# Forests and global change: what can genetics contribute to the major forest management and policy challenges of the twenty-first century?

Bruno Fady, Joan Cottrell, Lennart Ackzell, Ricardo Alia, Bart Muys, Arantxa Prada, Santiago C. González-Martínez

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## To cite this version:

Bruno Fady, Joan Cottrell, Lennart Ackzell, Ricardo Alia, Bart Muys, et al.. Forests and global change: what can genetics contribute to the major forest management and policy challenges of the twenty-first century?. Regional Environmental Change, 2023, 16 (4), pp.927-939. 10.1007/s10113-015-0843-9. hal-02640944

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# Forests and global change: what can genetics contribute to the major forest management and policy challenges of the 21st century?

Running title: Genetics and sustainable forest management and policy

Bruno Fady¹, Joan Cottrell², Lennart Ackzell³, Ricardo Alía⁴, Bart Muys⁵, Arantxa Prada⁶, Santiago C. González-Martínez⁴

## Author affiliations

¹ INRA, UR629, Ecologie des Forêts Méditerranéennes (URFM), Avignon, France
bruno.fady@avignon.inra.fr

² Forest Research, Northern Research Station, Roslin, Midlothian, Scotland
joan.cottrell@forestry.gsi.gov.uk

³ Federation of Swedish Family Forest Owners, Stockholm, Sweden
lennart.ackzell@lrf.se

⁴ INIA, Forest Research Centre (CIFOR), Madrid, Spain
santiago@inia.es
alia@inia.es

⁵ European Forest Institute, Barcelona, Spain and University of Leuven, Belgium
Bart.Muys@efi.int

⁶ General Directorate for Environment, Valencia, Spain
gis_banco@gva.es

Number of words contained in the manuscript text, including abstract and
acknowledgements: 7460.

## Acknowledgements

This paper stems from the work of the stakeholder panel of the EU supported EraNet BiodivERsA project "Linking genetic variability with ecological responses to environmental changes: forest trees as model systems (LinkTree)" whose financial help is acknowledged. BF wishes to thank the French "Commission des ressources génétiques forestières (http://agriculture.gouv.fr/conservation-des-ressources)" (CRGF) and EUFORGEN (http://www.euforgen.org/) for insightful discussions. SCG-M acknowledges receipt of a Senior Marie Curie Intra European Fellowship within the 7th European Community Framework Programme (PIEF-GA-2012-
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328146) at the Department of Ecology and Evolution, University of Lausanne, Switzerland.

## Abstract

The conservation and sustainable use of forests in the 21st century pose huge challenges for forest management and policy. Society demands that forests provide a wide range of ecosystem services, from timber products, raw materials and renewable energy to socio-cultural amenities and habitats for nature conservation. Innovative management and policy approaches need to be developed to meet these often conflicting demands in a context of environmental change of uncertain magnitude and scale. Genetic diversity is a key component of resilience and adaptability. Overall, forest tree populations are genetically very diverse, conferring them an enormous potential for genetic adaptation via the processes of gene flow and natural selection. Here, we review the main challenges facing our forests in the coming century and focus on how recent progress in genetics can contribute to the development of appropriate practical actions that forest managers and policy makers can adopt to promote forest resilience to climate change. Emerging knowledge will inform and clarify current controversies relating to the choice of appropriate genetic resources for planting, the effect of silvicultural systems and stand tending on adaptive potential and the best ways to harness genetic diversity in breeding and conservation programs. Gaps in our knowledge remain and we identify where additional information is needed (e.g. the adaptive value of peripheral populations or the genetic determinism of key adaptive traits) and the types of studies that are required to provide this key understanding.

Keywords: sustainable forestry; assisted migration; climate change; adaptation; genetic diversity; gene conservation.

