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Journal of Heredity 2007:98(7):640–645
doi:10.1093/jhered/esm089
Advance Access publication November 2, 2007
Extensive Long-Distance Pollen
Dispersal in a Fragmented Landscape
Maintains Genetic Diversity in White
Spruce
LISA M. O’CONNELL, ALEX MOSSELER,
AND
OM P. RAJORA
From the Canada Research Chair in Forest and Conservation Genomics and Biotechnology, Faculty of Forestry and
Environmental Management, University of New Brunswick, PO Box 44555, 28 Dineen Drive, Fredericton, NB E3B 6C2,
Canada (O’Connell and Rajora); and the Canadian Forest Service—Atlantic Forestry Centre, Natural Resources Canada,
PO Box 4000, Fredericton, NB E3B 5P7, Canada (Mosseler).
Address correspondence to O. P. Rajora at the address above, or e-mail: [email protected].
Abstract
Conifers are among the most genetically diverse plants but show the lowest levels of genetic differentiation, even among
geographically distant populations. High gene flow among populations may be one of the most important factors in
maintaining these genetic patterns. Here, we provide empirical evidence for extensive pollen-mediated gene dispersal
between natural stands of a widespread northern temperate/boreal conifer, Picea glauca. We used 6 polymorphic allozyme
loci to quantify the proportion of seeds sired by pollen originating from different sources in a landscape fragmented by
agriculture in North Central Ontario, Canada. In 7 stands, a small proportion of seeds were sired by self-pollen or
neighboring trees but 87.1% (±1.7% standard error [SE]) of seeds were sired by pollen from at least 250 to 3000 m away. In
4 single isolated trees, self-fertilization rates were low and more than 96% (±1.3% SE) of seeds were sired by immigrant
pollen. The average minimum pollen dispersal distance in outcrossed matings was 619 m. These results provide strong
evidence that extensive long-distance pollen dispersal plays a primary role in maintaining low genetic differentiation among
natural populations of P. glauca and helps maintain genetic diversity and minimize inbreeding in small stands in a fragmented
landscape.
During the last 2 million years, trees in the northern
hemisphere have undergone a series of range contractions
and expansions during recurring glacial–interglacial cycles
(Critchfield 1984). Unlike herbaceous plants, trees—and
particularly conifers—do not generally show evidence of
strong genetic differentiation among populations (Hamrick
and Godt 1996), even in recently colonized areas. Conifers
are also among the most genetically diverse plants (Hamrick
and Godt 1996). Pollen-mediated gene flow has been
invoked as one of the most important factors in maintaining
high connectivity between tree populations and maintaining
high genetic diversity within populations (Liepelt et al. 2002;
Burczyk et al. 2004; Hamrick 2004). However, gene flow has
generally been inferred indirectly from the degree of genetic
differentiation among populations measured by FST (Wright
1931). More recently, research has focused on contemporary
gene flow in trees. Pollen-mediated gene dispersal distances
have been estimated in an ever-increasing number of
640
animal-pollinated tropical tree species (Chase et al. 1996;
Nason and Hamrick 1997; Hamilton 1999; White et al.
2002). In northern temperate tree species, pollen is
predominantly wind dispersed. Pollen-mediated gene flow
distances have been estimated in wind-pollinated oaks
(Quercus spp.) (Smouse and Sork 2004) and ash (Fraxinus
spp.) (Bacles et al. 2005) and in a single or very few isolated
stands of conifers (Burczyk et al. 1996; Schuster and Mitton
2000; Dyer and Sork 2001; Robledo-Arnuncio and Gil
2004). Conifer seed orchard populations usually show about
50% pollen contamination from outside the orchard, even
when isolated from other stands by a few kilometers
(Adams and Birkes 1991; Paule et al. 1993; Xie and Knowles
1994; Harju and Nikkanen 1996; Adams et al. 1997).
Although long-distance pollen dispersal events over several
kilometers have been observed in natural populations of
tropical and temperate trees (Xie and Knowles 1994;
Schuster and Mitton 2000; White et al. 2002; Bacles et al.
O’Connell et al. Extensive Pollen Dispersal in White Spruce
2005), little is known about the frequency of these events at
the landscape level in natural populations of wind-pollinated
conifers.
White spruce (Picea glauca [Moench] Voss) is a well-suited
species for quantifying pollen movement in northern
conifers. It is wind pollinated and has a transcontinental
range across the boreal forest of North America (Nienstaedt
and Zasada 1990). Like most conifers, white spruce shows
high allozyme genetic diversity (He 5 16%) (Godt et al.
