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Population Biology |
2Department of Geography, The University of Georgia, Athens, Georgia 30602 USA; 3Departments of Botany and Genetics, The University of Georgia, Athens, Georgia 30602 USA; 4Department of Botany, University of Kansas, Lawrence, Kansas 66045 USA
Received for publication April 27, 2001. Accepted for publication December 11, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: allozymes • biogeography • genetic diversity • Pinaceae • Pinus flexilis • population genetics • western North America
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Hamrick, Godt, and Sherman-Broyles, 1992
). Furthermore, gymnosperms as a group, and conifers in particular, have a circumboreal distribution, and the distributions of many species have been affected by Pleistocene glacial advances.
Pinus flexilis James (limber pine) is the most widespread white pine in western North America. The species occurs from the Canadian Rocky Mountains to northern Arizona and New Mexico and across the Great Basin into eastern California; additionally, numerous isolated populations are scattered from North Dakota to Oregon to southern California (Fig. 1). Within its range, P. flexilis occurs over a wide variety of elevations and substrates, although it is primarily found in upper montane to subalpine zones or in drier, windswept sites at lower elevations (Steele, 1990
). Despite the wide ecological and geographic range of P. flexilis, almost no trends for quantitative trait variation have been found (Steinhoff and Andresen, 1971
). A study of xylem monoterpenes did suggest that populations in the extreme southwestern portion of the range were distinct from other populations (Zavarin, Kool, and Snajberk, 1993
); however, no subspecies or varieties of P. flexilis are recognized (Steele, 1990
). In contrast, P. ponderosa Dougl. ex Laws. (ponderosa pine), which, like P. flexilis, occurs over a wide area, has three geographically defined varieties, ‘Pacific Coast’, ‘Rocky Mountain’, and ‘Arizona’ (Oliver and Ryker, 1990
). At least five geographic races have been described for P. contorta Dougl. ex Loud. (lodgepole pine) (Lotan and Critchfield, 1990
).
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; Wells and Stewart, 1987
); the current distribution of the species may have been derived from a number of Pleistocene-era populations. In fact, one analysis of mitochondrial DNA suggests that P. flexilis differentiated in several refugia (Mitton, Kreiser, and Latta, 2000
), although the study did not include many samples from the Northern Rocky Mountains. Given that P. flexilis had multiple populations during the Wisconsin glacial period, there may be significant variation in genetic diversity over its range, and the patterns would likely reflect both the location and the relative size of the glacial populations.
Patterns of genetic diversity in P. flexilis may also be affected by dispersal of its seeds by birds. Clark's nutcrackers (Nucifraga columbiana Wilson; Corvidae) harvest ripening seeds, placing them in numerous shallow soil caches (Tomback and Linhart, 1990
). Although the pinyon jay (Gymnorhinus cyanocephalus Wied; Corvidae) may have been the primary disperser responsible for the development of the large, wingless seeds of P. flexilis (Lanner, 1980
), today Clark's nutcracker is the only systematic mechanism for the species' regeneration (Lanner, 1984
). At the local or stand level, seed dispersal by nutcrackers may have profound consequences. Perhaps most obvious is the multi-trunk architecture common in many stands of P. flexilis. Multi-trunk trees are created when multiple seeds in a cache germinate. Linhart and Tomback (1985) demonstrated that such trees often consist of several genetically unique stems ("tree clusters"). Individuals within tree clusters tend to be related on the order of half to full sibs, while individuals from different clusters are unrelated (Schuster and Mitton, 1991
; Carsey and Tomback, 1994
). These results are virtually identical to those found for P. albicaulis Engelm. (Furnier et al., 1987
; Rogers, Millar, and Westfall, 1999
), the other pine species in North America whose regeneration is solely dependent on seed dispersal by Clark's nutcracker. Nutcrackers have been observed to disperse seeds as far away as 22 km (vander Wall and Balda, 1977
), although distances of several hundred meters are probably more common (Mitton, Kreiser, and Latta, 2000)
. Nevertheless, at both local and landscape scales, seed dispersal by Clark's nutcracker may result in widespread and unpredictable patterns of gene flow (Tomback and Linhart, 1990
).