## Introduction

The development of appropriate and informed policy for the conservation and sustainable use of forests worldwide, during the 21st century and beyond, presents several challenges. The long life-span of trees makes them susceptible to both short and long term environmental disturbances (Alberto et al. 2013). The natural cycles of environmental disturbances are being modified by human activities and this is predicted to intensify in the future with major effects on biodiversity (Alfaro et al. 2014, Sala et al. 2000). Thus, policies that guide forest management decisions must be amenable to both short and long term assessment. Innovative forest management and policy approaches are necessary to meet the often conflicting demands of a changing society and the need to deliver an array of provisioning, regulating and socio-cultural ecosystem services (MEA 2005, TEEB 2012). To ensure effective implementation in practice, these new approaches need to be more responsive to the future needs of society in general, more amenable to cross-sectorial cooperation and more evidence-based than is currently the case (Vanhanen et al. 2007).
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Because of the incomplete scientific evidence on the effect of silviculture on long
term forest sustainability and because forests provide a wide range of goods and
services for society, forest-related societal challenges can result in controversy,
polarization of views, stalemates and deadlocks (van Eeten 1999). While some of the
controversies are philosophical in nature, others could be resolved by further scientific
research. For example, it is debatable whether management based on natural
regeneration is more sustainable than planting in reforestation programs (Espelta et al.
2003, Morrissey et al. 2010) because the outcome will depend on a number of factors,
including availability of sufficient appropriate seed sources for natural regeneration,
ecological traits of the planted trees species, etc. Similarly, there is lack of clarity
regarding the relative merits of gradual tree selection versus clear-felling as a
harvesting strategy for timber production in commercial forests (Lundqvist et al.
2013). Other controversies relate to the relative benefits of stand conversion compared
to ecological restoration; the use of exotic species (or non-autochthonous parent
material of native species) instead of native material of local origin as a source of
forest reproductive material in plantation forests; the use of multiple versus single
species forest plantations; the acceptance and application of clonal forestry and the
use of genetically-modified trees in intensive forestry; among others (MCPFE 2008).

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In addition to these uncertainties and societal controversies, there is the recognition
that climate change will have an impact and should therefore be included in these
longstanding debates (Noss 2001). The realization that many local habitats will cease
to offer the same potential for forest cover and production as they have in the past
represents a serious paradigm shift for forestry. The uncertainty regarding the
magnitude of the change at different spatial scales presents yet another difficulty for
the development of appropriate forestry policy. For example, due to their location at
the rear-edge of species distributions, countries in the Mediterranean region are
generally expected to experience the consequences of climate change more abruptly
than the more northerly countries of Europe (Hampe & Petit 2005). Nevertheless,
habitat changes are also expected to be severe at high latitudes and generally greater
in the lowlands than at high elevations (Loarie et al. 2009). There is therefore, a need
for sound, informed policy development that is tailored to both local and regional
scales to ensure that the most appropriate forest management strategies are
implemented. The recognition that there is no single approach underlines the
importance of selecting appropriate practices that fit the conditions and objectives of
each particular situation (Millar et al. 2007).

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The term adaptation (see Annex 1 for definitions of this and other terms used
throughout the paper) is commonly used to cover a range of purposes in the context of
global, and particularly climate, change (Biesbroek et al. 2010). In forestry, the term
is generally used to encompass all aspects of forest management that need to be
modified to prepare forests so that they can continue to provide their usual ecosystem
services under (the uncertainties of) global change (Bernier & Schoene 2009), as in
“adapting forests to climate change” or “adaptive forestry”. However, from a genetic
perspective, adaptation has a different, more restrictive meaning, i.e. the evolutionary
capacity of a population to cope with a changing environment through genetic
changes. The ability of forests to adapt in a genetic way, i.e. genetic adaptation, to the
new environments that will result from climate change depends on: (i) the speed and
intensity of climate change across species ranges, (ii) the existence of genetic
diversity among individuals in natural populations and (iii) the ability of this diversity to migrate between populations through pollen and seed movement, i.e. gene flow (Savolainen et al. 2007; Kremer et al. 2012). Populations with high genetic diversity for adaptive traits (i.e. rich in genetic resources) are more likely to be able to respond via natural selection to the challenges posed by climate change (Jump et al. 2008). The adaptive potential (Scotti 2010) of forests worldwide thus depends on the genetic resources found both within populations and among forest stands that are connected via effective gene flow.

