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Reproductive Biology |
Centre for Forest Gene Conservation and Department of Forest Sciences, University of British Columbia, 3041-2424 Main Mall, Vancouver, British Columbia, V6T 1Z4, Canada
Received for publication May 13, 2006. Accepted for publication May 7, 2007.
ABSTRACT
Because mating system can be influenced by effective neighborhood size, density, and isolation, populations at range peripheries may differ from those in the center. The importance of peripheral populations to conservation and evolution is controversial, and additional information about their genetic structure and evolutionary dynamics will inform conservation strategies. In wind-pollinated species, selfing rate is generally negatively correlated with population size and density, and inbreeding may therefore increase toward range peripheries. Picea sitchensis has a long and narrow range along the Pacific Coast of North America that tapers toward the northern and southern peripheries. We investigated whether central and peripheral populations differ in mating system parameters. The results suggest that population position within the range has a strong effect on mating system, and geographic isolation appears to be associated with higher selfing. The estimated effective number of pollen donors was much higher in the center of the range (mean = 18.5) than at the periphery (mean = 3.6), while selfing rate increased from 7.3% in central populations to as high as 35.2% in the northern, isolated population. These strong geographical patterns suggest mating system is influenced by both population size and isolation at range peripheries.
Key Words: biparental inbreeding • isolated populations • mating system • Picea sitchensis • Pinaceae • range periphery • selfing • Sitka spruce
Mating system in plants can be influenced by various ecological and physical conditions. Geographic conditions may determine species occurrence and plant density, and population size generally decreases toward the species range peripheries (Brown, 1984
; Lawton, 1993
). Many empirical studies suggest that population density influences mating system in plant species. Reduced density, and thus smaller effective population size, can influence mating system indirectly, by affecting pollinator availability and behavior. In some animal-pollinated species, increased pollen flow is observed with lower plant density (Nason and Hamrick, 1997
; Dick, 2001
; White et al., 2002
) because high plant density results in shorter pollinator flights (Levin and Kerster, 1974
; Murawski, 1987
). However, outcrossing rate is often positively correlated with population size in both animal-pollinated (e.g., Murawski and Hamrick, 1992
; Franceschinelli and Bawa, 2000
; Lee, 2000
) and wind-pollinated tree species (e.g., Farris and Mitton, 1984
; Raijmann et al., 1994
; Rajora et al., 2002
). Higher population size and density can result in a higher diversity of available gametes within populations and increased outcrossing rates. While the mating system in animal-pollinated species is a result of complex interspecific interaction between plants and pollinators, wind-pollinated species may show a simple positive correlation between population size and outcrossing rate. This is expected because pollen dispersal by wind decreases exponentially with distance (Levin and Kerster, 1974
; Farris and Mitton, 1984
), and outcrossing rate is both density-dependent, and dependent on the frequency of genotypes in surrounding pollen neighborhoods in wind-pollinated species (Holsinger, 1991
). These empirical results indicate that population size and density are strong factors determining mating system in plant species. However, studies of mating system with a geographical context are relatively limited.
The value of peripheral populations for conservation has been a topic of considerable debate (Lesica and Allendorf, 1995
). On the one hand, peripheral populations can differ genetically and morphologically from central populations because of their smaller sizes and greater physical and ecological distances from the center of the range, and may contain genotypes adapted to extreme environmental conditions. On the other hand, peripheral populations may be demographic sinks with little evolutionary potential, sustained only by dispersal from central populations. Small peripheral populations can experience higher inbreeding compared to central populations, which can further decrease effective population size because of inbreeding depression (Charlesworth and Charlesworth, 1987
). A better understanding of the genetic dynamics of peripheral populations, including mating system dynamics and inbreeding, will inform conservation strategies.