We used allozyme loci to examine the population genetics of P. flexilis. Our objectives were to (1) determine the amount and distribution of genetic diversity within and among populations, (2) identify patterns of variation among geographic regions occupied by the species, especially postglacial migration and establishment patterns, and (3) compare the results for P. flexilis with the population genetics of other pines with similar western North American distributions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Small chromatography-paper wicks were used to absorb the crude extract and were placed in microtest plates for storage at –70°C.
Electrophoresis was conducted with 10% starch gels. Four buffer systems were used to resolve 21 putative loci representing 12 enzyme systems. d-Aspartate aminotransferase (Aat-1, Aat-2) and glutamate dehydrogenase (Gdh) were resolved with buffer system H; aldolase (Ald), isocitrate dehydrogenase (Idh), and 6-phosphogluconic dehydrogenase (6Pgd-1, 6Pgd-2) were resolved with buffer system 4; fluorescent esterase (Fe-1, Fe-2, Fe-3), malic enzyme (Me), phosphoglucomutase (Pgm-1, Pgm-2), phosphoglucoisomerase (Pgi-1, Pgi-2), shikimate dehydrogenase (Skdh), and triose-phosphate isomerase (Tpi-1, Tpi-2) were resolved with buffer system 34/40; malate dehydrogenase (Mdh-1, Mdh-2, Mdh-3) was resolved with buffer system 5. Recipes for all enzyme stains and buffer systems were adapted from Soltis et al. (1983)
with the exceptions of buffer system H, which was a modification of buffer system B from Conkle et al. (1982)
, and buffer system 34/40, which was from Mitton et al. (1979)
. Loci were designated with numbers placed after the enzyme abbreviations; lower numbers indicate faster-migrating loci. An analogous system was used to label individual alleles at each polymorphic locus.
Statistical analyses
The following standard measures of genetic variation were calculated at the species (noted by the subscript "s") and population levels (subscript "p"): percentage of polymorphic loci (PL; a locus was considered polymorphic if more than one allele was present), mean number of alleles per polymorphic locus (A), observed heterozygosity (Ho), and expected heterozygosity or genetic diversity (He = 1 – 
p2i, where pi = frequency of the ith allele at a locus). In addition, Weir and Cockerham's (1984)
parameter f(FIS), a measure of inbreeding within populations, was calculated for each population. Observed heterozygote frequencies were compared to Hardy-Weinberg expectations for each polymorphic locus in each population using Wright's fixation index, F = 1 –Ho/He (Wright, 1922
). Significance from the expected value of F = 0 was determined with a chi-square analysis, where 
2 = NF2(a – 1), with degrees of freedom (df) = a(a – 1)/2, N being the total sample size, and a = the number of alleles at a locus (Li and Horvitz, 1953
).
To examine broad geographic trends in genetic diversity, we classified according to four geographic regions: Northern Rocky Mountains, Utah Rocky Mountains, Basin and Range, and Colorado Rocky Mountains. Regional averages were calculated for PL, A, He, and f. An analysis of variance (ANOVA) was conducted to examine whether significant regional variation was found in these parameters, exclusive of the Colorado Rocky Mountains, from which only two populations were sampled. If significant regional variation was indicated by the ANOVA, Fisher's protected least significant difference (LSD) procedure was used to determine which groups were significantly different in their mean values.
Genetic variation among populations was analyzed several ways. First, genetic structure was investigated via Nei's (1973)
measures of genetic diversity, which include total genetic diversity (i.e., heterozygosity) at a polymorphic locus (HT), mean genetic diversity within populations (HS), and the proportion of genetic diversity occurring among populations (GST = [HT – HS]/HT). Second, Weir and Cockerham's (1984)
estimates of Wright's (1965)
F statistics were generated for each polymorphic locus. Significant deviations from the null expectation of F = 0 were determined by 500 bootstrap replicates; calculations were done with the program FSTAT (Goudet, 1995
). In the bootstrap analysis, F (corresponding to Wright's FIT) was estimated by alleles permutated among populations, f (FIS) was estimated by the permutation of alleles within samples, and 
(FST) was estimated by the permutation of alleles among samples or, if the results of f were significant, genotypes were permutated among samples. Third, Hillis's (1984)
modification of Nei's (1972)
genetic distance was calculated among all pairs of populations. The relationship of genetic distance to geographic distance between populations was analyzed with a Mantel test (Mantel, 1967
). Finally, genetic distance data were used to analyze the relationship among populations with two phenetic analyses. An unweighted pair-group clustering based on arithmetic averages (UPGMA) was completed with the program NTSYS-pc (Rohlf, 1993
). A two-dimensional representation of population genetic distances was generated with the iterative procedure multidimensional scaling (MDS). The MDS was conducted with the function PROC MDS in SAS (SAS, 1997
), which uses an algorithm to generate an initial configuration of populations. Correlations between genetic distances as portrayed in the phenetic analyses and actual genetic distances among populations were also determined.
