Understanding the evolution of native
pinewoods in Scotland will benefit their
future management and conservation
MATTI J. SALMELA1,2, STEPHEN CAVERS2*, WITOLD WACHOWIAK2,3,
JOAN E. COTTRELL4, GLENN R. IASON5 and RICHARD A. ENNOS1
1 Institute
Summary
Scots pine (Pinus sylvestris L.) is a foundation species in Scottish highland forests and a national icon. Due to heavy
exploitation, the current native pinewood coverage represents a small fraction of the postglacial maximum. To reverse
this decline, various schemes have been initiated to promote planting of new and expansion of old pinewoods. This
includes the designation of seed zones for control of the remaining genetic resources. The zoning was based mainly on
biochemical similarity among pinewoods but, by definition, neutral molecular markers do not reflect local phenotypic
adaptation. Environmental variation within Scotland is substantial and it is not yet clear to what extent this has shaped
patterns of adaptive differentiation among Scottish populations. Systematic, range-wide common environment trials
can provide insights into the evolution of the native pinewoods, indicating how environment has influenced phenotypic
variation and how variation is maintained. Careful design of such experiments can also provide data on the history and
connectivity among populations, by molecular marker analysis. Together, phenotypic and molecular datasets from such
trials can provide a robust basis for refining seed transfer guidelines for Scots pine in Scotland and should form the
scientific basis for conservation action on this nationally important habitat.
Introduction
Scots pine (Pinus sylvestris L.) is a national icon in Scotland
and a foundation species in the Caledonian forest. Currently, 84 Scots pine woodlands of different sizes in Scotland are recognized as native (Anonymous, 1998). In total,
these constitute <1 per cent of the maximum postglacial
range and represent the only recognized UK resource for
this habitat, Caledonian pinewood, which receives protection under the European Commission Habitats Directive.
These pinewoods represent the north-western extreme of
the species’ distribution, which is one of the widest of all
conifers, extending from northern Finland to Turkey and
from western Spain to eastern Siberia (Critchfield and Little, 1966), covering a huge range of environments. In many
places, Scots pine is also a commercially important timber
species, its wood being used for construction, furniture and
other products. In Scotland, native trees of commercially
desirable form persist in a few relatively large populations,
© Institute of Chartered Foresters, 2010. All rights reserved.
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e.g. Abernethy, Rothiemurchus and Glen Tanar (Mason
et al., 2004). Recognition of the biological, cultural and
recreational value of the species to Scotland has resulted
in initiation of replanting programmes, and the commercial
prospects for native pine are currently being re-evaluated,
e.g. in ‘Developing the Scots Pine Resource’ project in
collaboration with institutes from the Nordic Countries
(Macdonald et al., 2008).
Adaptation to local climatic conditions through genetic
differentiation is a widespread feature of forest tree species
(Howe et al., 2003; Savolainen et al., 2007). This characteristic is of high importance for strategies focused on conservation of genetic resources, especially under changing
environments. The use of maladapted planting stock or the
uncontrolled translocation of non-local provenances may
lead to losses in productivity or dilution of local gene pools,
impacts to which highly reduced or fragmented populations
may be especially vulnerable (McKay et al., 2005). Despite
the many unique characteristics of Scottish pinewoods, the
Forestry, Vol. 83, No. 5, 2010. doi:10.1093/forestry/cpq036
Advance Access publication date 2 November 2010
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of Evolutionary Biology, School of Biological Sciences, Ashworth Laboratories, University of Edinburgh, Edinburgh
EH9 3JT, Scotland
2 Natural Environment Research Council Centre for Ecology and Hydrology, Edinburgh, Bush Estate, Penicuik, Midlothian
EH26 0QB, Scotland
3 Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, Poland
4 Forest Research, Northern Research Station, Roslin, Midlothian EH25 9SY, Scotland
5 Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, Scotland
*Corresponding author. E-mail: scav@ceh.ac.uk
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extent of possible local adaptation has not been studied in
detail. The aims of this paper are to review current knowledge about the evolution of pinewoods in Scotland and
to demonstrate how understanding the species’ history and
evolution could provide valuable information with which
to refine current guidance on the conservation and expansion of the existing pinewood resources. This is particularly
timely given the Scottish government’s aim of increasing
forest land cover from 17.1 to 25 per cent (Scottish Forestry
Strategy 2006, 2006).