2001), a low percentage of genetic variation among
populations (FST 5 1.6%) (Godt et al. 2001), and high
levels of outcrossing in natural populations (t . 90%)
(Denti and Schoen 1988; O’Connell et al. 2006a). The
fragmentation of forests into small stands may isolate
populations by decreasing the amount of pollen dispersed
between populations, thus changing the natural patterns of
genetic structure and evolutionary dynamics. Previously, we
found that reproductive success in white spruce stands is
positively correlated with the number of trees in a stand,
suggesting that forest fragmentation limits pollen dispersal
into small stands (O’Connell et al. 2006b). However, we
found no difference in the genetic composition of the pollen
pool or levels of genetic diversity in the resulting offspring
in these small pollen-limited stands compared with large
contiguous stands with thousands of trees (O’Connell et al.
2006a). However, small stands (1–8 trees) showed a significantly lower number of effective pollen donors compared
with medium-sized (23–56 trees) and large stands (100
trees) (O’Connell et al. 2006a).
The source of pollen siring seeds in a stand can be
separated into different mating categories. Seeds can be
sired by the same tree (self-fertilized) or by another tree
(outcrossed). The father can be from within the stand
(neighbor) or from outside the stand (immigrant pollen).
The outcrossed father within a neighborhood can be related
(related neighbor) or unrelated (unrelated neighbor).
Immigrant pollen can further be divided between pollen
with allelic combinations that cannot be produced by any
local father (directly observable immigrant) and immigrant
pollen with a multilocus haplotype identical to pollen from
within the stand (cryptic immigrant).
In this study, we used allozyme markers and a combination of the neighborhood and mixed-mating models to
identify the source of pollen siring seeds and determine
pollen dispersal distances in small isolated stands of white
spruce in a landscape fragmented by agriculture.
Materials and Methods
Study Area
The study area was located around the western arm of Lake
Nipissing in North Central Ontario, Canada (46°20#N,
80°10#W; Figure 1). This area has been heavily fragmented
by agriculture making it an ideal landscape to study pollenmediated gene flow in isolated stands of temperate/boreal
zone wind-pollinated trees. Residual tree stands are
composed for the most part of white spruce, eastern white
pine (Pinus strobus L.), white birch (Betula papyrifera Marsh.),
and trempling aspen (Populus tremuloides Michx.). Tree stands
remain on rocky outcrops and are surrounded by larger
tracts of agricultural fields. Small stands also occur on
islands in Lake Nipissing (Figure 2). In the surrounding
tracts of contiguous forest, white spruce makes up less than
10% of the trees.
Sample Collection and Genotyping
Cones were collected from 32 white spruce trees from 11
small stands in August and September 1994 within
a 378-km2 area (O’Connell et al. 2006b). Seeds from an
additional 72 trees from 12 larger stands were sampled to
obtain background allele frequencies (O’Connell et al.
2006a). All sampled stands were separated by 250–3000 m
from the nearest adjacent white spruce stand. Most of these
stands were located on rocky outcrops surrounded by
agricultural fields, but 4 stands were located on islands in
Lake Nipissing (stands A, B, C, and D; Figure 1). The
average distance to the nearest conspecific tree within
a stand was 20 m. All reproductive white spruce trees were
sampled in each of the 11 small stands. Four stands had
a single isolated tree, and 7 stands had 3–8 reproductive
trees per stand (Table 1). We genotyped a total of 2967
seeds (96 per tree, except for 2 trees in stand C where only
31 and 56 seeds were genotyped) at 6 polymorphic allozyme
loci (Fum1, Idh1, Lap1, Lap2, Pgm1, and Pgm2) from 4
enzyme systems. We detected 3–5 alleles per locus, with
a total of 24 alleles at these loci (O’Connell et al. 2006a).
Megagametophytes were also separately assayed for 10% of
seeds. Assaying the haploid megagametophyte, which has
the same genetic constitution as the female gamete,
identifies the maternal allele passed on to the embryo.
Although highly variable markers, such as microsatellites,
improve the power to discriminate between individual
pollen parents, allozymes are less vulnerable to genotyping
error or new mutations. Even a small genotyping error can
greatly inflate gene flow rates (Burczyk and Chybicki 2004).
