquish subspecies.
Hultén (1959)
suggests that ssp. alaskensis may have arisen from a ssp. octopetala-like ancestor during the Pleistocene in the isolation of unglaciated refugia in Alaska and Yukon. Reduced genetic variability in derived taxa relative to progenitor taxa has been widely reported (e.g., Gottlieb, 1973, 1974
; Baskauf, McCauley, and Eickmeier, 1994
; Pleasants and Wendel, 1989
; Sherman-Broyles et al., 1992
; Purdy, Bayer, and Macdonald, 1994
; Purdy and Bayer, 1995, 1996
), yet we found no evidence supporting this relationship in D. octopetala. However, the pattern of allozyme variation is consistent with Hultén's (1959)
hypothesis that contemporary Alaskan populations of both subspecies originated relatively recently from glacial refugia. Crawford (1983, 1985)
reviews several allozyme studies that also report divergence among subspecies comparable to divergence among isolated populations within subspecies. He points out that divergence at allozyme loci reflects time since isolation of populations/subspecies and argues that isolation of subspecies may often take place on the same time scale as isolation of populations within subspecies. A similar result was obtained by Godt and Hamrick (1998)
who also found little evidence of progenitor-derivative relationship between subspecies of Sarracenia rubra.
Morphological differentiation
In contrast to the allozyme data, subspecies of D. octopetala showed significant genetic differences in morphological traits. Although much of the variation in morphological traits occurred within populations, we found significant differences between subspecies for almost every trait measured. These differences are consistent with McGraw's (1985a, b, 1987b)
extensive investigations of morphological, ecological, and growth differences between subspecies of D. octopetala at Eagle Summit. We conclude that differences between subspecies at Eagle Summit reported by McGraw extend to other sites in central Alaska as well.
In contrast to the clear differences between subspecies, morphological variation among populations within subspecies paralleled the allozyme data and indicated little differentiation among populations. While differences among populations were statistically significant, these differences generally accounted for <5% of the variance observed, suggesting that within a subspecies different populations display the same range of variation in morphological traits. The occurrence of one suite of traits in ssp. alaskensis and another suite of traits in ssp. octopetala suggests that the evolution of these traits is linked. Rather than evolving independently, evolutionary change in one trait parallels evolutionary change in a host of other traits. This may occur for three reasons (Armbruster and Schwaegerle, 1996
): (1) the morphological features of ssp. alaskensis were fixed at the time of its origin and have not evolved since that time; (2) traits are genetically correlated due to linkage and/or pleiotropy, so that natural selection acting on one trait brings about a correlated response in other traits; or, (3) natural selection acts on traits in a correlated manner so that one combination of traits is favored in one environment and another combination of traits is favored in another environment. This third scenario is reminiscent of Wright's shifting-balance model, which presumes epistatic interaction among fitness traits, such that natural selection favors certain combinations of traits and eliminates other combinations. This third scenario also follows McGraw and Antonovics (1983)
and McGraw (1987a)
who concluded that selection maintains differences between subspecies. They found strong selection against alien transplants in both snowbed and fellfield habitats and reported that intermediates showed no advantage over native subspecies in either habitat or in intermediate habitat.
The high degree of fertility between subspecies and between hybrids and parental subspecies adds further support to the role of selection in maintaining subspecies differences. The absence of gene flow between subspecies suggested by the allozyme data and the lack of genetic barriers to interbreeding indicates that selection against hybrids eliminates the possibility of significant gene flow between subspecies.
Conclusions
Our results together with biogeographic and paleoecological data suggest relatively recent origins for Alaskan populations of D. octopetala ssp. octopetala and ssp. alaskensis. Divergence between subspecies at allozyme loci appears to have occurred on the same time scale as divergence among populations within subspecies. Lack of morphological differentiation among populations within each subspecies further supports a recent origin for these populations. Morphological differences between subspecies follow earlier studies that indicate natural selection is responsible for subspecies differences, and the high degree of interfertility between ssp. octopetala, ssp. alaskensis, and their hybrids strengthens claims that natural selection against intermediates maintains complete or nearly complete reproductive isolation between subspecies.