The last glaciation has strongly influenced the distributions
of numerous species in Europe as, during the last glacial
maximum 23 000–18 000 years ago, ice covered the majority of northern Europe (Svendsen et al., 1999). Pine survived through the ice age in the Iberian, Italian and Balkan
peninsulas (Bennett et al., 1991), but macrofossil evidence
for refugia has also been found in central parts of Europe
(Willis et al., 2000; Willis and van Andel, 2004; Birks and
Willis, 2008). Climate modelling suggests that these areas
would have been suitable for pine at that time (Cheddadi
et al., 2006). Populations from the Iberian and Italian
Peninsulas harbour unique seed-transmitted mitochondrial DNA (mtDNA) variation that is not found elsewhere in Europe (Sinclair et al., 1999; Soranzo et al.,
2000; Cheddadi et al., 2006; Pyhäjärvi et al., 2008),
and the Iberian pinewoods have also been found to differ from other continental populations for monoterpene
and allozyme variation (Tobolski and Hanover, 1971;
Prus-Glowacki and Stephan, 1994). These patterns support the view that more northern pine populations
originate from refugia located north of the southern
peninsulas and south of permafrost.
According to pollen studies, pine reached Scotland
~8000 years ago, and appeared first in the Wester Ross area
in the north-west, and then shortly afterwards in the Cairngorms (Birks, 1989), the latter presumably having spread
northwards through England (Bennett, 1995). Interpreting
pollen data in species like pine can be challenging due to
its abundance and long dispersal distances, and therefore
macrofossil data are needed to verify presence of local populations (Birks, 2003). In fact, fossil stomata from two sites
in the highlands indicate that pine was locally present 1600
–600 years earlier than suggested by pollen data (Froyd,
2005). Contemporary populations from Wester Ross differ
from those in the rest of Scotland in their allozyme and
monoterpene frequencies, suggesting that the contemporary Scottish population derives from multiple refugia
(Forrest, 1980, 1982; Kinloch et al., 1986). For example,
in contrast to the rest of the populations, the frequency of
3-carene in the north-west is very low (Forrest, 1980); biochemically, populations from this area seem more closely
related to southern European populations than those from
north-central Europe, which are similar to the rest of the
Scottish pinewoods (Forrest, 1982). It is possible that the
Current status of native Scottish pinewoods
During its history in Scotland, pine has fluctuated in abundance, sometimes very rapidly, due to various factors such
as competition from deciduous tree species, decrease of
deciduous forests, climate change and human activity
(Bennett, 1995). Nowadays, the only natural pinewoods
on the British Isles are patchily distributed in Scotland
from latitude 55° N to 57° N and from longitude 3° W
to 1° W at altitudes up to 600 m (Mason et al., 2004).
According to the most recent available estimate, the native pinewood area in Scotland covers 18 000 ha in 84
separate pinewoods varying in size from <1 to >2000
ha (Anonymous, 1998); some populations are small
and sparse consisting of little more than 100 trees at a
density of <1 tree per ha (e.g. Martin, 1995). A substantial number of the native populations were already identified and described in the influential book ‘The Native
Pinewoods of Scotland’ by Steven and Carlisle (1959).
Natural pinewood regeneration is often prevented by
grazing of domestic livestock or wild deer, muir burning
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Re-colonization and history of pinewoods in
Scotland
north-western trees originate from refugia near south-west
Ireland or western France (Ballantyne and Harris, 1994;
Bennett, 1995), but this has not yet been verified by analysis of Irish macrofossils or potentially native pinewood
remnants. Alternatively, natural selection or genetic drift
(random loss of genetic diversity due to, e.g., sudden decrease in population size) may account for the differences,
as these populations are on the edge of the species’ range
and under strong oceanic influence. The wet, mild climate
is markedly different from that in other parts of the range
and provides potentially divergent selective pressures involving, e.g., pathogen attack, which may have driven biochemical differentiation. Biochemical similarity between
north-west Scotland and southern Europe may reflect the
effects of adaptation in a similar direction. However, if
variation was due to drift, this would imply lack of gene
flow between populations in western Scotland and elsewhere. In their mtDNA study, Sinclair et al. (1999) found
two molecular variants in Scotland, the less common type
being found in the western part of Scotland. Such differentiation further supports the view of colonization from
two directions. Similarly, multiple origins might be suggested by the presence of a unique, paternally inherited
chloroplast DNA (cpDNA) microsatellite allele that was
found only in the Wester Ross area (Provan et al., 1998).