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RESULTS |
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Individual populations averaged 64.2% polymorphic loci. Values of PLp ranged from 47.6% (populations 14 and 22) to 81.0% (populations 2, 27, and 30). The mean number of alleles per polymorphic locus within populations was 2.46 and varied little among populations. Genetic diversity within populations (Hep) varied substantially, ranging from 0.120 (population 7) to 0.219 (population 18); mean expected heterozygosity was 0.166. Observed heterozygosity was less than expected in 25 of 30 populations, as was the overall mean (f = 0.097), although a high degree of variation in the magnitude of f was seen among populations. Of 400 chi-square tests for individual loci within populations, 62 (15.5%) deviated significantly from the expected value of F = 0, and all but two were in the direction of heterozygote deficiency; this result is approximately three times the number of significant deviations expected on the basis of chance alone (P < 0.05).
Distribution of genetic variability among populations
Approximately 10% of the genetic diversity within P. flexilis was distributed among populations (GST = 0.101) (Table 2). Excluding Mdh-3 and Tpi-1, values for individual loci varied from 0.027 (Aat-1) to 0.261 (Gdh), both loci with a low level of heterozygosity (HT). Among those loci with HT 
0.1, the mean GST was 0.096.
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, > 0); these deviations are tempered by the large sample sizes in this study, however.
The mean genetic distance (Hillis, 1984
) among populations was 0.0281. The least genetic distance between populations, D = 0.0019, was between population pairs 9–10 and 9–23, and the greatest genetic distance (0.0947) was between populations 17 and 30. Among all population pairs, a weak, but significant, relationship was found between genetic and geographic distance (r = 0.290, Mantel's t = 2.595, P = 0.005). A significant correlation (r = 0.290, t = 2.195, P = 0.014) was also seen in the 15 combined Northern and Utah Rocky Mountain populations, which form a rather continuous north-south distribution. Conversely, no significant relationship between geographic and genetic distance was seen among the 13 Basin and Range populations (r = 0.173, t = 1.146, P = 0.126).
Two UPGMA clustering solutions were identified (Fig. 2), but the solutions varied only for the relationships among populations 9, 10, and 23. The correlation between distances as portrayed in the phenogram and actual genetic distances (cophenetic correlation) for the phenogram was r = 0.717, indicative of a poor fit (Rohlf, 1993
). Three groups were apparent when mean genetic distance was used as a guideline for identification. The first group included populations from Montana, a single Canadian population, and the two Colorado Rocky Mountain populations. A second group consisted of two main clusters that joined below the mean genetic distance value. The smallest cluster comprised three populations, two from southern Idaho and one from Canada; the other cluster contained the Utah Rocky Mountain populations and all but two of the Basin and Range populations. In the last group were two Basin and Range populations that joined above mean genetic distance; these populations (17 and 18) were separated by a geographic distance of less than 150 km. The correlation between genetic distance and distance as portrayed in the MDS analysis (Fig. 3) was r = 0.936, indicating a very good portrayal of the relationships among populations. While the overall pattern was similar to the UPGMA analysis, further relationships were illuminated by the MDS analysis. For example, populations from the Utah Rocky Mountains and the Basin and Range regions intermingle in the UPGMA phenogram; in the MDS analysis, however, it is clear that the Utah Rocky Mountain populations are nested within the Basin and Range populations and that the Basin and Range populations have the greatest variation among them.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), its genetic diversity value is typical of those reported for other pine species that are widespread in western North America, such as ponderosa pine (P. ponderosa) and western white pine (P. monticola Dougl. ex D. Don) (Table 3). When the disjunct nature of P. flexilis populations is considered, however, these results are somewhat surprising. Typically, plant species with disjunct, montane ranges have less genetic diversity within their populations and more genetic diversity among populations than more widespread species with similar life histories (Hamrick and Godt, 1996
; Berg and Hamrick, 1997
).
