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Population Biology |
2Department of Biology, St. Olaf College, Northfield, Minnesota 55057 USA; 3Department of Plant Biology, University of Minnesota, St. Paul, Minnesota 55108 USA
Received for publication August 14, 2001. Accepted for publication November 20, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Abies balsamea • allozymes • balsam fir • gene flow • genetic variation • habitat fragmentation • Pinaceae • small population size • spatial autocorrelation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Frankham, 1998
). Isolated populations of widespread species can serve as models of the likely effects of decreased population size due to habitat fragmentation. It is generally thought that populations near the center of a species' range are contiguous and genetically diverse, whereas marginal populations are isolated, smaller, and less genetically variable (Hamrick, Blanton, and Hamrick, 1989
). Theory predicts that the smaller the population, the more rapid the loss of genetic variability due to genetic drift (Wright, 1969
). Reduced genetic variability may also result from severe selection in ecologically marginal habitats and from the stochastic effects of long-distance dispersal during species migration (Cwynar and MacDonald, 1987
; Levin, 1988
).
Balsam fir (Abies balsamea (L.) Mill.), found in northeastern North America, has the distribution pattern of a wide-ranging common species, with a continuously inhabited central area and isolated populations on the periphery. This pattern makes balsam fir ideal for population genetic studies on the effects of habitat fragmentation. The central part of the range occurs in the boreal and mixed hardwood–coniferous forests of southeastern Canada and the northeastern United States as far west as Minnesota. The isolated populations occur in what has been called the Driftless Area of southeastern Minnesota and northeastern Iowa. Balsam fir is thought to have migrated north and west from refugia in the Appalachian Mountains following Pleistocene glaciation (Bakuzis and Hansen, 1965
). Commercially, balsam fir is primarily of interest for pulpwood, Christmas trees, and wildlife habitat.
This study focuses on a comparison of two ecologically central populations from the Sylvania Wilderness Area in western Upper Michigan with two isolated populations, one in southeastern Minnesota and one in northeastern Iowa. The Sylvania Wilderness Area consists of a mosaic of old-growth mixed hardwood and conifer forests established on a glacial moraine deposited 12 000 yr BP (Davis et al., 1994
). The hardwood forests are dominated primarily by sugar maple (Acer saccharum Marsh.), while the conifer forests are dominated by hemlock (Tsuga canadensis (L.) Carr.). Balsam fir in the Sylvania Wilderness Area is usually associated with hemlock. Pollen studies (Frelich, Calcote, and Davis, 1993
; Davis et al., 1994
) have shown that hemlock migrated into the area, previously dominated by white pine (Pinus strobus L.), oak (Quercus), and maple (Acer), from the east about 3000 yr BP as conditions became cooler and moister. The westward expansion of hemlock corresponds with a regional increase in spruce (Picea) and fir pollen, interpreted as evidence for cooler, moister conditions (Davis, 1987
).
Balsam fir is also found south of its continuous range in northeastern Iowa and southeastern Minnesota in a region with karst topography. Stream erosion during the Wisconsin glacial period, 20 000–17 000 BP formed the topographic relief currently found in the region (Hallberg, Bettis, and Prior, 1984
). Fir pollen and macrofossils have been found dating from 10 000 to 8000 yr BP in northeastern Iowa (Baker et al., 1996
). Today, balsam fir in this area grows in isolated populations on steep north-facing algific talus slopes. These slopes have a unique buffered microclimate in which soil temperatures rarely exceed 15°C in the summer because of cold-air flows from ice-filled caves under the slope (Frest, 1982
; Nekola, 1999
). Algific talus slopes have a number of disjunct boreal and endemic plant species and several rare snail species. They are thought to be paleorefugia containing relict populations from boreal spruce forests that survived south of the Pleistocene glaciers (Wright, 1981
; Frest, 1982
).