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FOOTNOTES |
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2
Author for correspondence (ffkes{at}aurora.alaska.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Antonovics, J. 1971 The effects of a heterogeneous environment on the genetics of natural populations. American Scientist 59: 593–599.[ISI][Medline]
Armbruster, W. S., and K. E. Schwaegerle. 1996 Causes of covariation of phenotypic traits among populations. Journal of Evolutionary Biology 9: 261–276.[CrossRef][ISI]
Barrett, S. C. H., and J. R. Kohn. 1991 Genetic and evolutionary consequences of small population size in plants: implications for conservation. In D. A. Falk and K. E. Holsinger [eds.], Genetics and conservation of rare plants, 3–30. Oxford, New York, NY.
Baskauf, C. J., D. E. McCauley, and W. G. Eickmeier. 1994 Genetic analysis of a rare and widespread species of Echinacea (Asteraceae). Evolution 48: 180–181.[CrossRef][ISI]
Berger, E. 1975 Heterosis and the maintenance of enzyme polymorphism. American Naturalist 110: 823–839.[CrossRef][ISI]
Cheliak, W. M., and J. A. Pitel. 1984 Techniques for starch gel electrophoresis of enzymes from forest tree species. Information report PI-X-42. Petawa National Forestry Institute, Canadian Forestry Service, Agriculture Canada.
Clausen, J., D. D. Keck, and W. M. Hiesey. 1948 Experimental studies on the nature of species, III: Environmental responses of climatic races of Achillea. Carnegie Institution of Washingtion Publication 581: 1–129.
Crawford, D. J. 1983 Phylogenetic and systematic inferences from electrophoretic studies. In S. D. Tanksley and T. J. Orton [eds.], Isozymes in plant genetics and breeding, part a, 257–287. Elsevier Science, New York, NY.
———. 1985 Electrophoretic data and plant speciation. Systematic Botany 10: 405–416.[CrossRef][ISI]
Elkington, T. T. 1971 Biological flora of the British Isles: Dryas octopetala L. Journal of Ecology 59: 887–905.[CrossRef]
Federov, A. A. 1969 Chromosome numbers of flowering plants. Nauka, Leningrad, RUS.
Felsenstein, J. 1985 Phylogenies and the comparative method. American Naturalist 125: 1–15.
Freiley, K. J. 1994 Clonal diversity patterns in marginal populations of the geographically restricted shrub Neviusia alabamensis (Rosaceae). Southwest Naturalist 39: 34–39.[CrossRef]
Galen, C., J. S. Shore, and H. Deyoe. 1991 Ecotypic divergence in alpine Polemonium viscosum: genetic structure, quantitative variation, and local adaptation. Evolution 45: 1218–1228.[CrossRef][ISI]
Godt, M. J. W., and J. L. Hamrick. 1998 Allozyme diversity in the endangered pitcher plant Sarracenia rubra ssp. alabamensis (Sarraceniaceae) and its close relative S. rubra ssp. rubra. American Journal of Botany 85: 802–810.
———, B. Johnson, and J. L. Hamrick. 1996 Genetic diversity and population size in four rare southern appalachian plant species. Conservation Biology 10: 796–805.[CrossRef][ISI]
Gottlieb, L. D. 1973 Genetic differentiation, sympatric speciation, and the origin of a diploid species of Stephanomeria. American Journal of Botany 60: 545–553.[CrossRef]
———. 1974 Genetic confirmation of the origin of Clarkia lingulata. Evolution 28: 244–250.[CrossRef][ISI]
———. 1984 Genetics and morphological evolution in plants. American Naturalist 123: 681–709.[CrossRef][ISI]
Grant, M. C., and J. B. Mitton. 1977 Genetic differentiation among growth forms of Engelmann spruce and subalpine fire at tree line. Arctic and Alpine Research 9: 259–263.[CrossRef][ISI]
Hamrick, J. L., and M. J. W. Godt. 1990 Allozyme diversity in plant species. In H. D. Brown, M. T. Clegg, A. L. Kahler, and B. S. Weir [eds.], Plant population genetics, breeding, and genetic resources, 43–63. Sinauer, Sunderland, MA.
———, Y. B. Linhart, and J. B. Mitton. 1979 Relationships between life history characteristics and electrophoretically detectable genetic variation in plants. Annual Review of Ecology and Systematics 10: 173–200.
Hebert, P. D. N., and M. J. Beaton. 1989 Methodologies for allozyme analysis using cellulose acetate electrophoresis. Helena Laboratories, Beaumont, TX.