We obtained an exclusion probability of 63% based on the
allele frequencies of the pollen pool at the 6 loci (O’Connell
et al. 2006a; calculated following Jamieson 1994). Because of
the low exclusion probability of isozymes, we sampled a large
number of seeds per tree (i.e., 96 seeds per tree) to reduce
experimental error for the mating system parameter estimates.
Mating System and Gene Flow Analysis
We estimated mating system parameters in the 11 small
stands of white spruce using a combination of the
neighborhood (Adams 1992; Burczyk et al. 2002) and
mixed-mating models (Ritland 2002). To identify immigrant
pollen, all trees within a stand were genotyped at all
6 allozyme loci. Knowledge of background allele frequencies, although not necessary, yields a more accurate estimate
of cryptic gene flow (Burczyk and Chybicki 2004), and these
data were available (O’Connell et al. 2006a). The background pollen allele frequencies were estimated from the
genotypes of 9880 embryos sampled from 104 trees from
641
Journal of Heredity 2007:98(7)
Figure 1. The location of 23 sampled white spruce stands near the western arm of Lake Nipissing, Ontario. The location of the
study site is indicated on the inset map by an open square. Mating system parameters were estimated for small stands only in this
study (A–K, represented by triangles; stands with single trees include B, E, G, and I). Medium-sized stands (L–Q) and large stands
(R–W), respectively, represented by circles and squares, were sampled to obtain background allele frequencies. Not all white spruce
stands are indicated on the figure, only sampled stands. This figure is reproduced from O’Connell et al. (2006b) with the
permission of the National Research Council of Canada Research Press.
the 23 pooled stands (O’Connell et al. 2006a) using
Multilocus Mating System Program MLTR version 3.0
(Ritland 2002) and fixing the outcrossing rates at 94%. We
detected 26 different alleles in the background pollen pool.
In single trees, selfing (s) was estimated with MLTR using the
Newton–Raphson method, where s 5 1 tm and tm is the
multilocus outcrossing rate. Standard errors (SEs) were
Figure 2.
642
Isolated tree stands on islands in Lake Nipissing.
obtained from 300 bootstraps of the data with resampling
of individuals within families. For single isolated trees, all
seeds that are not self-fertilized are pollinated by immigrant
pollen (m) so that m 5 tm. To quantify the amount of pollen
immigration into stands with 3–8 reproductive trees, we used
the program NEIGHBOR version 2.0 (Burczyk et al. 2002).
This program simultaneously estimates selfing rates (s) and the
proportion of seeds sired by immigrant pollen (m) using the
Newton–Raphson method. SEs are derived from the Hessian
(variance–covariance) matrix (Burczyk et al. 2002). The
proportion of seeds sired by trees within a stand (neighborhood) was calculated as 1 s m. The percentage of directly
observable immigrants (b) is the number of embryos with
allele combinations that cannot be produced by fathers within
a stand divided by the total number of seeds analyzed and was
obtained with NEIGHBOR. The proportion of cryptic
immigrants is equal to m b. MLTR was used to estimate
the proportion of related neighbor matings (i.e., biparental
inbreeding) calculated as (tm ts), where ts is the mean singlelocus outcrossing rate. The proportion of unrelated neighbor
matings was calculated as (1 s m) (tm ts). Based on
the large sample size, we assumed a standard normal
distribution of the data, and 95% confidence intervals of
mating system parameters were obtained by multiplying the
SEs by the critical value, 1.96.
O’Connell et al. Extensive Pollen Dispersal in White Spruce
Table 1.
Stand
The percentage of pollen from different sources siring seeds in 11 small stands of white spruce in North Central Ontario
c
B
2000
E
300
G
700
I
250
Single treesb
A
400
C
3000
D
1500
F
300
H
500
J
300
K
250
3–8 treesb
N/n
s (SE)
1/96
1/96
1/96
1/96
4/384
3/288
3/183
3/288
4/384
3/288
8/768
4/384
28/2583
—
6.4 (4.0)
—
25.6 (7.1)
3.8 (1.3)
12.9 (3.6)
0.04 (1.1)
5.3 (3.6)
4.9 (2.6)
5.9 (2.8)
15.3 (2.7)
0.8 (2.1)
6.0 (1.0)
95% CI
1.7–5.9
4.0–8.0
ma (SE)
95% CI
—
93.6
—
74.4
96.2
68.7 (5.0)
112.9 (1.7)
66.0 (6.4)
82.2 (4.6)
92.4 (3.9)
108.8 (5.9)
95.7 (2.9)
87.1 (1.7)
1sm
tm ts (SE)
95% CI
b
1.9–5.5
27
84
32
53
49
18
12
16
12
34
15
11
16
93.7–98.7
83.8–90.4
18.4
13.2
28.7
12.9
1.7
24.1
3.5
6.9
5.4
3.1
3.1
0.1
4.3
6.5
1.8
3.7
(2.7)
(4.3)
(3.4)
(2.5)
(2.6)
(1.6)
(2.3)
(0.9)
c, distance to the closest neighboring white spruce stand in meters; N, the number of reproductive trees in a stand; n, the number of seeds sampled; s, the
percentage of self-fertilized matings; CI, confidence interval; m, the percentage of immigrant pollen; 1 s m, the percentage of cross-fertilized matings
within a stand (neighbor); tm ts, the percentage of biparental inbreeding (related neighbor matings); b, the percentage of directly observable immigrants.