However, this variant could also represent a recent mutation. Had it been an ancestral polymorphism it would
have been surprising that the allele was restricted to the
area, considering efficient pollen-mediated transmission of
cpDNA. Currently, the low number of mtDNA haplotypes
detected prevents precise definition of the colonization
routes of pine in Europe (Sinclair et al., 1999; Naydenov
et al., 2007; Pyhäjärvi et al., 2008), but further evidence
for separate evolutionary origins of eastern and western
pinewoods in Scotland has recently been found in candidate gene variation (Wachowiak et al., 2010).
UNDERSTANDING THE EVOLUTION OF NATIVE PINEWOODS
Management of pinewoods in Scotland
Since the late 1980s, protection and expansion of pinewoods have been included in various policies and grant
schemes (Mason et al., 2004). For example, the ‘Native
Pinewood Grant Scheme’ between 1989 and 2004 aided
the regeneration of existing pinewoods and created 48 000
ha of new pinewoods (16 per cent natural regeneration, 84
per cent plantations) while the ‘Native Pinewood Habitat
Action Plan’ aimed at increasing the remnant pinewood
area by 5600 ha by 2005 and assisting natural regeneration
(McIntosh, 2006). However, there are no recent estimates
available on the overall success of these projects or current coverage of (semi-)natural pinewoods. To guide seed
transfers, the Scottish pinewoods have been divided into
seven seed zones (Figure 1) such that when (semi)-natural
pinewoods are being expanded, in order to qualify for
grant support, planting stock must come from within the
same seed zone in an attempt to protect the local ‘genetic
integrity’ (Anonymous, 1998). For other planting objectives, such as timber production, the rules are somewhat
less restrictive. The seed zones are based largely on monoterpene studies (Forrest, 1980) so that biochemically similar
pinewoods are clustered within one zone.
The general purpose of seed transfer guidelines in forestry is to prevent planting of maladapted trees and to
maximize survival and growth. Ideally, management of
any economically important tree species would include
transfer restrictions, zoning species on the basis of climate, soil and topography and the results of provenance
trials replicated in multiple environments (White et al.,
2007). In other words, guidelines would take into account
broadly assessed patterns of local adaptation, with quantified evaluation of the phenotypic effects of seed transfers
along environmental gradients. As adaptation is driven by
the environment, and the spatial scale of environmental heterogeneity can differ widely among regions, transfer rules
Figure 1. Map of the current Scots pine seed zones in Scotland.
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and planting of non-native trees (Anonymous, 1998), and
many of the populations have been reduced to very small
numbers due to human interference. Also, in the past, trees
of poor growth form have often been left in the forests
while those considered to be superior from the silvicultural perspective have been felled and extracted for timber
(Mason et al., 2004). In such cases, the surviving trees
could negatively affect the quality of later generations
if they contribute to mating (Ennos et al., 1998; Mason
et al., 2004). However, the extent of such practices is not
known. In addition, undocumented quantities of trees of
continental origin have been introduced to Scotland since
the 19th century (Taylor, 1993; Forrest and Fletcher, 1995)
which potentially could cause genetic contamination of
local populations via pollen flow. The coverage of Scots
pine plantations, which are mainly used for timber production, totals 100,000 ha (Mason et al., 2004). However, the extent to which they contribute to the pollen
pool in Scotland is not known.
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Local adaptation is common in trees
Adaptations to local climate conditions have been described in many tree species using provenance trials (for reviews, see Howe et al., 2003; Savolainen et al., 2007) and
in Scots pine in other parts of its range. Despite significant
phenotypic differentiation, molecular marker variation
may show an opposite trend: due to efficient pollen-mediated
mixing of pollen pools even distant populations can
seem very similar at molecular markers that are not under
selection (e.g. Karhu et al., 1996). Phenotypic divergence
is mostly driven by environmental variation among sites.
In the northern hemisphere, due to differences in length of
the growing season and in the severity of seasonal periods
of stress, trees alternate between periods of active growth
and dormancy in order to avoid frost damage in the spring
or the autumn (Howe et al., 2003), and traits chosen for
studies are usually expected to be linked to these environmental factors. Growth patterns of Scots pine have been
extensively studied and, e.g., timing of growth cessation
is thought to be influenced by both photoperiod and accumulated temperature (Koski and Sievänen, 1985). In
common environment conditions, first-year pine seedlings
from colder areas generally set their terminal buds and become frost hardy earlier than the ones from warmer conditions (e.g. Hurme et al., 1997). Also, when seedlings from
different parts of Europe were grown under photoperiods
typical of 50° latitude, seedlings from northern regions set
buds earlier compared with seedlings from more southern
locations (Oleksyn et al., 1992). The same pattern has also
been found in height growth cessation of older trees (Repo
et al., 2000; Oleksyn et al., 2001). In Sweden, provenance
transfers from north to south resulted in increased survival,
but transferred provenances grew less than local ones due
to phenological differences (Eriksson et al., 1980; Persson
and Ståhl, 1990). On the other hand, northward transfers
increased mortality. Commonly, trees from sites experiencing
harsher – e.g. drier or colder – conditions grow more slowly
than those originating from milder environments, but
they are also more tolerant of stress (Howe et al., 2003).