In 1994, in recognition of the importance of genetic diversity for forest sustainability, FOREST EUROPE (the pan-European political process for the sustainable management of the continent's forests, http://www.foresteurope.org/) created EUFORGEN (http://www.euforgen.org/), a collaborative network of European countries whose remit is to promote the conservation and sustainable use of forest genetic resources. However, despite this high level recognition of the importance of forest genetic diversity, the National and European forest policy agencies frequently ignore this aspect when developing indicators and guidelines on how forest management should prepare for and react to climate change (Koskela et al. 2007). Similarly, the role of forest genetic resources is often omitted from the recommendations (Graudal et al. 2014) issued by habitat and species conservation agencies and non-governmental organizations, such as those within the framework of the European Habitat directive (Council Directive 92/43/EEC). This is despite the consideration that forest genetic resources in forest management strategies are key in ensuring that forests can adapt to climate change (Lefèvre et al. 2013). The overall lack of attention given to the genetic dimension of forest adaptation is probably due to a general lack of knowledge of the recent advances in forest genetics among forest managers and policy makers.

In this article, we review the major challenges faced by forest managers and policy makers in temperate Europe in the 21st century for which recent progress in genetics can contribute to the development of appropriate practical solutions. We deliberately focus on the practical issues that arise from these forest challenges, listing them as they are perceived in a management context. Seven major challenges emerged from discussions between the stakeholders of the Linktree project who had direct roles in developing policy and appropriate management to prepare forests for climate change. These range from natural regeneration to assisted migration and from conservation to breeding. We address naturally regenerated and plantation forests but exclude genetically modified organisms from our report as they are not currently available for most species of interest to European forestry. We present examples where uncertainty adds complexity to management decisions. For these examples, we provide insights into how science, and particularly an understanding of genetics, can help to inform policy directions. In doing so, we aim at bridging the gaps between science, management and policy which typically operate within different spheres of influence and across different time frames and are not always driven by the same concerns.

We also aim to demonstrate that some key forest management and policy questions can be resolved by genetic studies, in particular those using new generation technology that is now increasingly becoming accessible and of practical use for forest trees. These studies give insights into the current and future consequences of particular management strategies on the evolutionary response of tree populations
and, in turn, can guide how management strategies should be adapted to foster the evolutionary potential of forests under changing conditions. Figure 1 shows a summary of the processes affecting the genetic diversity of forest trees and how management can use and modify these processes to prepare forests for climate change.

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Figure 1. Processes affecting the genetic diversity of forest trees and how management can harness these processes to prepare forests for climate change. The pressure applied by forest management on the state of genetic diversity has impacts that affects the forest as a whole. Climate change drives the system and the selection pressure it imposes can be reduced by management practices.

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## Challenge 1: Will the genetic resources available in natural forests remain appropriate and be sufficient under climate change?

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This question relates to the adaptive potential of forest tree populations and their reaction to climate change. Depending on the management goal (e.g. production, protection or recreation), phenotypic traits of interest to managers will be wood quantity and quality or survival and health. Standing genetic variation and the phenotypic plasticity found in forest tree populations provide the means to cope with the new conditions.

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Climate envelope modelling shows that species distribution ranges and the species composition of forests are likely to change considerably over the coming decades (e.g. Thuiller et al. 2005). However, this modelling approach, based on correlation of geographic distribution with a range of climate variables, cannot accurately predict the future distribution of species because it does not take into account important ecological and evolutionary processes such as competition at the community level, dispersal, phenotypic plasticity and adaptive potential. In the few studies in which genetic diversity has been included in the modelling frameworks, it has been found to modify the predicted range of forest tree species under climate change considerably (Benito-Garzón et al. 2011, Oney et al. 2013). This highlights the urgent need for

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appropriate genetic methods and data to determine the adaptive potential of existing material.

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Currently, the best available source of genetic data on phenotypic traits of importance for local genetic adaptation comes from “common garden” trials which contain material sourced from a range of origins, called provenances in the forestry literature.

Published results from such trials show that adaptive genetic diversity is large in most forest tree species, mainly within but also among populations (Ducousso et al. 1996), although there are remarkable exceptions (e.g. *Pinus pinea*, Mutke et al. 2010). These trials also provide evidence of local genetic adaptation across the range of species and demonstrate that most tested provenances display large phenotypic plasticity for key adaptive traits when grown under different climatic conditions (Rehfeldt et al. 2002).

These findings are important because they indicate that, provided climate shifts are not too steep and some degree of growth yield reductions are acceptable for management objectives, current genetic resources of many tree species are likely to remain appropriate in many of their current habitats, particularly within the core of geographic distribution ranges.