Hedrén, M. 1996 Allozyme variation and racial differentiation in Swedish Carex lepidocarpa s.l. (Cyperaceae). Biological Journal of the Linnean Society 59: 179–200.[CrossRef]
Hedrick, P. W. 1986 Genetic polymorphism in heterogeneous environments: a decade later. Annual Review of Ecology and Systematics 17: 535–566.[CrossRef][ISI]
Hultén, E. 1959 Studies in the genus Dryas. Svensk Botanisk Tidskrift 53: 507–542.
———. 1968 Flora of Alaska and neighboring territories; a manual of the vascular plants. Stanford University Press, Stanford, CA.
Jain, S. K., and A. D. Bradshaw. 1966 Evolutionary divergence among adjacent plant populations. I. The evidence and its theoretical analysis. Heredity 21: 407–441.[ISI]
Kihlman, A. O. 1890 Pflanzenbiol. Studien aus Russ. Lappland. Acta societatis pro fauna et flora Fennica. VI, 3.
Krogulevich, R. E., and T. S. Rostovtseva. 1984 Chromosome numbers of flowering plants of Siberia and the Far East. Nauka, Novosibirsk, Russia.
Löve, A., and D. Löve. 1975 Cytotaxonomical atlas of the arctic flora. J. Cramer, Vaduz, Lithuania.
Loveless, M. D., and J. L. Hamrick. 1984 Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15: 65–95.
McGraw, J. B. 1985a Experimental ecology of Dryas octopetala ecotypes: relative response to competitors. New Phytologist 100: 233–241.[CrossRef][ISI]
———. 1985b Experimental ecology of Dryas octopetala ecotypes III. Environmental factors and plant growth. Arctic and Alpine Research 17: 229–239.[CrossRef][ISI]
———. 1987a Experimental ecology of Dryas octopetala ecotypes. IV. Fitness response to reciprocal transplanting in ecotypes with differing plasticity. Oecologia 73: 465–468.[CrossRef][ISI]
———. 1987b Experimental ecology of Dryas octopetala ecotypes. V. Field photosynthesis of reciprocal transplants. Holarctic Ecology 10: 308–311.[ISI]
———, and J. Antonovics. 1983 Experimental ecology of Dryas octopetala ecotypes. I. Ecotypic differentiation and life-cycle stages of selection. Journal of Ecology 71: 879–897.[CrossRef][ISI]
Meizel, S., and G. L. Markert. 1967 Malate dehydrogenase isozymes of the marine snail Ilyanassa obsoleta. Archives of Biochemistry and Biophysics 122: 753–765.
Miller, P. C. 1982 Environmental and vegetational variation across a snow accumulation area in montane tundra in central Alaska. Holarctic Ecology 5: 85–98.
Mopper, S., J. B. Mitton, T. G. Whitham, N. S. Cobb, and K. M. Christensen. 1991 Genetic differentiation and heterozygosity in pinyon pine associated with resistance to herbivory and environmental stress. Evolution 45: 989–999.[CrossRef][ISI]
Moran, G. F., and S. D. Hopper. 1983 Genetic diversity and the insular population structure of the rare granite outcrop species, Eucalyptus caesia Benth. Australian Journal of Botany 31: 161–172.[CrossRef]
Murdy, W. H., and M. E. Brown Carter. 1985 Electrophoretic study of the allopolyploidal origin of Talinum teretifolium and the specific status of T. appalachianum (Portalucaceae). American Journal of Botany 72: 1590–597.[CrossRef][ISI]
Pleasants, J. M., and J. F. Wendel. 1989 Genetic diversity in a clonal narrow endemic, Erythronium propulans, and its widespread progenitor, Erythronium albidum. American Journal of Botany 76: 1136–1151.
Porsild, A. E. 1947 The genus Dryas in North America. Canadian Field Naturalist 61: 175–192.
Premoli, A. C., S. Chischilly, and J. B. Mitton. 1994 Levels of genetic variation captured by four descendant populations of pinyon pine (Pinus edulis Engelm.). Biodiversity and Conservation 3: 331–340.[CrossRef][ISI]
Purdy, B. G., and R. J. Bayer. 1995 Genetic diversity in the tetraploid sand dune endemic Deschampsia mackenzieana and its widespread diploid progenitor D. cespitosa (Poaceae). American Journal of Botany 82: 121–130.[CrossRef][ISI]
———, and ———. 1996 Genetic variation in populations of the endemic Achillea millefolium ssp. megacephala from the Athabasca sand dunes and the widespread ssp. lanulosa in western North America. Canadian Journal of Botany 74: 1138–1146.