a
Estimates with a dash failed to converge because of the small sample size (i.e., one tree per stand).
b
Mating system parameters are not means but are estimated simultaneously for the group.
Pollen Dispersal Distance
The minimum pollen dispersal distance was estimated for
outcrossed matings only. The mean minimum dispersal
distances of pollen siring seeds in each small stand were
estimated as
ð1 s mÞnd þ mnc
ð1 sÞn
where, for each stand, s is the selfing rate, m is the
immigration rate, n is the number of seeds sampled in
a stand, d is the mean distance to all other trees within
a stand, and c is the distance to the closest neighboring
stand. The overall mean dispersal distance was weighted by
the number of seeds sampled in each stand.
Results
At the stand level, selfing rates ranged from 0.04% to
25.6%, but all stands showed high levels of immigrant
pollen (66–100%; Table 1). Estimates of m . 100%, and
1 s m and ts tm , 0% are statistical artifacts. The
biological range for these parameters is 0–100%. Thus, the
biological estimates corresponding to the statistical estimates .100% and ,0% are 100% and 0%, respectively.
In the 4 single isolated trees, 96.2% of seeds were sired by
outcrossed, immigrant pollen (Table 1). About half of the
outcrossed seeds were sired by directly observable immigrant pollen and the remainder by cryptic immigrants
(Figure 3). In stands with 3–8 trees, 87.1% of seeds were
sired by outcrossed, immigrant pollen (Table 1). Matings
within the stands were divided between inbred matings
(6.0% selfed and 3.7% related neighbor) and unrelated
neighbor matings [(1 s m) (tm ts) 5 3.2%] (Figure 3).
Only 16% of the seeds in stands with 3–8 trees were pollinated by directly observable immigrant pollen (Figure 3).
Although the overall power to directly detect immigrant pollen
was low, we obtained small SEs for the mating estimates over
all single trees (SE 5 1.3) and overall stands with 3–8 trees
(SE , 1.7; Table 1). We did not observe any relationship
between the size of a stand (N ) or the distance to the closest
stand (c) and any of the mating system parameters.
We estimated that the minimum pollen dispersal distance
in outcrossed matings was 619 m for all the trees and 654 m
when single isolated trees were excluded.
Discussion
The extensive pollen-mediated gene flow we observed into
small isolated stands of white spruce indicates that there is
high connectivity among these fragments at the landscape
scale. The estimates of pollen immigration into these small
white spruce stands are higher than the observed levels of
around 50% in conifer seed orchards (Adams and Birkes
1991; Xie and Knowles 1994; Harju and Nikkanen 1996;
Adams et al. 1997). There is increasing evidence that
fragmentation may increase gene flow in forest trees (Young
et al. 1996; Dyer and Sork 2001; White et al. 2002; Smouse
and Sork 2004). We have indeed found that in small
fragmented stands, the majority of seeds were sired by
pollen from outside the stands and few matings occurred
between neighbors (6.9%). However, we do not have any
evidence that these gene flow rates are higher than in larger
stands in this landscape. Nevertheless, in large stands, given
the same amount of background pollen, the additional
pollen must come from within the stand, thus lowering the
proportion of immigrant pollen, that is, gene flow rate.
Selfing and biparental inbreeding levels in 6 medium-sized
(23–56 trees) and 6 large stands (100 trees) were
previously estimated and did not significantly differ from
levels in the 11 small stands in this study (O’Connell et al.