Phenotypic divergence among populations is generally
thought to be due to differentiation at multiple underlying
genes driven by diversifying selection (for reviews on the
genetic basis of complex trait variation in trees, see Howe
et al., 2003; González-Martínez et al., 2006; Savolainen
et al., 2007; Neale and Ingvarsson, 2008), but so far candidate gene studies in trees have revealed more about past
demographic processes than about effects of selection (see
Lascoux et al., 2008). However, additional factors can also
contribute: in Norway spruce (Picea abies (L.) Karst.) it
appears that maternal effects, e.g. differences due to environmental conditions during seed development, can greatly
influence trait variation (Skrøppa, 1994; Skrøppa et al.,
1994; Johnsen et al., 2005), but in Scots pine such effects
seem much smaller (Ruotsalainen et al., 1995).
For maintenance of natural patterns of adaptive variation, the safest option is usually to use local seed material
or seeds from an environment that matches conditions at
the planting site (McKay et al., 2005; Aitken et al., 2008).
Using genotypes from other locations might negatively affect the local population due to outbreeding depression
(hybridization among excessively diverged populations)
leading to decreased fitness (Frankham et al., 2002). The
definition of ‘local’ depends on the species: in Douglasfir (Pseudotsuga menziesii (Mirb.) Franco), genetic differentiation can occur at 100–200 m (Campbell, 1979),
while populations of western white pine (Pinus monticola
Dougl.) seem genetically similar across a wide range covering 10° in both latitude and longitude (Rehfeldt et al.,
1984). Relatively short transfers can actually be beneficial for growth and survival: some conifer populations on
the northern edge of the species distributions have been
found to perform better if transferred southward of their
origin (e.g. Savolainen et al., 2007), while in other species
a similar response can be seen in transfers further north
(Carter, 1996).
Is Scots pine locally adapted in Scotland?
The current abundance of pinewood in Scotland is only
a small fraction of what it used to be, and potentially the
exploitation of the resources could have interfered with
local adaptation by randomly removing best-adapted trees.
However, the previous molecular marker studies based
on monoterpenes (Forrest, 1980, 1982) and allozymes
(Kinloch et al., 1986) and recent work on nucleotide variation in candidate genes (Wachowiak et al., 2010) show
that even in relict populations, levels of molecular variation
are similar to those observed in the continuous part of the
species’ range and, as is usual in the case of long-lived,
randomly mating forest trees with effective gene flow by
pollen (Hamrick et al., 1992), almost all of the variation
was found within populations. In theory, colonization
events (such as postglacial migration) are expected to decrease genetic variation through bottlenecks, but the life
history characteristics of trees (longevity, multiple age and
size classes, overlapping generations and late reproduction)
seem to buffer against these effects (Austerlitz et al., 2000).
For example, due to their postglacial colonization history,
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are not easily transferable between different countries.
Although apparently practical where field data are in short
supply, applying single-source data (such as monoterpenes
and allozymes which can be considered selectively neutral
molecular markers) to devise seed zones is likely, at best,
to poorly reflect adaptive patterns (Merilä and Crnokrak,
2001; McKay and Latta, 2002) or, at worst, results in detrimental effects on survival and growth if environmental
conditions vary greatly among the origin of seed and the
plantation site. Hence, while variation at molecular markers can accurately reflect other evolutionary features, such
as population structure, demography and mating system
(i.e. relative levels of inbreeding and outbreeding), they
should be applied in combination with data on environments and adaptively significant traits if seed zoning is to
be meaningful.