When peripheral populations are small relative to central populations, it is expected that selfing rates will be higher in peripheral populations. This expectation is based on the concept of "abundant center distribution." Empirical studies have, however, shown mixed results, limiting the generalization of this concept. The selfing rate was significantly increased in a small peripheral population of Scots pine (Pinus sylvestris) compared to core populations (Robledo-Arnuncio et al., 2004
). Estimated multilocus outcrossing rate was slightly but not significantly higher in central compared to a peripheral population for both yellow starthistle (Centaurea solstitialis, Sun and Ritland, 1998
) and eastern white pine (Pinus strobus, Rajora et al., 2002
). There was no difference in selfing rate between central and peripheral populations in red columbine (Aquilegia canadensis, Herlihy and Eckert, 2005
). However, these studies found other effects of population size and density in peripheral populations, such as a higher correlation of paternity compared to central populations (Sun and Ritland, 1998
), higher proportion of empty seeds, higher correlation of outcrossing rate with plant density (Rajora et al., 2002
), and smaller flower size (Herlihy and Eckert, 2005
). Interestingly, there were no differences in outcrossing rates among continuous populations with varying densities of Scots pine (Robledo-Arnuncio et al., 2004
). This may imply continuous peripheral populations have large population sizes despite low plant densities. Mating system and population structure may be influenced by effective population size rather than plant density per se when species are capable of high gene flow. We would expect in wind-pollinated species that outcrossing rate and effective neighborhood size are lower in peripheral populations relative to central populations when peripheral populations are small.
The abundant center distribution model predicts that reduced population sizes at range peripheries will result in lower genetic diversity and higher population instability as well as higher inbreeding rate at the margins of the range compared to the center (Lesica and Allendorf, 1995
). While some authors have concluded that genetic diversity declines toward range peripheries (e.g., Guries and Ledig, 1982
; Rajora et al., 2002
), there is approximately equal empirical evidence against this prediction from studies where no differences in genetic diversity have been found among central and peripheral populations (e.g., Mouna et al., 1990
; Gamache et al., 2003
; Muir et al., 2004
). This controversy may exist because population size does not always decrease with distance from the center of the range, especially when a species is distributed over heterogeneous environments with multiple optimum niches, and when niches are truncated abruptly, such as at water–land boundaries. Sagarin and Gaines (2002)
tested the abundant center distribution and found only 39% of 145 tests supported this distribution pattern. Schwartz et al. (2003)
claimed that a critical problem in the central/peripheral argument is a lack of operational definitions of peripheral populations for a species.
Sitka spruce (Picea sitchensis) is a predominantly outcrossing, wind-pollinated conifer endemic to the Pacific coast of North America, from northern California to southwest Alaska. Its distribution is restricted to a narrow strip along the Pacific coast stretching over 22 degrees of latitude, with soft boundaries at the northern and southern range limits (Fig. 1). Core populations between southwest Washington and southern Alaska can contain large, productive, nearly pure stands of Sitka spruce. More often it is a common component of mixed-species, temperate rainforest stands along the coast and up river valleys to a maximum of 200 km inland (Peterson et al., 1997
). Under exceptional circumstances, individuals can grow to nearly 100 m in height, making it the largest Picea sp. and one of the largest conifers in the world. The width of the range tapers to the southern periphery where Sitka spruce is found in pure stands in a narrow belt often of small stature and poor form in the salt spray zone, and as a minor component of large stature trees in mixed species stands in the fog belt within a few km of the coast. The range also tapers north to the northern periphery along the Gulf of Alaska because of the relatively low cold hardiness of this species.
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), we expect that peripheral populations have smaller sizes, higher inbreeding rates. and greater correlated paternity, especially in populations that are disjunct from the major portion of the species range and thus geographically isolated. In this study, we defined peripheral populations as those at both the southern and northern soft boundaries of the species, where population size and species density gradually decrease. These peripheral populations are found at opposite extremes of the ecological niche of this species. They also have different population histories due to the relatively recent northward postglacial migration of Sitka spruce since the last glacial maximum (approximately 15 000 years before present) (Mann and Hamilton, 1995
). We previously documented substantially lower genetic diversity in peripheral than central populations based on pollen haplotypes (Mimura and Aitken, 2007
; see Table 1) and higher inbreeding in the genotypes of mature trees (Gapare et al., 2005
) in this species. If the effects of population size and isolation are strong, peripheral populations at opposite ends of the range should have similar mating systems despite ecological and historical differences. Our objective was to evaluate the influence of population position within the species range on mating system.