Unfortunately, common garden trials are only available for a restricted number of commercially important forestry species, they rarely include representatives of all the ecologically relevant seed sources and in many cases the trials are insufficiently replicated across the distribution range of the target species. Notably, peripheral populations (i.e. coming from the ecological and geographical distribution margins)

are under-represented in existing field trials. There is therefore an urgent need for the establishment of pan-European and range-wide species and provenance trials of novel and native species (see for example the REINFFORCE initiative,

http://reinfforce.iefc.net/). These should be established using provenances from across the distribution range grown at multiple sites which include locations within the current distribution ranges as well as those that are beyond the current range but are predicted to become suitable in the future for the target species.

When field trials already exist, their analysis at a national or range-wide scale could provide immediate answers to some of the questions raised by managers regarding the potential of their populations to adapt to climate change (see for example www.treedivnet.ugent.be, an international network of common garden experiments where monocultures are compared with mixed species or mixed provenance treatments, and EU funded initiatives, such as Trees4Future, http://www.trees4future.eu/, and the COST action FP1202, http://map-fgr.entecra.it/).

The measurement of meaningful adaptive traits in these trials is recognized to be challenging in terms of the time and expertise required to obtain them (e.g. drought tolerance, phenology, seed production, and other life history traits, Chambel et al.

2007) and rapid and cost-effective phenotyping methods of many hundreds of individuals need to be developed if the full benefit of these expensive trials is to be secured (Neale & Kremer, 2011). Progress in fast phenotyping approaches is being made with modern methods such as terrestrial Lidar scanning for measurement of tree size and form (Eysn et al. 2013), chlorophyll fluorescence for estimating stress via photosynthetic efficiency (Salmela et al. 2011) and others (Alia & Majada 2013)

becoming available. Greenhouse trials, in which treatments such as drought and pests and diseases can be imposed, represent a useful and sometimes alternative strategy to expose and assess standing genetic variation and phenotypic plasticity in key traits for
284 seedlings and young trees (Sagnard et al. 2002, Chambel et al. 2007). Results from
285 these trials will provide an understanding of variation in adaptive traits and how it is
distributed across the landscape. This knowledge will form a framework with which
287 to guide advice on the scale of current and future movement of planting material can
288 be practiced without the fear of maladaptation. It will also contribute to models which
289 aim to determine the evolutionary potential of our forests to cope with climate change.
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291 Advances in molecular approaches are beginning to make it possible to link
292 phenotypes to variation in genetic markers (González-Martínez et al. 2006). For
293 example, such approaches have already been used to explore cold and drought
294 resistance in several conifers (Neale & Kremer 2011, Eveno et al. 2008, Grivet et al.
295 2011). By taking advantage of new cost-effective genotyping-by-sequencing (GbS)
296 methods it is now possible to adopt a genome scanning approach to generate millions
297 of data points across the genome. In one of the first such studies in forest trees it was
298 shown that extensive variation exists within natural populations of pines for genes
299 linked to ecologically-relevant traits (Parchman et al. 2012). Ultimately, it is
300 anticipated that these approaches will provide managers with the practical tools to
301 determine whether their targeted trees and stands have the capacity to adapt to climate
302 change, at low cost even in non-commercial species.
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304 In conclusion, most genetic studies to date indicate that there is a large amount of
305 heritable adaptive variation available in tree species on which natural selection can
306 operate. Thus, the rather dramatic predictions made by climate envelope models of
307 large scale changes in forest distribution within the coming decades require
308 reassessment and refinement to include genetic processes. However, adaptive
309 potential depends on the species and local ecological conditions and demographic
310 constraints could severely limit the capacity of populations to evolve under the most
311 severe climate changes. Thus, although usually appropriate, management scenarios
312 based solely on locally existing forest material and genetic resources may be
313 hazardous particularly at range and ecological edges.
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## Challenge 2: What should be monitored to determine whether the native species in natural woodlands are currently at risk under climate change?