UNDERSTANDING THE EVOLUTION OF NATIVE PINEWOODS
Scotland’s populations form a unique part of the species’
range due to its oceanic climate; only in western parts of
Norway do Scots pine woodlands occur in similar environments (Øyen et al., 2006). To summarize climatic variation
among Scottish native pinewood sites, we extracted data
for all 84 pinewoods from the gridded (5 × 5 km) longterm average (1961–1990) UK Met Office data. Details on
the climate data generation can be found elsewhere (Perry
and Hollis, 2005). The climate data indicate that some
western populations in Scotland experience an annual
rainfall of close to 3000 mm compared with only ~700 mm
in the eastern parts. The length of the growing season
(the number of days with average temperature above +5°C)
varies from ~100 days in some eastern pinewoods to 300
days near the west coast. To study whether climatically
similar pinewoods were found within each seed zone, we
performed a principal component analysis to transform the
seven variables into two components (Figure 2, Table 1).
The data suggest that different pinewood sites within seed
zones do not form climatically uniform clusters, which indicates that climatic variation within one zone can be large.
For example, the north-west seed zone covers areas with
growing season lengths varying from ~130 to almost 300
days (Table 2). Because of this extensive within-zone variation and considering for instance the effects of provenance
transfers along latitudinal gradients in Sweden (Persson
and Ståhl, 1990), it is possible that current guidance results
in seedlings being planted at non-optimal sites. However,
Figure 2. Plot of the first principal components, which account for 69 and 24% of total variation, respectively, of climatic
variation among 84 native pinewood sites. The seven variables used are shown in Table 1. Current seed zones are represented
by different symbols, and the closer the populations are in the graph, the more similar they are climatically. PC1 represents
a gradient in annual rainfall and temperature: populations with more negative values are generally located in the west (high
rainfall, mild climate); positive values represent more eastern pinewoods with less rainfall and colder winters.
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northern Fennoscandian Scots pine populations are much
more recently established than those from Central Europe
(Willis et al., 1998), but despite their different histories, the
two parts of the range have very similar levels of nucleotide variation at candidate genes (Pyhäjärvi et al., 2007).
Some quantitative traits have been found to have less adaptive variation towards the northern range edges, but this
pattern is not seen in all traits, and differences could be
caused by varying selection pressure (Notivol et al., 2007).
In Scottish populations, low marker divergence among
populations suggests that gene flow among sites has, at
least historically, been sufficient to homogenize genetic
variation across populations (Kinloch et al., 1986). Also,
when comparing differentiation at cpDNA markers between Scotland and eight European mainland populations,
only ~1.5 per cent of the variation was found between
populations, indicating high levels of gene flow (Provan
et al., 1998). Within Scotland, 3.2 per cent of the variation
was among populations. Glen Falloch, a relict population
consisting of <100 trees, had the lowest diversity. Despite
drastic changes in the abundance of Scots pine in Scotland,
it seems that the level of neutral molecular variation remains high, with the majority of this variation being found
mainly within populations.
Despite the relatively small area covered by pinewoods
in Scotland, the environmental conditions among them
vary tremendously, providing potential for different selection pressures to lead to local adaptation. Furthermore,
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Table 1: List of climatic variables used in the principal
component (PC) analysis
Variables
Length of the growing season
February mean temperature
July mean temperature
Annual extreme temperature range
Air frost days per year
Ground frost days per year
Annual precipitation
Percentage of variation
PC1
PC2
−0.45
−0.45
−0.35
0.10
0.44
0.43
−0.30
69.20
−0.12
−0.12
−0.47
−0.72
−0.03
−0.13
0.46
23.99
Values in the table are correlation coefficients that vary
between −1 (strong negative correlation) and 1 (strong positive
correlation); the further the coefficient is from zero, the stronger
the association between the variable and the PC. PC1 is the main
component, explaining 69% of the variation.
height growth and slower development of frost hardiness
than other provenances. The only study where genetic parameters of adaptive variation were estimated was by Perks
and Ennos (1999) who also sampled four provenances,
each represented by 100 open-pollinated progeny (10 from
each of 10 mother trees). Seedlings were grown at one site
and measured at 7 years of age. Significant differentiation
among populations was found in diameter, height and bud
burst. Adaptive variation was found in all of the measured
characters, demonstrating the presence of genetic variation
for adaptively important traits, but due to the sample size,
estimates on the amount of adaptive variation are not precise. Also, while it was possible to show clear differentiation among populations in the traits considered, geographic
coverage was too limited to offer a full picture of patterns
of adaptive variation and the study did not attempt to link
observed trends to variation in climatic variables.
Ideally, in Scotland, the seed transfer guidelines for Scots
pine should be based on climatic and environmental characterization of the remnant pinewoods and provenance trials,
ideally replicated in different environments. Considering the
environmental variation that exists within Scotland, differentiation in traits of adaptive importance such as phenology,
stress tolerance and growth seems likely. For the maintenance of healthy pinewoods in Scotland and to update existing
seed transfer guidelines, it is essential to study adaptive variation in a number of traits across the whole Scottish range.