2006a). On the other hand, we previously observed lower
643
Journal of Heredity 2007:98(7)
Figure 3. Source of pollen fertilizing seeds in 11 small isolated stands of white spruce in (a) 4 single isolated trees and (b) 7 small
stands with 3–8 trees (total of 28 trees). Estimates are within ±1.3% SE for single trees and ±1.7% SE for small stands.
fertilization rates in these small stands due to pollen limitation.
Although fragmentation negatively affects the fertilization
rates, it does not seem to decrease genetic diversity or increase
inbreeding levels in resulting fully-developed seeds.
In this study, mating system parameters were obtained
from filled seeds so that the realized gene flow does not
necessarily represent the pollen flow. In most conifers, most
inbred embryos are eliminated due to inbreeding depression
before they are genotyped at the seed stage. We have
previously found that trees in stands with 3–56 trees have
a higher proportion of empty seeds (47%) than trees in
larger stands (100 trees; 35% empty seeds), suggesting
higher levels of primary selfing in the former stands
(O’Connell et al. 2006a). The elimination of inbred embryos
can increase the genetic heterozygosity of the resultant seed
and contribute to the maintenance of genetic diversity. In
contrast, the low proportion of aborted seeds (30%) in the
4 single isolated trees was comparable with that in the larger
continuous stands, suggesting low primary rates of selffertilization in single trees. Although strong selection against
inbred seeds through early abortion can contribute to the
maintenance of genetic diversity in offspring, the primary
mechanism contributing to the high genetic diversity of seed
produced in these isolated white spruce populations seems
to be extensive pollen-mediated gene flow.
The large pollen dispersal distances we observed in white
spruce may partly be due to the scale of the study. The scale
of this study and the mean pollen dispersal distances that we
observed are an order of magnitude greater than previous
studies in wind-pollinated trees (Burczyk et al. 2004; Bacles
et al. 2005). Another explanation for our observation of
such extensive gene dispersal in this agricultural landscape is
that it is surrounded by relatively contiguous forest, albeit
with a white spruce component of ,10%. Pollen from
single trees or small groups of trees may not be competitive
with pollen produced in the surrounding forest. Most of the
644
local pollen in small stands may be carried away by strong
winds. Other studies estimating pollen-mediated gene dispersal
distances in conifers were conducted on relict (RobledoArnuncio and Gil 2004), seed orchard, or extremely isolated
populations (Schuster and Mitton 2000) in which less than
10% of seeds were sired by pollen from outside the stands.
Rather than observing the occasional long-distance
dispersal event, we have shown that mating between trees
separated by several hundred meters is common in the small
geographically isolated white spruce stands in this study. We
have provided empirical evidence of extensive gene flow
through long-distance pollen dispersal in a widespread,
temperate and boreal zone conifer at the landscape level.
These results may be representative of pollen-mediated gene
dispersal patterns between conifer populations, which, like
white spruce, show high genetic diversity and low
differentiation among populations (Hamrick et al. 1992).
Long-distance gene flow also maintains genetic diversity in
small stands so that trees and stands separated by several
hundred meters from large contiguous tracts of forest are
not genetically isolated. Thus, forest fragmentation does not
necessarily affect the levels of genetic diversity of the seed
produced by isolated white spruce. Extensive, long-distance,
pollen-mediated gene flow seems to be the primary
mechanism for maintaining connectivity and genetic diversity among these populations. This empirical evidence of
extensive gene flow in a temperate/boreal conifer may also
explain how conifer populations maintain genetic connectivity despite a geological history of massive range
contractions and expansion during recurring glacial cycles.
Funding
Natural Sciences and Engineering Research Council of
Canada (L.M.O.); Canada Research Chair Program (CRC
O’Connell et al. Extensive Pollen Dispersal in White Spruce
950-201869) (O.P.R.); Natural Sciences and Engineering
Research Council of Canada Discovery Grant RGPIN
170651 (O.P.R.); Canadian Forest Service (A.M.).
Acknowledgments
We thank J. Burczyk for providing the program NEIGHBOR version 2.0;
I. DeMerchant and R. Simpson for producing the map of the study site;
B. Arsenault and L. Deverno for help in the laboratory; L. Dobrich for
locating and collecting samples; and P. Smouse, R. Latta, J. Burczyk,
K. Percy, and Y.-S. Park for comments on the manuscript. O.P.R. holds the
Senior Canada Research Chair in Forest and Conservation Genomics and
Biotechnology.
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Corresponding Editor: James Hamrick
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