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319 Both a lack of genetic adaptation and demographic collapse can drive populations to
320 extinction. Determining which genetic and demographic thresholds will lead to
321 maladaptation is crucial to make informed management decisions, particularly in
322 forests where, despite predictions, evidence of decline due to climate change is not yet
323 strong. This can be achieved by genetic monitoring.
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326 Although forest monitoring is often carried out by countries to assess the state of their
327 forests and the social, economic and environmental benefits they derive from them, it
rarely includes any assessment of genetic resources (Graudal et al. 2014).
328 Aravanopoulos (2011) defines genetic monitoring as "the quantification of temporal
329 changes in population genetic variation and structure". He suggests that genetic
330 monitoring should focus on ecologically and economically important forest tree
331 species and on four key genetic processes: (1) natural selection, (2) genetic drift and
332 (3) gene flow and one demographic process linked to gene flow: the mating system.
333 Carried out at regular intervals, genetic monitoring will provide much needed
334 information on adaptive potential. Protected areas where there is less human mediated
335 interference and management practices are carried out with a lighter touch than in
336 other forest types constitute excellent sentinels of the effects of climate change and
337 are thus also appropriate candidates for genetic monitoring.
338 Neutral molecular markers can now be used with relative technical and financial ease
339 to monitor genetic drift, gene flow and the mating system. The relationship between
340 neutral genetic diversity and standing genetic variation at fitness related genes in large
341 populations is not straightforward (Le Corre & Kremer 2013) and genomic
342 approaches are not yet sufficiently generally accessible to be applied to clarify the
343 relationship. There is therefore a need to determine the most efficient ecological
344 proxies that could be used instead to assess the adaptive potential of forest
345 populations by forester. Aravanopoulos (2011) suggests that several demographic
346 indicators, such as: age class structure, filled seed set and seedling density can be used
347 as these proxies. A system of genetic monitoring for forest tree species broadly based
348 on the concepts discussed here, was proposed and successfully tested in Germany for
349 providing early warning signs of environmental changes affecting forests (Konnert et
350 al. 2011).
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352 Studies using novel approaches will be needed to assess standing genetic variation
353 and adaptive potential directly. General information can come from progeny tests in
354 common gardens (Houle 1992) or *in situ* experimentation (e.g. reciprocal
355 transplantation schemes), where heritability and genetic variance can be measured.
356 Sophisticated association and genome-wide ecological studies will increasingly
357 provide information on standing genetic variation available for adapting to changing
358 environments (see references above in Challenge 1). It is expected that genes involved
359 in genetic adaptation will vary along the geographical range of species (see Hancock
360 et al. 2011 for the model plant species *Arabidopsis thaliana* and Prunier et al. 2012
361 for an example in forest trees), thus the establishment of an inventory of such
362 adaptively important genes (and their allelic variants) across the full species range is a
363 priority for current and future applied genetics research.
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365 In conclusion, monitoring the potential of forests to adapt genetically under climate is
366 necessary over broad areas to inform management. Monitoring based on parameters
367 used in classical forest management (such as adult age classes, seedling density and
368 presence of pests) can now be coupled with molecular genetics assessment methods to
369 provide early warning signs of maladaptation risks. Incorporating genetic monitoring
370 as a component of the current pan-European forest monitoring efforts would provide
371 key indicators of evolutionary and adaptive potential.
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374 **Challenge 3: Is assisted migration the answer for managing forests and their habitats under climate change?**
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377 This question typically arises when sound evidence suggests that current genetic
378 resources at a site will cease to offer an appropriate option under future climate
379 (Challenge 1) and introduction of non-local resources is being considered. Assisted
380 migration concerns the sourcing of seed and planting stock and can take two forms:
381 the use of exotic species (i.e. species that do not naturally occur at the planting
382 location or, more generally, within the country) or the use of non-local genetic
383 resources (i.e. populations of naturally occurring species which originate from other
parts of the species distribution range). In management plans, the definition of assisted migration is often restricted to the use of exotic species and the option to use conspecific material from a different origin is frequently overlooked.

The use of exotics has been practiced in forestry for centuries, often with great success in terms of sustaining wood production (e.g. *Pseudotsuga menziesii*, *Pinus radiata*, *Abies grandis*, *Picea sitchensis*, etc introduced in Europe). Such successful introductions are often the culmination of extensive trials and on the basis of their results, the elimination of many species from the candidate list. Although there are numerous examples of successful introductions (e.g. mountain habitat restoration in France in the 19th century (Charry 1996, Bartoli & Musch 2003), there are also notable instances of spectacular failures. A classic example is eastern white pine, *Pinus strobus* L., a five-needle pine which was introduced into France from North America in the mid-16th century, and into England and Germany 150 and 300 years later, respectively. In the mid-19th century the European plantations were colonized by the pathogenic fungus *Cronartium ribicola* of Asian origin, with catastrophic results due to lack of resistance to the disease (Karlman 2001). Consequently, this species is now rarely used in European forestry. Also, some of the successfully introduced species in Europe have become invasive (e.g. *Robinia pseudoacacia* and *Quercus rubra*), causing habitat management problems on a massive scale.