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Six populations were selected based on population position within the species range (Fig. 1). One continuous–disjunct pair of populations was sampled from each of three different regions: northern peripheral, central, and southern peripheral. The northern disjunct population was from Kodiak Island, Alaska (AK), separated by over 100 km of ocean from the nearest continuous populations (Rocky Bay). The southern disjunct population was from Fort Bragg, California (CA), separated from the southernmost continuous population of Redwood, California by over 100 km, apparently due to local climatic variation, and estimated to contain fewer than a thousand reproductively mature trees (F. Lee, California Department of Forestry and Fire Protection, unpublished data). The central disjunct population was from the Queen Charlotte Islands, British Columbia (BC), one of the most productive and high density regions for Sitka spruce, with many pure or nearly pure stands and located approximately 60 km from central mainland populations. The central continuous population sample was from Ocean Falls on the central BC coast, also an area of relatively high population density and wide east–west range. The northern disjunct population was from Kodiak Island, colonized by Sitka spruce around four centuries ago (J. Alden, University of Alaska, personal communication). Sitka spruce is the only conifer on Kodiak Island, where it has a fairly large population size and highly variable density. The northern continuous population was from Rocky Bay, a maritime, coastal environment at the periphery.
An average of 204 open-pollinated seeds in total from 10 to 20 open-pollinated seed parents per population were genotyped for each of the six populations to estimate mating system parameters (Table 1). The progeny of each seed parent are hereafter referred to as open-pollinated families. Seeds were obtained from maternal trees located at low elevation (<70 m) on the coast to eliminate environmental effects such as elevation on mating success and to avoid contamination though introgression with white spruce (P. glauca, Bennuah et al., 2004
). Seed samples were provided by the United States Department of Agriculture Forest Service, Alaska (samples from Alaska) and the British Columbia Ministry of Forests and Range (samples from Canada). These seeds originated from large collections made for provenance and progeny testing in tree breeding programs; samples are collected when cone crops are moderate to large, with many seeds and cones collected per tree from trees separated by a minimum of 50 m to avoid sampling closely related individuals. There were no adequate family-sampled seed collections available from the southern peripheral populations; therefore, we collected seeds early in the fall of 2003 near Redwood and Fort Bragg in California.
Genotyping
In conifer seeds, the megagametophyte that surrounds and provides nutrition to the embryo has the same haplotype as the egg resulting in the embryo. Genotyping both embryo and the corresponding megagametophyte with codominant genetic markers for each seed allows the unambiguous determination of the pollen gamete haplotype that fertilized the egg. Such genotyping more accurately estimates mating system parameters than does inferring maternal and paternal haplotypes from progeny arrays, as is necessary for angiosperms (Ritland, 2002
). In total, 1223 germinants and their corresponding megagametophytes were genotyped.
After soaking in water for 48 h, seeds were stratified at 4°C for 3 wk on filter paper in petri dishes and then germinated at room temperature. One- to 2-wk-old germinants and megagametophytes were stored at –80°C until DNA was extracted following Hodgetts et al. (2001)
. Seven polymorphic nuclear microsatellite markers were selected for genotyping: UAPgAG150 and UAPgAG105 developed for P. glauca (Hodgetts et al., 2001
), SPAGC1 and SPAGG3 developed for P. abies (Pfeiffer et al., 1997
), EAC7H07 developed for P. abies (Scotti et al., 2002
), and WS0073.H08 and WS0061.K02 developed for P. glauca and P. sitchensis (Rungis et al., 2004
). Polymerase chain reactions (PCR) were conditioned at 95°C for 5 min of initial denaturing; followed by 30 cycles of 94°C for 45 s, 53–57°C for 45 s, and 72°C for 45 s; and a final extension at 72°C for 10 min. PCR cocktails followed the LiCor (Lincoln, Nebraska, USA) 4200 manual with slight adjustments for individual primer sensitivities. PCR products were visualized on a LiCor 4200 automated sequencer. Images were scored using Saga Generation 2 (LiCor) with manual adjustments. One marker that had very low frequency of polymorphism (UAPgAG105) and one that had a high frequency of null alleles in the central disjunct and both northern populations (EAC7H07) were not included in further analyses.
Data analysis
Mating system parameters were estimated from offspring genotypes with maternal gamete information using the MLTR program (Ritland, 2002
). Maximum likelihood estimates of outcrossing rate were obtained under a mixed mating model (Ritland, 1990
, 2002
). Multilocus outcrossing rate (tm), single-locus outcrossing rate (ts), multilocus and single-locus correlation of paternity among families (rp(m) and rp(s), respectively), and correlation of selfing (rs) among families and loci were estimated based on the allele frequencies of all populations using maximum likelihood with the numeric Newton–Raphson method (Ritland, 2002
). Because family sizes and numbers were unequal among the tested populations, SD were estimated by sampling 1000 bootstrap replicates of individuals within families. Selfing rate(s), biparental inbreeding rate, and number of effective pollen donors (Nep) were estimated as 1 – tm, tm – ts, and 1/rp(m), respectively. The significance of differences in parameter estimates between members of each continuous–disjunct population pair was tested using bootstrapping.