Maintenance of variation in pinewoods
The current seed zones of Scots pine are meant to protect the genetic integrity of local populations. However,
the definition of genetic integrity remains unclear. While
maternally inherited mtDNA variation might show differentiation among some of the pinewoods (Sinclair
et al., 1998), this does not mean that populations containing the diverged mtDNA lineages are unconnected. In
forest trees, the fact that most of the variation measured
with neutral molecular markers occurs within populations
can be attributed to efficient pollen-mediated gene flow
(Hamrick et al., 1992). Pollen flow can effectively mix the
Table 2: Range of climatic variation in four variables within each seed zone according to the UK Met Office long-term average data
(Perry and Hollis, 2005)
LGS (days)
FMT (°C)
JMT (°C)
AP (mm)
Seed zone
Min
Max
Min
Max
Min
Max
Min
Max
EC
N
NC
NE
NW
SC
SW
154
162
204
108
134
219
179
216
251
299
234
295
252
297
−0.8
−0.5
0.6
−2.0
−0.9
0.8
0.0
1.0
2.4
4.0
1.9
4.0
1.8
3.9
10.6
10
11.1
9.4
8.5
11.9
9.7
13
13.9
14.4
13.7
14
13.4
14.1
743
1215
1346
785
1912
1159
1164
1223
1778
2900
1343
2790
2904
2934
Seed zones: EC = east central, N = north, NC = north central, NE = north-east, NW = north-west, SC = south central,
SW = south-west. Climatic variables: LGS = length of the growing season, FMT = February mean temperature, JMT = July mean
temperature, AP = annual precipitation.
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it should be kept in mind that this data were generated
by interpolation from data from weather stations which
are not equally distributed across the country, and the precision of models for different variables varies (Perry and
Hollis, 2005). In addition to climate, there is also variation
in soil types; generally pine prefers freely draining podzol
and ironpan soils with relatively low nutrient levels, but
it is also found in brown earths, gleys and peats (Mason
et al., 2004). In wet conditions, poor drainage can lead to
poor growth and water logging.
Some evidence of local adaptation in the native pinewoods exists, but the data currently available are not extensive. Old provenance experiments set up by the Forestry
Commission in Scotland starting in the 1920s show that
populations from the mainland of Europe generally perform worse than Scottish material (Lines and Mitchell,
1965). Within Scotland, trees transferred from continental to strongly oceanic areas usually perform worse than
local populations, possibly due to pathogen stress (Mason
et al., 2004). Perks and McKay (1997) found significant
differences in root frost hardiness and growth in seedlings
from four provenances; for instance, seedlings from Loch
Maree, located in the west close to the Atlantic, had poorer
UNDERSTANDING THE EVOLUTION OF NATIVE PINEWOODS
and Mackay, 1996). Genetic variation in phenotypic traits
can be assessed by growing seedlings in a common environment in which environmental variation is kept to a
minimum (e.g. White et al., 2007). Only variation that can
be passed on to the next generation has evolutionary significance; therefore, estimating levels of such variation requires observations based on samples of a known family
structure (e.g. open-pollinated half-sib families). In the
majority of the forest trees studied, populations generally maintain high levels of adaptive variation (Howe
et al., 2003; Savolainen et al., 2007; Aitken et al., 2008),
even in range-edge populations under extreme conditions
(Savolainen et al., 2004; Notivol et al., 2007). In traits with
high levels of such variation, the change in the phenotypic
mean in response to new selection pressures can be rapid
(Falconer and Mackay, 1996). However, the life history
characteristics of trees can slow down rates of adaptation:
they are long lived, have long generation times and, due to
phenotypic plasticity, can continue to grow and reproduce
even in changed environments (Mátyás, 1996; Hamrick,
2004; Savolainen et al., 2004, 2007). For example, Swedish provenance trials suggest that climate-related mortality
in Scots pine occurs mainly in the early stages (first 20
years) of a tree’s life cycle (Persson and Ståhl, 1990). In
addition, if grazing pressure prevents natural regeneration,
the adaptive variation present in seedlings is lost.