———, and S. E. Macdonald. 1994 Genetic variation, breeding system evolution, and conservation of the narrow sand dune endemic Stellaria arenicola and the widespread S. longipes (Caryophyllaceae). American Journal of Botany 81: 904–911.[CrossRef][ISI]
Raup, D. M., and S. J. Gould. 1974 Stochastic simulation and the evolution of morphology-towards a nomothetic paleontology. Systematic Zoology 23: 305–322.[CrossRef][ISI]
Rieseberg, L. H., and D. Gerber. 1995 Hybridization in the Catalina Island Mountain Mahogany (Cercocarpus traskiae): RAPD evidence. Conservation Biology 9: 199–203.[CrossRef][ISI]
Ritchie, J. C., and L. C. Cwynar. 1982 The late quaternary vegetation of the north Yukon. In D. M. Hopkins, J. V. Matthews, C. E. Schweger, and S. B. Young [eds.], Paleoecology of Beringia, 113–126. Academic Press, New York, NY.
Rogers, J. S. 1972 Measures of genetic similarity and genetic distance. Studies in Genetics VII, University of Texas Publication 7213: 145–153.
SAS. 1990 SAS/STAT user's guide, version 6, 4th ed. SAS Institute, Cary, NC.
———. 1997 SAS/STAT software: changes and enhancements through release 6.12. SAS Institute, Cary, NC.
Schaal, B. A., and W. G. Smith. 1980 The apportionment of genetic variation within and among populations of Desmodium nudiflorum. Evolution 234: 214–221.
Schwaegerle, K. E., and B. A. Schaal. 1979 Genetic variability and founder effect in the pitcher plant Sarracenia purpurea L. Evolution 33: 1210–1218.[CrossRef][ISI]
Shaw, A. J., and R. E. Schneider. 1995 Genetic biogeography of the rare "copper moss", Mielichhoferia elongata (Bryaceae). American Journal of Botany 82: 8–17.[CrossRef][ISI]
Sherman-Broyles, S. L., J. P. Gibson, J. L. Hamrick, M. A. Bucher, and M. J. Bucher. 1992 Comparisons of allozyme diversity among rare and widespread Rhus species. Systematic Botany 17: 551–559.[CrossRef][ISI]
Soltis, D. E., C. H. Haufler, D. C. Darrow, and G. J. Gastony. 1983 Starch gel electrophoresis of ferns: a compilation of grinding buffers, gel and electrode buffers, and staining schedules. American Fern Journal 73: 9–27.[CrossRef][ISI]
Swofford, D. L., and R. B. Selander. 1981 BIOSYS-1: a computer program for the analysis of allelic variation in genetics. University of Illinois, Urbana, IL.
Tikhmenev, E. A. 1985 Pollination and self-pollinating potential of entomophilic plants in arctic and mountain tundras of the northeastern USSR. Soviet Journal of Ecology 15: 166–172. (Translation from original Russian: 1984. Ekilogiya 4: 8–15).
Viereck, L. A., C. T. Dyrness, A. R. Batten, and K. J. Wenzlick. 1992 The Alaska vegetation classification. General Technical Report PNW-GTR-286. U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station, Portland, OR.
Wendel, J. F., and N. F. Weeden. 1989 Visualization and interpretation of plant isozymes. In D. E. Soltis and P. E. Soltis [eds.], Isozymes in plant biology, 5–45. Dioscorides Press, Portland, OR.
Workman, P. L., and J. D. Niswander. 1970 Population studies on southwestern Indian tribes. II. Local genetic differentiation in the Papago. American Journal of Human Genetics 22: 24–49.[ISI][Medline]
Wright, S. 1978 Evolution and the genetics of populations. Volume 4. Variability within and among natural populations. University of Chicago Press, Chicago, IL.
Young, A., T. Boyle, and T. Brown. 1996 The population genetic consequences of habitat fragmentation for plants. Trends in Ecology and Evolution 11: 413–418.[CrossRef]
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