RESULTS
Mating system parameters varied with both geographic position within the range and with isolation. All estimates and their standard errors are summarized in Table 2. Estimates of multilocus selfing rates (1 – tm) were lower at the range center and higher at the northern and southern peripheries (Table 2, Fig. 2a). The highest selfing rate was in the northern disjunct peripheral population (mean ± SE for Kodiak Island, s = 0.352 ± 0.030), while the central continuous population had the lowest selfing rate (Ocean Falls, s = 0.024 ± 0.017). There was a strong correspondence between selfing and population isolation. Selfing rates of the continuous populations were significantly lower than those of the nearby disjunct populations in all three regions (Fig. 2a). The selfing rates in the disjunct populations averaged 0.21, higher than the average of 0.07 for continuous populations.
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The results of this study suggest that population size and isolation in relation to geographic position within the species range have strong impacts on mating system and that population position may be a good predictor of effective number of pollen donors and other mating system parameters in Sitka spruce. Selfing rate increases and the effective number of pollen donors decreases from the center of the range towards the northern and southern range peripheries. Because only six populations were sampled, differences among population classes should be interpreted cautiously. The range of this species contains only two disjunct, peripheral populations and one central disjunct population, and these were all sampled. The sampled populations may have differed for factors other than range position and isolation that were not controlled such as local population size, local stand density, and fecundity. Nonetheless, the results agree closely with our expectations and strongly suggest that geographic factors leading to differences in mating system between central and peripheral, particularly disjunct peripheral, populations may result in significantly different evolutionary trajectories. To determine the generality of these results, a meta-analysis across species would be needed because most natural distributions do not offer sufficient numbers of disjunct populations for robust analyses.
Effects of population position and isolation on mating system
The estimated mean selfing rate in this study was quite high for a conifer (mean s = 0.14, range from 0.024 to 0.352) and higher than previous estimates for a seed orchard of this species (s = 0.08, Chaisurisri et al., 1994
). Conifers generally have low (
10%) selfing rates (Mitton, 1992
). Because four of our six sample populations were peripheral and two of these were disjunct, where effective population size is likely smaller than in the majority of continuous populations, the mean species-wide selfing rate was likely overestimated.
Selfing rates increase when effective population size is small or plant density is low (Loveless and Hamrick, 1984
). Higher selfing in peripheral continuous and disjunct populations compared to the central continuous population suggests that peripheral continuous and disjunct populations are smaller, less dense, have fewer trees that produce pollen or seed cones, and have a higher variance in fecundity of reproducing individuals or stronger within-population structure. A previous study concluded that southern and northern peripheral mature stands of Sitka spruce are more spatially structured and more inbred than central populations, likely due to the lower population densities in stands sampled (Gapare and Aitken, 2005
). It is harder to explain the higher selfing rates estimated for the central disjunct population from the Queen Charlotte Islands (QCI) compared to the central continuous population on the mainland (Ocean Falls). Differences in selfing rate can also be caused by differences in sample sizes per seed parent. When more seeds are sampled per open-pollinated family, estimates of selfing and correlation of paternity may increase for a limited number of loci. This may explain why the QCI population (a central disjunct population) had relatively high selfing rates despite high densities and the ecological dominance of Sitka spruce in this central population. The QCI population had more progeny sampled per seed parent but fewer seed parents sampled than Ocean Falls. Nonetheless, the QCI population had a correlation of paternity estimate as low as and comparable genetic diversity to the Ocean Falls population, suggesting that the two central populations have similar, large effective population sizes.