Studies of genetic variation have shown that forest trees, especially conifers, generally have higher levels of genetic variability than other plants (Hamrick, Godt, and Sherman-Broyles, 1992
) because of life history characteristics such as wind pollination, high levels of outcrossing, high fecundities, long generation time, and large geographic range. Studies of other Abies species have found lower than expected levels of genetic variation (Matusova, 1995
; Suyama, Tsumura, and Ohba, 1997
; Aguirre-Planter, Furnier, and Eguiarte, 2000
), results that are explained by migration patterns, historical events, or small population size. Little previous work has been done on the population genetics of balsam fir. Jacobs, Werth, and Guttman (1984)
found that A. balsamea and A. fraseri (Pursh) Poir. (Fraser fir), from the Appalachian Mountains, are closely related taxa of Pleistocene origin. Neale and Adams (1985)
found no significant differences in allele frequences in balsam fir along an elevational transect in New Hampshire, but documented lower outcrossing rates at the high-elevation site. Diebel and Feret (1991)
found no significant differences in gene frequencies and little or no genetic substructuring among three subpopulations of A. fraseri on Mount Rogers, Virginia.
Because population genetics studies have shown that most of the genetic variation in tree species occurs within populations, patterns of genetic variation on a microgeographic scale need to be examined to better understand microgeographic evolution and to develop genetic conservation and breeding programs. Evidence of genetic substructure within populations has been found in some studies (Linhart et al., 1981
; Knowles, 1984
; Furnier et al., 1987
; Shea, 1990
), but not others (Guries and Ledig, 1977
; Roberds and Conkle, 1984
; Epperson and Allard, 1989
; Knowles, 1991
). Spatial structuring may be influenced by microenvironmental heterogeneity, leading to spatially varying selection pressures, and by seed dispersal patterns (Perry and Knowles, 1991
; Epperson, 1993
; Chung and Epperson, 1999
). In this study the genetic substructure within populations was examined using spatial autocorrelation analysis, a statistical procedure designed to detect and quantify spatial dependency in a variable (in this case, allele frequency) on the basis of sampled values from mapped locations (Sokal and Oden, 1978a, b
; Cliff and Ord, 1981
).
The purpose of the current study is to analyze the genetic structure of balsam fir both within and among populations in order to better understand the evolutionary processes that have shaped this species and may affect it in the future. More specifically, this study used allozymes to (1) estimate levels of genetic variation for balsam fir, (2) compare genetic variation of balsam fir in central and isolated populations, and (3) examine the spatial structure of genetic variation within populations of balsam fir.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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5 cm).
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; Davis et al., 1994
). At Sylvania, the balsam fir studied were in plots approximately 5 ha in size, while in the isolated populations, plot size was approximately 0.5 ha. Density comparisons among sites showed a lower fir density in the old-growth sites (15 trees/ha in SYB; 16 trees/ha in SYC; 351 trees/ha in MMH; 150 trees/ha in BSC). Plots in Sylvania had both hardwoods and conifers, whereas plots in the isolated populations were located in areas where balsam fir was in the canopy and the understory comprised mountain maple (Acer spicatum Lam.) and yew (Taxus canadensis Marsh.) at MMH and sugar maple at BSC. Comparisons of mean fir diameter (13.6 cm in SYB; 15.7 cm in SYC; 15.4 cm in MMH; 9.9 cm in BSC) using anaylsis of variance (ANOVA) showed significant differences (p 
0.001) among the sites. Post hoc pairwise comparisons revealed that trees at BSC were significantly smaller (p 0.05) than those in the other three populations and that the two Sylvania populations were significantly (p 0.05) different in diameter. Few seedlings were seen in the isolated populations, while seedling establishment was more common in the old-growth forest sites.