The translocation of genetic resources from one region of the species distribution to another is also a form of assisted migration (sensu Richardson et al. 2009), i.e. within-species assisted migration or “assisted gene flow” sensu Aitken and Whitlock (2013). Again, foresters have used this management option extensively at least since the 19th century, very often as a strategy for planning large scale reforestation programs when local seed supplies were insufficient or thought to be less productive than non-local resources (Bartoli & Musch 2003) or to overcome budget limitations: for example 4000 tons of oak seed were brought into Germany for planting from south-eastern Europe (Kleinschmit, 1993); cherry seedlings were sold in Europe from seeds obtained in jam factories (Kleinschmit & Kleinschmit, 2009). Here again, despite some general success, maladaptation of the planting stock has also resulted in severe economic lost (see for example the massive dieback of Portuguese seed sources of maritime pine planted in South West France after the 1984-1985 severe winter frost, Timbal et al. 2005).

It is now well recognized that assisted gene flow is neither risk-free for the target species themselves nor for their associated communities (see for example Aitken & Whitlock 2013). This understanding underpins the European Council Directive 1999/105/EC on the marketing of forest reproductive material which requires seed companies to attach clear passport data to traded resources. This traceability allows forest managers to make informed decisions regarding the likelihood of maladaptation of purchased planting stock and the potential ecological consequences of using it. Some managers have attempted to reduce the risk of planting failure under climate change by mixing seed lots within and among regions of provenance and among years (i.e. ‘composite provenancing’). However, according to Ennos et al. (1998) the use of assisted gene flow for such insurance purposes should only be considered if levels of variation within indigenous populations are so low that they are unlikely to be able to adapt to future conditions by themselves and if the imported material is considered to
be better adapted to future climatic conditions than the indigenous populations, which are both difficult to ascertain (see Challenge 2).

Thus, assisted gene flow could offer a reasonable solution for situations in which local resources are declining, adult tree mortality is above a set threshold and natural regeneration is low or absent despite supplementation efforts using locally sourced seed (Ledig & Kitzmiller 1992, Hubert & Cottrell 2007, CRGF 2008). This is a form of genetic rescue where hybridizing local resources with genetically unrelated resources could restore fitness (Hedrick et al. 2011). It requires seed material to come from stands "preadapted" to a future (and uncertain) climate and it is not free of risk as it could also result in outbreeding depression (i.e. lower overall fitness because of disruption of co-adapted gene complexes). Ecological risks, such as within-species introgression or modification of biotic interactions, although somehow attenuated compared to those from exotics, are also present with assisted gene flow (Aitken & Whitlock 2013). Broad scale analyses such as those of Rehfeldt et al. (2002) for *Pinus sylvestris*, where the fitness of exotic provenances is compared to that of the local provenances at a trial site, enable the appropriateness of local resources to be evaluated and the need for transfer across seed zones to be assessed.

In conclusion, assisted migration programs can disrupt local genetic adaptation and affect the present and future dynamics of forest genetic resources. We can take advantage of past experiences in the introduction of species and provenances, but these are not real experiments to test the effectiveness of present-day assisted migration programs. Caution is needed in the use of extensive assisted migration as the responses will likely affect not only trees but also the whole forest community in which they are established.

**Challenge 4: Is natural regeneration the most appropriate management technique for promoting the adaptation of natural forests to climate change?**

Natural regeneration is being promoted in a European context of close-to-nature forest management for several reasons including those that relate to cost reduction, decreased disturbance, better selection potential due to larger seedling density and conservation and continuous evolution of the local gene pool. It is thus generally considered to be the most appropriate management method in protected habitats. However, the success of natural regeneration is variable and factors such as soil type, abundance of competing weeds, herbivore pressure, species light requirements and availability of seed sources may force management to consider other regeneration approaches.