Due to within-species genetic differentiation, adaptive
responses may vary among populations from different
parts of the range. According to Rehfeldt et al. (2002), the
immediate response to a warming climate will be positive
in Scots pine populations growing in harsh (suboptimal)
conditions, e.g. northern parts of Europe, while populations in mild (optimal) environments, e.g. southern Europe,
will suffer. Using simulations, Savolainen et al. (2004) concluded that while Finnish Scots pine populations have potential to adapt in timing of bud set and frost hardiness,
their response will be delayed and will lag behind the moving optimum, partly because of the already established
trees growing at the site. Increased mortality could facilitate adaptation by creating open spaces for regeneration
(Kuparinen et al., 2010). Specific forest management practices have also been suggested as methods for enhancing
adaptation; for instance, seedlings could be transferred
according to the predicted climate (St. Clair and Howe,
2007), or the interval between recruitment events could be
shortened (Kramer et al., 2008).
Before specific provenances can be chosen for future climate, data on the effects of tree transfers between variable
sites and on variation of adaptively important traits are
needed. With such data in hand, models may be developed
to test responses to specified variables, although making
predictions will remain challenging. Not only is adaptation
a complex process involving a number of traits simultaneously but environmental change may also involve changes
in the structure of stands, stress frequency, growth rates and
competition (Richardson et al., 2007), and it is impossible
to include all possible variables at the same time. Current
models have yet to combine genetics and ecology effectively,
e.g. models based on niche concepts often fail to take into
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gene pools of populations even if they are under diversifying
selection. However, although a significant proportion of
pollen can originate from sites located even a few dozen
kilometres away, the great majority of fertilizing pollen
usually comes from trees located within the same stand
as the mother tree (e.g. Smouse and Sork, 2004). Nonetheless, such mixing can contribute to the maintenance of
variation in adaptive traits (Slatkin, 1978; Barton, 1999)
which in turn can facilitate adaptation to changing conditions, as potentially beneficial alleles are introduced to
the gene pool of the population. Yeaman and Jarvis (2006)
studied the effects of environmental heterogeneity on variation in height growth in 142 populations of lodgepole
pine (Pinus contorta Douglas ex. Loudon) and found that
variability among the populations in drought occurrence,
annual precipitation and temperature explained 7–20 per
cent of the variation in height growth. Due to influx of genetic variation from other populations, gene flow can also
counteract adaptation, especially in peripheral populations
(Garcia-Ramos and Kirkpatrick, 1997). It is unlikely that
the native pinewoods represent independently evolving
units. Previous studies on Scottish pinewoods show low
levels of population differentiation (Kinloch et al., 1986;
Provan et al., 1998), although the gene flow estimates are
indirect and may not reflect current landscape-level processes (Sork et al., 1999; Smouse and Sork, 2004).
Ongoing climate change is affecting forests all over the
world, and changes in temperature, rainfall and frequency
of extreme weather events are expected (e.g. IPCC, 2007).
In Scotland, models predict warmer summers and milder
winters, with changes in the distribution of rainfall (Ray,
2008). In the east, summers are predicted to become drier,
possibly leading to drought, while winters may become
wetter, also a problem if it leads to water-logging and anaerobic conditions in soils. Warmer conditions may help
pests and pathogens spread to new areas. For example,
the northward spread of the pine processionary moth
(Thaumetopoea pityocampa, Dennis and Schiff) in Italy has
been attributed to increasing winter temperatures (Battisti
et al., 2005), and since the late 1990s, the occurrence of
red needle blight, a fungal disease infecting a wide range
of Pinus species, has increased in the UK with first outbreaks occurring in Scotland in 2002 (Brown et al., 2003).
Changes in climate can lead to situations where environments are no longer optimal for the populations growing in
them. Trees have experienced warming conditions before,
following the retreat of continental ice at the end of the ice
age (e.g. Davis and Shaw, 2001). In current conditions the
problem for trees is likely to be the rate of change which
is projected to be faster than that following the latest ice
age. After the last glaciation, European trees migrated at
average speeds of ~100–700 m per year, depending on the
species (Brewer et al., 2002; Magri et al., 2006). According
to Malcolm et al. (2002), trees will have to be able to
migrate at a rate of >1000 m per year to be able to keep
pace with human-induced change. This time, however,
trees face environments already occupied by other species.
For a change in fitness of the population, selection must
work on the variation present in the population (Falconer
541
542
FORESTRY
studied forest tree species in the world, and its biology
has been studied from DNA to the whole ecosystem level.