There are two mechanisms that may lead to higher inbreeding levels in lower density populations compared to higher density populations. First, when relatively few trees are present to contribute to the local pollen cloud, a tree's own pollen will contribute a higher proportion of the local pollen. This will increase selfing rates in lower-density compared to higher-density stands. This may be the case for the small, low-density Fort Bragg population. Similarly, increased variance in fecundity among individuals can also result in increased selfing for those individuals producing a lot of pollen. Second, when a species is at a relatively low density, seed shadows of different mother trees will have relatively little overlap compared with higher density stands. In this case, young trees getting established near one another are more likely to be related than trees in higher-density stands, resulting in stronger spatial structure (as observed for peripheral Sitka spruce populations by Gapare and Aitken, 2005
) and creating the opportunity for more biparental inbreeding. This is likely contributing to the high inbreeding in the Kodiak Island population. In some previous studies, however, populations with a relatively wide range of local plant densities have shown no differences in selfing rate (Neale and Adams, 1985
; Morgante et al., 1991
). It may be that only large differences in size or density, which cause strong population isolation, detectably affect mating system (Robledo-Arnuncio et al., 2004
). However, our results combined with those of Gapare and Aitken (2005)
generally indicate that both of these mechanisms increase inbreeding in lower-density peripheral populations.
In addition to plant density, effective neighborhood population size is an important factor affecting mating system. Wind-borne pollen can be transported long distances, and while most pollen travels relatively short distances, contributing only to local pollen clouds, small amounts of long-distance transport from many origins may cumulatively have a substantial effect on background pollen cloud density and diversity (Silen, 1962
). Continuous populations should have more potential sources of paternal variation and thus higher levels of background pollen than disjunct populations and may have larger effective neighborhood population sizes. This may explain why the continuous peripheral populations of Redwood and Rocky Bay, despite having relatively restricted local populations, have generally high outcrossing rates.
The generally high correlation of paternity in peripheral, particularly disjunct populations suggests a considerably higher probability of full-sibs in open-pollinated families in these populations than in central ones. Although Nep is usually much smaller than the effective population size Ne (Smouse and Sork, 2004
), the observed pattern in effective pollen donor size indicates a higher effective population size at the center of the range than at the periphery for Sitka spruce. Peripheral populations, particularly those that are physically isolated from the continuous portion of the range, seem to have relatively small effective population sizes and considerable genetic isolation.
The continuous and disjunct populations from the central region both had low correlations of paternity, despite differing significantly in selfing rates. Gapare and Aitken (2005)
found that central disjunct populations also had a stronger within-population spatial genetic structure than central continuous populations. One of these central disjunct populations, also included in the current study, is from the Queen Charlotte Islands (QCI), a large archipelago of approximately 10 000 km2. Our results indicate that this population may have an effective population size of a similar magnitude to that of Ocean Falls, the central continuous population on the mainland. This is supported by low biparental inbreeding rate in the central disjunct population and absence of male gamete substructure. Biparental inbreeding may reflect the amount of genetic diversity within populations (Ritland, 2002
). Despite strong spatial structure and substantial selfing, the QCI population may consist of many unrelated individuals at a larger scale, and high pollen flow among families may increase available male gametes within populations and thus the numbers of effective pollen donors.
Biparental-inbreeding rate had a somewhat different geographic pattern than selfing rate and effective number of pollen donors. Low biparental inbreeding indicates that matings occur largely between unrelated individuals. The reduction of biparental inbreeding from the north toward the south in continuous populations may reflect historical postglacial migration. Sitka spruce has likely been present continually for the longest time at the southern periphery. As a result, the continuous population we sampled in the southern region may have maintained historical refugial levels of genetic diversity; however, in the small, low density southern disjunct population at Fort Bragg, California, USA, isolation and reductions in population size may have increased relatedness within the population.
The concept of the abundant center distribution and related predictions have been debated (Sagarin and Gaines, 2002
), and there are several reasons why some species deviate from this hypothetical distribution. Discrete species boundaries, such as at water–land interfaces, determine species range limits without causing a decline in population size towards the edge. When a species has discrete or multiple landscape optima across its geographic range, plant density may not be a function of population position. For example, increased plant density in Aquilegia canadensis in northern peripheral populations compared to central populations may be caused by geographic restrictions of available habitat in central regions (Herlihy and Eckert, 2005
). The genetic model for species distribution predicting a decrease in density toward range peripheries assumes a linearly heterogeneous environment for a species (Kirkpatrick and Barton, 1997
). We found striking reductions in effective numbers of pollen donors toward the periphery of Sitka spruce, perhaps due to reductions in population size near soft boundaries. Allelic richness is also higher in central and lower in peripheral populations (Table 1). Sitka spruce has a reduced east–west range width at its northern and southern peripheries and an almost linearly heterogeneous environment along the coast at lower elevations (Fig. 1). These factors make Sitka spruce appear to fit the abundant center model reasonably well.