Whether natural regeneration is a better strategy for regenerating forests than plantation remains an open question (Espelta et al. 2003, Morrissey et al. 2010), but it is clear that within this debate, genetic considerations are rarely given the importance they deserve (except when the management goal is to use the local gene pool or GMOs are involved). This is unfortunate as genetic diversity considerations can be an important basis for preferring one strategy over the other (Ledig & Kitzmiller 1992), particularly in small forest stands (Vranckx et al. 2014) and their relevance is central to climate change related issues (Koskela et al. 2007, Alfaro et al. 2014).
The question geneticists must address to help management in this context is whether the level of genetic diversity (and the amount of seedlings) available from natural regeneration is sufficient (Vranckx et al. 2014). Decisions regarding whether natural regeneration is more appropriate than planting for the maintenance of genetic diversity (and ultimately adaptive potential) can be informed by some level of genetic monitoring based on appropriate methods (Aravanopoulos 2011 and see Challenge 2). If the stand to be regenerated is genetically of average or above average diversity for the species, and if seedlings are abundant, then natural regeneration is likely to be the most appropriate option. When using natural regeneration, managers should make sure that: i) adult trees contributing to natural regeneration are plentiful and not too similar phenotypically (see minimum requirements for conservation of genetic diversity in Koskela et al. 2013), ii) varied silvicultural treatments are implemented at the landscape scale (see the effect of structure and density on the spatial genetic diversity of seedlings in Sagnard et al. 2011) and iii) enough time is left for natural regeneration to be thinned by varying levels and forms of natural or silviculture-based selection (competition for light and water, resistance to herbivores, pests and diseases).

If natural regeneration is scarce and/or a species in the stand has significantly lower than average genetic diversity which may result in detrimental effects such as fixation of deleterious alleles at adaptive loci (see how to monitor in Challenge 2), then a strategy based on planting is likely to be beneficial. Managers who adopt this approach should ensure that there is high genetic diversity in their planting stock by insisting that seed lots used for plantation are based on equal contributions from at least 30 to 50 seed trees (legal standards of most countries do not include this requirement). They should also give careful consideration to the geographic origin of the stock and choose the source that is most likely to be adapted to the conditions at planting site.

Greater mortality (and thus potential for selecting advantageous phenotypic traits) is expected under a natural regeneration regime than one based on planting. A plantation will typically install 1200 to 2500 seedlings/ha, whereas this number increases by one or two orders of magnitude with natural regeneration. Amm et al. (2012), for example, show that selection intensity could be as high as 0.0001 between the seed production and the recruitment stage in *Abies alba* Mill. For any given heritable phenotypic trait of importance to forestry, it would be necessary to increase initial densities of plantations dramatically to reach the same level of selection intensity as that of natural regeneration, and these are unlikely to be acceptable under current operational conditions.

In conclusion, to provide sufficient material on which natural selection can operate to bring about evolutionary change, the option of natural regeneration is likely to be most appropriate as it typically provides a much larger base population than is the case for plantations. Forestry will need to rethink its strategies for long rotation species to make it possible for selection to occur in those areas where climate change is expected to have its strongest impacts.

**Challenge 5: Should/can the conservation of genetic diversity be included as a component of habitat and species conservation strategies?**
533

Managers tend to give much less consideration to the conservation of the genetic resource (gene conservation) than to that of the species and habitat. Habitat conservation usually aims to protect a set of particular ecological processes that sustain a defined range of species, often rare or endangered, or are particular to an ecosystem. In contrast, the in situ conservation of a genetic resource aims to maintain the process of genetic adaptation under natural selection and demographic shifts so that the individuals of a target species which are best adapted to current conditions survive and breed to produce the next generation. Thus, a holistic biodiversity conservation strategy consists of several different strands, the aims and approaches of which are not necessarily compatible.

544

Management of protected areas is mostly directed towards the conservation of rare and endangered species and habitats (Peterken 1977, Klein et al. 2009) and there is little direct focus on gene conservation. In contrast, *in situ* gene conservation is generally practiced in large plots consisting of the major forest tree species in common habitats where genetic processes can occur. The networks of gene conservation units for forest tree species in Europe follow a set of minimum requirements, including range-wide genetic diversity representativeness and their management procedures aim to shield conservation units from maladaptive gene flow (see Koskela et al. 2013 for a full description). Thus, networks of gene conservation units provide a level of protection of biodiversity that is seldom considered in protected areas that, we believe, warrants worldwide recognition such as categorization as IUCN protected areas. Gene conservation units are also useful for demonstrating that the integration of genetic principles into management does not hinder silviculture and forest planning and instead, can significantly contribute to adaptive forest management by introducing evolutionary considerations into everyday practice (Lefèvre et al. 2013, Koskela et al. 2013).