At each site, needle and bud tissue was collected from 71–96 mature trees (5 cm DBH). Foliage samples were numbered, placed in plastic bags, and stored in an ice-filled cooler. Samples were kept in cold storage until processed, for up to several months. The enzyme polymorphism data were obtained with standard starch gel electrophoresis. The same loci could be scored on both bud and needle tissue; bud tissue was used because it provided clearer bands. (For the few trees that did not have buds, needle tissue was used instead.) Four buds were dissected from each tree and placed in several drops of a buffer that was 75% Yeh and O'Malley (1980)
extraction buffer and 25% vegetative extraction buffer II (Cheliak and Pitel, 1984
). Buds were homogenized with a plastic pestle attached to an electric drill. Needle tissue was processed using the methods of Mitton, Sturgeon, and Hamrick (1979)
. Twenty-two loci representing 17 enzyme systems were scored using three running buffers on 12% starch gels. Colorimetric esterase (Est-1), peroxidase (Per-2), phosphoglucose isomerase (Pgi-1, Pgi-2), and triosephosphate isomerase (Tpi-1, Tpi-2) were scored on the tris-citric acid buffer of Mitton et al. (1977)
. Aspartate aminotransferase (Aat-1, Aat-2), glutamate dehydrogenase (Gdh-1), leucine-amino peptidase (Lap-1, Lap-2), and peptidase (Pep-2) were scored on the tris-citric acid system of Ridgeway, Sherburne, and Lewis (1970)
. Aconitase (Aco-1), aldolase (Ald-1), glyceraldehyde-3-phosphate dehydrogenase (G3Pdh-1), isocitrate dehydrogenase(Idh-1), malate dehydrogenase (Mhd-1), phophoglucomutase (Pgm-1), 6-phosphogluconate dehydrogenase-2 (6Pgd-2), shikimate dehydrogenase (Skdh-1), and uridine-5' diphosphogluconase (Ugpp-1, Ugpp-3) were scored on the histidine buffer (H) of Cheliak and Pitel (1984)
. Data are reported for loci that had consistent, clearly interpretable banding patterns. Mendelian inheritance patterns have been documented for some of these loci (Neale and Adams, 1981
), and the patterns of other loci are consistent with patterns found in other conifers (Cheliak and Pitel, 1984
). A locus was considered polymorphic if two or more alleles were detected, regardless of frequency.
Genetic variation was analyzed using the program BIOSYS-1 (Swofford and Selander, 1981
). The mean number of alleles per locus, the percentage of polymorphic loci, and the mean observed and expected heterozygosity were computed. Genetic structure among and within populations was analyzed with chi-square tests, F statistics, and Nei's genetic distance and genetic identity (Wright, 1965
; Nei, 1977, 1978
). FST measures the amount of genetic variation due to differentiation among populations, FIS measures the effects of nonrandom mating within populations, and FIT measures the departure from Hardy-Weinberg equilibrium over all populations. Deviations of values of FIS and FIT from zero were tested with chi-square tests (Nei, 1977
; Neel and Ward, 1972
).
The degree of genetic isolation among populations was estimated by Nm, the number of migrants per generation. Nm was estimated from FST (Wright, 1951
; Slatkin and Barton, 1989) as follows: Nm = (1 – FST)/4FST, where FST is the proportion of the total genetic diversity among populations. An alternate method (Slatkin, 1985
) could not be used because the populations had no private alleles.