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; Porter, Pierce, and Hamilton, 1983
). Pleistocene populations in much of the northern Rocky Mountains were likely smaller, more isolated, and at much lower elevations than modern populations of P. flexilis in this region; furthermore, current populations in the previously heavily glaciated northern areas must have been colonized by seeds from distant populations dispersed by Clark's nutcracker following glacial retreat. Each population must have been established by relatively large numbers of seeds because genetic diversity is not greatly reduced in populations from this region. Genetic data also suggest both an eastern and western source for current populations in the northern Rocky Mountains of the United States.
In contrast to the northern Rocky Mountains, the Basin and Range area was virtually free of ice during the Wisconsin glaciation (Porter, Pierce, and Hamilton, 1983
). Abundant macrofossil evidence confirms the presence of P. flexilis at numerous sites in the Great Basin (Wells, 1983
; Betancourt, 1990
), and the region likely supported large populations at elevations approximately 500 m lower than where populations occur today. Rather than being established by seeds from outside areas, present-day populations of P. flexilis in the Basin and Range may be descended directly from the extensive Wisconsin stage populations in the same mountain ranges. The high genetic diversity found in current Basin and Range populations (mean He = 0.178) and the large genetic distances separating some populations support the conclusion that a number of large Wisconsin populations once existed in the area (relative to other Wisconsin populations, if not the current distribution). For example, populations 17 and 18, which are located less than 150 km from each other in northeastern Nevada, have the highest levels of genetic diversity among all populations. The genetic distance among these populations, however, is well above the mean genetic distance among population pairs (Fig. 2), a finding that suggests these populations have long been separated. Topographic evidence indicates that population 17 could never have been in contact with any other population (Wells, 1983
).
Large, continuous populations of P. flexilis may have also been present in the western Great Plains during the Pleistocene. Wells and Stewart (1987)
argue that the widely disjunct populations of P. flexilis in eastern Colorado, Wyoming, and South Dakota are relicts of Pleistocene populations that grew throughout the plains. Because we sampled only two populations from the Colorado Rocky Mountains, it is difficult to make regional inferences here, but genetic diversity in these two populations is relatively high. Given that Great Plains populations may have been the source of the current Colorado populations, high levels of genetic diversity in the Colorado Front Range populations are consistent with an extensive distribution in the plains during the Pleistocene. On the basis of geographic considerations and genetic distance measures (Figs. 2, 3), the northern Rocky Mountain populations east of the U.S. continental divide appear to have been colonized by seeds from the large Great Plains Wisconsin age populations that also gave rise to the Colorado Rocky Mountain populations. These patterns are consistent with those reported by Mitton, Kreiser, and Latta (2000)
, although they sampled only two northern Rocky Mountain populations, both from Canada. Populations in the northern Rocky Mountain sites west of the divide and populations in the Utah Rocky Mountains, which had the lowest mean PLp and He values, have their closest genetic affinities to the Basin and Range populations. Interestingly, the east-west dichotomy in the northern Rocky Mountains is reversed for the Canadian populations, where the range of P. flexilis narrows to the spine of the Rocky Mountains. Because these populations would have been established by long-distance seed dispersal, our data indicate that the east-west contact zone spans the width of the species' range in the Canadian Rockies and also that there was little gene flow subsequent to establishment of the populations.
Genetic data and fossil evidence both indicate that populations of P. flexilis in some portions of its range may have been substantially larger during the Wisconsin stage than today. Consequently, while the concept of glacial refugia and restricted population sizes may be accurate for areas from which P. flexilis was entirely displaced during the Wisconsin, the idea does not hold for the Great Basin and Great Plains regions. How then to explain the low variation in mitochondrial DNA in Great Basin populations found by Mitton, Kreiser, and Latta (2000)
, a result that is consistent with constricted populations in the area? We suggest that this low level of variation may reflect the footprint of older glaciations. The Wisconsin glaciation was only the most recent of a number of glacial advances in North America during the Pleistocene. The Illinoian glacial period, which preceded the Wisconsin, had the greatest extent of Pleistocene glaciation (Cornwall, 1970
; Tage, 1983
). While few mountain ranges in northeastern Nevada were glaciated during the Wisconsin, more may have been present during the Illinoian, and populations of P. flexilis would have been forced farther downslope. Given that most of the closed basins in the northern portion of Nevada and most of western Utah contained paleolakes during glacial periods (Smith and Street-Perrott, 1983
), P. flexilis may have been squeezed out of many areas of the northern Great Basin where it later survived during the Wisconsin glacial period.