Selfing in isolated populations
The disjunct populations at both range peripheries (Kodiak Island and Fort Bragg) had high inbreeding rates, in contrast to the typical mating system of wind-pollinated temperate conifers (less than 10%). Given their differences in size and history, and depending on location, in stand structure and density, it is surprising that these populations have such similar mating systems. A large proportion of the "apparent" selfing (1 – ts) appears to result from biparental inbreeding (tm – ts). Sitka spruce appears to have reached the northeastern end of Kodiak Island only around four centuries ago, yet current population census size is fairly large. Older stands on the island consist of large, old founders at low density surrounded by smaller but reproductively mature second-generation trees at higher densities, while recently colonized areas have younger trees at low densities. There are many thousands of trees. In the older stands, the founders have much larger crowns and may have higher fecundities than second-generation mature trees as a result. The northern and southern peripheral disjunct populations also had fewer effective pollen donors than other populations.
The peripheral disjunct populations may experience severe inbreeding depression from both selfing and biparental inbreeding. However, the northern isolated population (with 35% estimated selfing) is continuing to extend the species limit and colonize nonforested areas on Kodiak Island (Griggs, 1937
) and the southern population continues to regenerate well following disturbance (F. Yee, California Department of Forestry and Fire Protection, personal communication). Despite comparatively high inbreeding levels, both the northern and southern disjunct populations appear to have higher juvenile fitness than nearby continuous populations when grown under the conditions of their native climate and day length (Mimura, 2006
). In most wind-pollinated conifers, it is widely accepted that inbreeding depression is severe at the individual level for fitness-related traits such as growth and seed production; however, this effect may not be important at the stand level (Williams and Savolainen, 1996
; Wang et al., 2004
). In tree species, inbred deleterious genotypes may be purged through natural selection because of low competitive ability (Plessas and Strauss, 1986
) during their relatively long juvenile period. Isolated conifer stands of reproductive age in natural populations do not always show a loss of fitness due to inbreeding. For example, isolated old-growth populations of red spruce (P. rubens) have significant selfing (Rajora et al., 2000
) but have growth rates comparable to large, continuous populations (Mosseler et al., 2000
). Both western redcedar (Thuja plicata) and red pine (Pinus resinosa) have a high tolerance to selfing with relatively high seed set per cone resulting from controlled self-pollination, indicating relatively low genetic loads of recessive lethal or severely deleterious alleles (Russell et al., 2003
; Boys et al., 2005
; Wang and Russell, 2006
). In both species, this selfing tolerance as well as lack of genetic diversity has been hypothesized to be the result of a Pleistocene bottleneck. Repeated founder events in the course of postglacial recolonization may have similarly facilitated purging at the leading edge of migration. The proportion of self-compatible plants of typically self-incompatible species has been shown to increase in peripheral populations when plant density is low (Butch, 2005
) because of reproductive assurance (e.g., Lloyd, 1979
, 1992
), indicating that selfing could evolve at range peripheries.
Isolated peripheral populations at the soft boundaries of species are thus potentially important for conservation even if those populations have high rates of inbreeding. Our results also indicate that open-pollinated seed collected for ex situ conservation, research, or reforestation from individual seed parents in peripheral populations will likely be less diverse than single-tree seedlots from central populations because of the relatively small number of male parents pollinating each seed parent in addition to the stronger spatial genetic structure and higher levels of inbreeding (Gapare and Aitken, 2005
). Sampling strategies developed for central populations may need to be modified in order to collect representative within-population genetic diversity from peripheral populations.
FOOTNOTES
1 The authors thank M. C. Whitlock, P. A. Arcese, and J. Whitton for comments on this manuscript; K. Ritland and C. Liewlaksaneeyanawin for comments on mating system analyses; C. Chourmouzis for editing; and J. Tuytel for technical assistance. This study was funded by a NSERC Discovery Grant to S.A. and by the Forestry Investment Account of BC through the Forest Genetics Council of BC to the Centre for Forest Gene Conservation at UBC. 
4 Author for correspondence (sally.aitken{at}ubc.ca
)
3 Current address: Gene Research Center and Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 305-8572, Japan
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