Spatial autocorrelation of alleles in each site was characterized by calculating Moran's I statistics (Sokal and Oden, 1978a
; Cliff and Ord, 1981
) using the Spatial Autocorrelation Analysis Program (SAAP) version 4.3 (Exeter Software, Setauket, New York, USA) developed by Daniel Wartenberg. Loci with allele frequencies less than 0.02 were excluded, and only one allele was considered at each locus because all loci were diallelic and the second allele would have contributed identical information. Genotypic data were coded so that allele frequency values of 0.0, 0.5, or 1.0 were assigned to individuals for one allele of each locus. All possible pairs of individuals were considered as joins and assigned to one of eight distance classes. The ranges of each distance class were determined by allocating an equal number of samples to each class, a procedure that results in favorable statistical properties (Epperson, 1993
). Moran's I was estimated for each of eight distance classes at each site. Each I value was tested for significant deviations from expected values, E[I] = –1/(N – 1) under the null hypothesis of a spatially random distribution (Cliff and Ord, 1981
), where N = number of individuals. Values of I significantly greater than the expected value indicated greater similarity of gene frequencies of individuals within that distance class than would be expected by chance, while values of I significantly lower than the expected I indicated less similarity among gene frequencies of individuals within that class than would be expected by chance. The significance of the correlogram, the set of I values for each locus constructed from a series of nonindependent I values, for each locus was determined using Bonferroni's criterion (Sakai and Oden, 1983
). A correlogram of the mean I value from each distance class, plotted as a function of distance for each site, allowed for visual examination of the variation in genetic spatial structure.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.99. One locus (Aat-2) was polymorphic in the population at Big Spring Cliff, and two loci (6Pgd-2, and Pgi-2) were polymorphic in the population at Mountain Maple Hollow. None of the polymorphic loci were variable at all four sites, and chi-square tests showed significant differences in allele frequencies among the four sites overall and for each of the four most variable loci (Table 1). In all populations alleles for the variable loci had either low or high frequencies.
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2, p 0.05) because there were fewer heterozygotes than expected.
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0.01) positive mean FIS value (0.154), suggesting a significant deficit of heterozygotes due to inbreeding within populations (Table 3). When individual loci were examined, three had positive FIS values and six had small negative FIS values; only Aat-2 was significantly different from zero. Heterogeneity among populations as measured by mean FST (0.037) was also significant (p 0.01) and indicated that 3.7% of the total genetic variation was due to differences among populations and 96.3% of the total genetic variability was found within populations. Four individual loci (Pgi-2, Aat-2, Ugpp-3, and 6Pgd-2) had significant FST values.
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), which showed little differentiation between pairs of sites. In all instances D = 0.001 except between the two Sylvania sites, where D = 0.000. Nm, the number of migrants per generation, estimated from FST, was 6.5. This value suggests some recent gene flow, recent separation, and/or relatively small genetic differences among the populations that originally colonized these sites.
Spatial genetic structure
Values of Moran's I were significantly different from the expected values in 15% (6/40) of the distance classes in SYB, 25% (8/32) of the classes in SYC, 19% (3/16) of the classes in MMH, and none of the classes in BSP (Table 4). The overall correlogram was significantly different from expected for two alleles (E[I] = –0.01) and both these alleles were in SYC. In the three shortest distance classes from all four populations, there were three significantly positive values of I and 33 values not significantly different from expected. The SYC population had two of the positive values and SYB had one, indicating that individuals possessing similar alleles were proximal more often than expected by chance. In the two midrange distance classes, values of I tended to decrease (four significantly negative and two significantly positive), while in the three longest distance classes, there were five significantly negative and three significantly positive values of I. The distance at which the correlogram first intercepts the value E[I] = –0.01 (for all sites) tends to represent the shortest length of an irregularly shaped patch (Sokal, 1979
). The mean correlograms (Figs. 2, 3) suggest that patch sizes ranged from 30 to 70 m in SYC and SYB, respectively, and were approximately 10 m in MMH and BSC. Because trees that could have provided alleles for an individual with the rare 6Pgd-2 genotype in MMH were 25 to 40 m away, the 10-m patch size is likely a low estimate.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In contrast, the BSC isolated population was polymorphic at 4.5% of its loci and averaged 1.05 alleles per locus (Table 3). The mean expected heterozygosity values varied threefold, from 0.008 to 0.026, and were lower than those reported for studies of other Abies species. Abies lasiocarpa [Hook.] Nutt., which is widespread in western North America (Shea, 1990
), had a mean He value of 0.125, while Abies in fragmented populations in southern Mexico (Aguirre-Planter, Furnier, and Eguiarte, 2000
) had mean He values from 0.069 to 0.113, and A. mariesii Mast. populations in Japan had a mean He value of 0.054 (Suyama, Tsumura, and Ohba, 1997
). The higher mean He value (0.274) from a study on mating systems in A. balsamea (Neale and Adams, 1985
) was based only on polymorphic loci. The levels of genetic variability found in A. balsamea were higher than two of its associated species, hemlock (Tsuga canadensis) (Zabinski, 1992
) and red pine (Pinus resinosa Aiton) (Simon, Bergeron, and Gagnon, 1986
), which have narrower ranges and are thought to have gone through a population bottleneck, but lower than the mean genetic variability found in gymnosperms (Pp = 53.4%, A = 1.83, He = 0.151) or other plant species with a boreal temperate distribution (Pp = 68.4%, A = 2.07, He = 0.204) (Hamrick, Godt, and Sherman-Broyles, 1992
).