Native remnant pinewoods of Scotland represent a distinct part of the distribution because of their proximity
to the Atlantic Ocean, highly variable climate conditions and the 500-km distance to the closest continental
populations. Scots pine’s current coverage in Scotland is
only a fraction of what it used to be, but there are plans
to expand old and plant new native woodlands. If local
adaptation has occurred and provided that other management practices (e.g. cultivation and deer management)
support successful regeneration, modifications to existing
seed transfer guidelines could improve the effectiveness
of re-plantation efforts by minimizing seedling mortality
due to maladapted stock and the consequent ecological,
economic and strategic effects. Current transfer rules are
based primarily on molecular variation that does not reflect the likely pattern of environmental adaptation across
Scotland. To update the existing management guidelines,
further research is recommended, with a particular focus
on the following:
1 Range-wide progeny trials are needed to characterize
general trends of adaptive variation in traits such as
phenology, growth and stress tolerance in relation to the
environment. Such data can also reveal whether plantations have diluted local adaptation in native pinewoods.
2 Effects of provenance transfers along climatic gradients
can be obtained by replicating trials at multiple environmentally diverse sites across Scotland. In such a design,
the performance of local trees can also be compared with
that of trees from more distant sources.
3 Neutral genetic markers should be used to assess other
types of natural processes occurring in populations, such
as effects of population fragmentation, mating system
variation and current gene flow dynamics.
4 Potential role of pollen contamination can be assessed by
e.g. observing synchronization of reproductive events between plantations and nearby native woodlands.
Funding
Scottish Forestry Trust (M.J.S.’ Ph.D. studentship); Natural
Environment Research Council; the European Commission-funded
Network of Excellence EVOLTREE (FP6, contract #016322;
W.W.’s mobility grant under IA4 – human resource exchange).
Acknowledgements
The authors wish to thank UK Met Office for allowing the
use of their climate data, Chris Quine, Editor Gary Kerr and
an anonymous reviewer for comments that improved the
manuscript.
Conclusions
Due to its economic and biological significance across
two continents, Scots pine is one of the most thoroughly
Conflict of Interest Statement
None declared.
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account the possibility of adaptation, while genetic models
deal inadequately with ecology. There is a pressing need,
for climate change mitigation, for the development of new,
landscape-scale models that integrate these fields.
Studies on adaptive variation would also benefit from an
understanding of current patterns of genetic connectivity
among forest fragments. For example, if only local material
is used for planting and gene flow is limited, local genetic
‘integrity’ of small populations will be maintained, but the
population might become vulnerable to changing conditions
due to insufficient adaptive variation for natural selection to
operate on. In the case of isolated populations, variation
could be introduced by bringing seedlings from other locations; however, if gene flow occurs naturally and if natural
regeneration occurs, such practices might be unnecessary.
Due to differences in the sizes of the native pinewoods (from
<1 to >2000 ha), there might also be variation in the patterns of mating system. In small populations, random drift
becomes a powerful force shaping allele frequencies, and
along with inbreeding, this can lead to lower fitness as detrimental alleles increase in frequency (Frankham et al., 2002).
Like other pines, Scots pine is mainly outcrossing (Muona
and Harju, 1989), i.e. matings usually occur between unrelated trees, but self-pollination, the most severe form of inbreeding, is also possible due to the lack of a genetic system
preventing self-fertilization (Sarvas, 1962). Normally, selfed
embryos are aborted early in their development due to early
inbreeding depression. However, in stands with limited
numbers of trees, bi-parental inbreeding (mating between
relatives) is a potential risk. Despite efficient gene flow, inbreeding might become a significant factor when isolation
is extreme. In Scots pine, gene flow and mating system have
been studied in e.g. Spanish populations occurring in isolated stands in mountainous regions. Although the proportions of self-pollination were eight times larger (25 vs 3 per
cent) in a population of 36 trees spread across a 15-ha area
compared with that of larger populations covering thousands of hectares (Robledo-Arnuncio et al., 2004), the rates
were nevertheless low when the degree of isolation of the
trees is taken into account. In the small population, 4.3 per
cent of the pollen originated from other populations, the
closest one being located 30 km away (Robledo-Arnuncio
and Gil, 2005). Kärkkäinen et al. (1996) documented variation in levels of inbreeding depression within larger populations in Finland: outcrossing rates in northern populations
were somewhat lower than in the south, but inbreeding
depression was weaker in the north, possibly due to selection having already removed detrimental recessive alleles
exposed by inbreeding. Understanding the mating system
is also beneficial for studies on adaptive variation in phenotype, as departures from the assumed family structure can
lead to biased estimates of adaptively significant genetic
variation (Namkoong, 1966; Squillace, 1974).
UNDERSTANDING THE EVOLUTION OF NATIVE PINEWOODS
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