Virtually all the populations (>93%) we sampled had an overall deficiency of heterozygotes, although the magnitude of f varied substantially among populations. These results are somewhat unexpected because pines, being wind-pollinated, have high rates of outcrossing (Brown, Barrett, and Moran, 1985
). In fact, most adult populations of conifers are in Hardy-Weinberg proportions or have a heterozygote excess, and inbreeding due to self-fertilization is usually seen only in embryos and young trees (Bush and Smouse, 1992
). Population substructuring (i.e., the Wahlund effect) could explain these patterns; however, this seems unlikely given that, apart from multigenotype tree clusters, no kin structuring is apparent within populations (Carsey and Tomback, 1994
). Inbreeding was greatest in the Basin and Range region, where populations are restricted to isolated stands at high elevations. These populations may have experienced recent population bottlenecks resulting in a higher degree of relatedness among individuals. Biparental inbreeding could also be facilitated by matings between related individuals within tree clusters (Jorgensen and Hamrick, 1997
).
Compared with most pines, P. flexilis had about 50% more of its genetic diversity distributed among populations (GST = 0.101 for P. flexilis vs. 0.065 for the typical pine [Hamrick, Godt, and Sherman-Broyles, 1992
]). This pattern is consistent with that of other pines with naturally disjunct geographic distributions (Hamrick and Godt, 1996
). The amount of genetic diversity distributed among P. flexilis populations is intermediate between that for P. monticola (GST = 0.148) and P. albicaulis (GST = 0.034), two other white pine species widely distributed in the mountains of western North America. Pinus flexilis occurs over a much wider elevational gradient than P. albicaulis, which is restricted to subalpine areas; thus, P. flexilis may have more opportunities for localized adaptation. Also, the pollen phenology of P. flexilis is strongly affected by elevation. In a study of Colorado populations, Schuster, Alles, and Mitton (1989)
found that sites separated by >400 m elevation did not have overlapping pollination periods and that pollen flow was restricted to a stepping-stone pattern along elevational gradients. Yet a study by Latta and Mitton (1997)
of seven locations in and just outside of Colorado indicates pollen flow, even though restricted among populations at varying altitudes, may be the main mechanism for gene flow among modern populations.
The results of previous studies of P. flexilis (Latta and Mitton, 1997
; Mitton, Kreiser, and Latta, 2000
) indicate that modern patterns of genetic diversity can be the result of many refugial locations plus modern gene dispersal among established populations. Our results support this conclusion. Genetic structure was lowest in the Utah Rocky Mountains, where the species has a generally continuous north-south distribution; also, there was a significant relationship between geographic and genetic distances among the Northern and Utah Rocky Mountain populations. Relatively recent establishment and one-dimensional, north-south gene flow likely characterize northern Rocky Mountain populations. In contrast, we found no relationship between geographic and genetic distances among populations in the Basin and Range region, which also had the greatest genetic heterogeneity among populations. Thus, while gene flow may be two-dimensional in the Basin and Range region, the magnitude of gene flow among populations is less. This observation reflects the isolated nature of populations in this region and is consistent with that for several other conifer species in the region (Hamrick, Schnabel, and Wells, 1994
). Small, isolated populations, which may be more dominated by drift, may consist of individuals that are more related to one another than expected by chance. Furthermore, the Basin and Range populations may have been continuously isolated throughout the last glacial advance, since the available paleoecological evidence (Wells, 1983
) indicates that the Basin and Range populations experienced shifts only in elevation. The current Basin and Range populations probably resulted directly from the upward expansion of local populations present during the Wisconsin stage rather than from a single glacial refugium, which may have characterized other geographic regions (e.g., Colorado Rocky Mountains).
In conclusion, our results indicate that current patterns of genetic diversity throughout the range of P. flexilis are complex and have probably resulted from the interaction of three factors: the geographic distribution of Pleistocene populations, the long-distance dispersal of seeds by birds following glacial retreats, and the recent gene flow by means of pollen and seeds.
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FOOTNOTES |
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5 Author for reprint requests (hamrick{at}dogwood.botany.uga.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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); Utah Rocky Mountains (+); Basin and Range (•); and Colorado Rocky Mountains (
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