The mean FST estimate, indicating 3.7% of the observed genetic diversity was found among populations, was less than the reported mean FST of 7.3% for gymnosperms (Hamrick, Godt, and Sherman-Broyles, 1992
) and 10% for eight Abies species (Aguirre-Planter, Furnier, and Eguiarte, 2000
). Both the mean FST and the mean genetic distance (D = 0.0008) measured relatively low levels of genetic differentiation among populations. The estimated value of Nm (6.5 immigrants per generation) also suggests some gene flow among populations, although the low levels of genetic variability may inflate the estimate. Values of Nm > 4 are thought to counteract the effects of drift (Jorgensen and Hamrick, 1997
), but they may not counterbalance drift as much as expected if migrants are related or if migration rates vary over time (Levin, 1988
). While there are other isolated populations of balsam fir in the Driftless Area, known populations are 2 km apart over hilly terrain and along different river systems. Dispersal among populations is likely rare. Estimates of gene flow in other conifers range from 0.67–3.17 immigrants per generation in four species of Abies in Mexico (Aguirre-Planter, Furnier, and Eguiarte, 2000
), 0.76–27.5 in Picea (Ledig et al., 1997
), to an average of 12.4 in Pinus (Ledig, 1998
).
The mean FIS value of 0.154 for balsam fir was larger than usually found in conifers and suggests inbreeding in the populations studied. Most conifers have an excess of heterozygotes, but other studies of Abies have also found a deficit of heterozygotes. In A. lasiocarpa FIS = 0.341 (Shea, 1990
) and in four species of Mexican Abies, FIS ranged from 0.074 to 0.235 (Aguirre-Planter, Furnier, and Eguiarte, 2000
). The value of FIS can be used to estimate the outcrossing rate t, such that t = (1 – Fe)/(1 + Fe) (Allard, Jain, and Workman, 1968
), where Fe is the equilibrium fixation index. Assuming FIS represents Fe, then t = 0.73. This value is lower than the mean outcrossing rate of 0.89 found in A. lasiocarpa (Shea, 1987
) and lower than the rates of 0.89–0.98 generally found in the Pinaceae (Schemske and Lande, 1985
). However, Ledig et al. (1997)
found high rates of selfing (0.85–1.0) in some isolated populations of Picea chihuahuana Martinez. The data from the study reported here (Tables 2 and 3) suggest that there are low levels of inbreeding in central populations and high levels of inbreeding in isolated populations.
The relatively low levels of genetic variability are consistent with the ecological characteristics and history of balsam fir. The medium stature of balsam fir, compared with other nearby hardwood and conifer species in the Sylvania populations, would tend to reduce pollen flow and make matings among nearby related individuals more likely. Studies of past Abies pollen records suggest that Abies has poor pollen dispersal and perhaps low pollen production (Jackson et al., 1997
). Canopy trees grow to 24 m tall, but most are shorter and seed is wind-dispersed, falling mainly within one to two tree heights from the base of the tree (Johnston, 1986
). Although an individual balsam fir may live to 200 yr of age, most die at 70–90 yr because trees are vulnerable to wind damage, spruce budworm, and root rot. Regular seed production begins at 30 yr, and good seed crops occur at 2–5 yr intervals (Johnston, 1986
). Therefore, since the retreat of the Wisconsin glaciation over 10 000 yr ago, there have been somewhere between 125 and 333 generations of balsam fir. Because the species has migrated into glaciated areas or persisted as small relict populations since glaciation, there has not been much time, in evolutionary terms, for differentiation within and among populations.
Spatial genetic structure
Spatial autocorrelation analyses showed more significantly positive values of I in the shorter distance classes, indicating that, at least in the central populations, individuals with similar alleles were proximal more often than expected by chance alone. This result supports Wright's (1943)
isolation by distance model in which limited dispersal distances result in excess matings among individuals in physical proximity. In the intermediate distance classes, the values tended to be more negative and more variable, making it difficult for any patterns to be discerned other than that individuals were more genetically distinct. Less variation in the longest distance classes suggest a repeating patchy distribution (Epperson and Clegg, 1986
) rather than a cline, with individuals becoming more genetically distinct with increased distance. Microenvironmentally similar sites could enhance development of patches with similar genotypes, shown in previous studies to develop within 50 generations and persist for long periods (Sokal and Wartenburg, 1983
; Epperson and Li, 1996
). In the isolated populations the paucity of genetic variation and the small area over which trees were distributed made the correlograms difficult to interpret, but the pattern of more similar alleles among individuals in closer proximity was found in all populations studied.
Statistical tests are not available for comparisons of differences between correlegrams (Sokal and Wartenberg, 1983
). However, comparisons among the few studies on spatial structure in temperate forest trees suggest that balsam fir tends to show more structure than lodgepole pine (Epperson and Allard, 1989
) and black spruce (Knowles, 1991) but less structure than sugar maple (Perry and Knowles, 1991
). The moderate spatial structure observed fits with the role of balsam fir as an intermediate-size tree with a patchy distribution. Being shorter than red pine, white pine, and hemlock would contribute to decreased pollen flow and more spatial structure. The patch size of 30–70 m found in the central populations of this study is similar to the results of Frelich and Reich (1995)
, who found that balsam fir, along with other late-successional species such as black spruce (Picea mariana (Mill.) B.S.P.), white cedar (Thuja occidentalis L.), and paper birch (Betula papyrifera Marsh.), occur in patches of approximately 35 m2 in southern boreal forests of Minnesota.
Conservation implications
It is generally acknowledged that species conservation depends on protecting genetic variability throughout the range of a species. Conservation of peripheral populations is currently included in protection plans for economically important and endangered species (Millar and Libby, 1991
; Lesica and Allendorf, 1995
). Peripheral populations should also be considered important for conserving the evolutionary potential of more widespread species such as balsam fir. The results of this study found no unique genetic markers, but the fact that balsam fir has likely survived for several thousand years in the isolated populations suggests that these populations may have unique alleles not discovered through allozyme analysis. Future studies using microsatellites may offer additional information about genetic variation and patterns of colonization after glaciation (Vendramin et al., 1999
). The small size of geographically peripheral populations makes them more prone to extirpation due to stochastic or catastrophic events than ecologically central populations. However, both isolated populations in this study had between 75 and 175 mature trees, more than the 50 individuals needed to avoid harmful loss of genetic variation in the short term (Frankel and Soule, 1981
; Lesica and Allendorf, 1992
).
In selecting populations for conservation, priority should be given to those with higher allelic diversity (Petit, El Mousadik, and Pons, 1998
). Although the two isolated populations were similar genetically, there was slightly more allelic variation in the MMH population than the BSC one, a finding supported by our preliminary study with two chloroplast microsatellite loci. Because MMH is a Nature Conservancy Reserve and BSC is part of a Minnesota state park, both populations will be preserved for the forseeable future. The main concern is management. Although cone production was observed, both populations had few or no fir seedlings. In MMH, the understory was covered with yews, and in BSC, maples were competing in the understory, leaving few openings for fir-seedling establishment in either site. When a number of the larger firs in MMH were cut in 1936, new trees became established as a result of the openings in the canopy (Conard, 1938
). Successful growth of fir seedlings is likely if there are cleared areas in the understory, whether these clearings occur from natural or human-managed events. Because only 3.7% of the genetic variation observed was due to differences among populations, transplanting seeds and seedlings could improve reproduction without greatly changing the genetic makeup of the populations. Transplantion should be kept to less than 1% of the extant population, however, to minimize the possibility of outbreeding depression while enhancing genetic diversity (Ellstrand and Elam, 1993
).
The future of the centrally located populations in the Sylvania Wilderness Area seems secure as long as human disturbance does not change the forest mosaic. When nearby forests were clear-cut, both the conifer-dominated and hardwood-dominated stands converted to hardwoods (Davis et al., 1994
). Although browsing by deer and periods of drier climate may have harmed conifers, the rapid regrowth of sugar maple is likely a major factor in the conversion to a hardwood stand. A comparison of the reproductive ecology of balsam fir and sugar maple in Quebec, Canada, found that seedlings of both species originate from the previous year's seed rain and postdispersal seed mortality is 70% for balsam fir and 20% for sugar maple (Houle, 1992
). Although sugar maple and balsam fir both reproduce at 3–5 yr intervals (Young and Young, 1992
), the higher viability and rapid growth of sugar maple will enable it to outcompete balsam fir and other conifers.
Given the general consensus that there will be rapid climate change over this century, many species of woody plants will be pushed to the limits of adaptation and/or will be forced to shift their range through seed dispersal (Davis and Shaw, 2001
). In North America and Japan, studies of forest trees have shown a decline in genetic variability at the edge of the the migration front, probably because of stochastic factors (Cwynar and MacDonald, 1987
; Suyama, Tsumura, and Ohba, 1997
). However, adaptation is more likely to be restricted at the trailing edge of the distribution because populations no longer receive gene flow from "preadapted" populations. For example, populations of jack pine (Pinus banksiana Lamb.) and red pine (P. resinosa) in the southeastern United States were extirpated at the beginning of the Holocene and the northern populations expanded (Jackson et al., 2000
; Davis and Shaw, 2001
). Something similar could happen to the isolated balsam fir populations in this study. A change in temperature of the algific talus slope microhabitats could enable the surrounding hardwoods to outcompete the balsam fir. Although the fir populations survived a warmer period 5500–3500 yr ago that had an estimated mean annual temperature increase of 1.5°C (Baker et al., 1996
), future temperature increases of 1.5°–4.5°C are predicted in the northern Great Plains by 2060 (Davis et al., 2000
).
The lower levels of genetic variability measured for balsam fir fit with the ecological characteristics of fir in the areas studied. It is one of several subdominant conifers in the hemlock-dominated forests of the Upper Peninsula of Michigan and western Wisconsin and the dominant conifer in the algific talus slope communities in Minnesota and Iowa. The medium stature and relatively large seed size of balsam fir contribute to localized seed dispersal, leading to populations with a patchy spatial structure. Because seed reproduction only occurs every 2–5 yr, there are fewer opportunities for genetic recombination than in other tree species. However, balsam fir's wide distribution over a variety of microhabitats suggests that it has adapted to low levels of genetic variation, that it will migrate in response to future environmental changes, and that the extremely low levels of genetic variation found in the isolated populations will make it difficult for them to adapt to rapid climate change.
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FOOTNOTES |
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4 E-mail for reprint requests: sheak{at}stolaf.edu
5 Current address: Tucson High Magnet School, 400 North 2nd Avenue, Tucson, Arizona 85705 USA
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Allard R. W. S. K. Jain P. L. Workman 1968 The genetics of inbreeding populations. Advances in Genetics 14: 55-131
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