561

The application of the greenway or ecological corridor approach used by planners to establish a network of linked land and water habitats in the landscape (Ignatieva et al. 2011) may in some cases reconcile habitat, species and gene conservation strategies. Corridors can facilitate both migration and gene flow which are key processes in the maintenance of adaptive potential (Savolainen et al. 2007). Gene flow is generally predicted to make a strong contribution to genetic adaptation (as it maintains the overall genetic diversity, on which natural selection operates) in most forest tree species (Kremer et al. 2012). However, large gaps of knowledge still exist. For example, the effects of different forest landscape components on the rates of long-distance gene flow are currently poorly understood. Although studies tend to demonstrate that fragmentation indeed increases genetic drift and loss of fitness (Vranckx et al. 2011) and the presence of woodland corridors and hedges generally improve genetic connectivity, the distance that native forests have to be apart to experience significantly reduced genetic connectivity is species specific and depends on pollen and seed dispersal. Monitoring whether ecological corridors really do promote gene flow, evolutionary processes and migration to more suitable habitats, as well as identifying which species are most at risk by fragmentation, remain a necessity.

580

The role of habitat connectivity is particularly controversial for the maintenance of evolutionary potential for populations from the periphery of the distribution range and
this is particularly relevant in the context of climate change. Models have shown that pollen flow may in fact decrease genetic adaptation rate in some instances (Kuparinen et al. 2010). Leading edge peripheral (as well as numerous small) populations in northern Europe do not always demonstrate local genetic adaptation (Leimu & Fischer 2008). For these, pollen flow from the core of the distribution area may be beneficial, particularly from a climate change perspective as core populations are better adapted to the future conditions that are predicted at the leading edge. In this case, connectivity will reduce inbreeding and drift at the leading edge (Willi & Fischer 2005). Conversely, disjunct populations at the rear edge, with a long history of demographic stability (Hampe & Petit 2005), will suffer from maladaptive gene flow from core populations (Lenormand 2002). Rear edge populations, geographically or ecologically disjunct from species distribution ranges, may constitute hotspots of evolutionary potential provided their census size is not too small (Lesica & Allendorf 1995). Plans to reconnect these to other populations within the main distribution range of the species should therefore be resisted to maintain their genetic distinctiveness. However, on the other hand, gene flow from these rear edge populations could be helpful for the adaptive evolution of core and leading edge populations in of the to climate change.

In conclusion, gene conservation of forest tree species should be viewed as an integral part of biodiversity conservation, alongside that for species and habitats. As each conservation focus has discrete objectives that may require different management strategies, it is important to run them in parallel and non-exclusively over the landscape at national and regional levels. However, protected forest areas in which there is little or no active management can sometimes directly contribute to the conservation of forest genetic resources and genetic diversity monitoring (Challenge 2) should become a priority concern there for the most relevant species.

**Challenge 6: Do the current objectives of tree breeding programs address climate change sufficiently? Does the current usage of forest reproductive material represent the best practice in preparation for climate change?**

Tree breeding involves selecting individuals that have particularly desirable traits and crossing these individuals to improve the trait or traits of interest within populations. Breeding programs can therefore produce genetic resources which are valuable in enabling forests to adapt to climate change and to provide more and/or better ecosystem services. Historically, selection in these breeding programs has targeted commercially important traits such as growth, wood density, stem straightness and complete resistance to particular pathogens in clonal forestry (e.g. poplars), with the goal of marketing the desired product within a minimum time span. This breeding paradigm only makes sense if the environment remains constant during the entire production rotation.

Despite risks related to climate change in the forest sector, many European countries continue to subsidize and support the use of a limited set of clones or varieties produced by breeding programs established long ago, and this for a limited set of commercial tree species (Alia & Majada 2013). Many species of interest in the 1970s have dropped out of financial support schemes and seed orchards (mostly for conifers) have been neglected or even destroyed and are no longer used to provide seed.
Moreover, new breeding efforts are scarce outside a few dominant commercial species. Both practice and breeding efforts are thus too limited and inadequate for the challenges of the 21st century (which is recognized by the community and has led, for example, to the EU initiative Trees4Future, see Challenge 1). A few breeding programs, however, are now incorporating in their objectives functional traits of relevance to adaptive potential (e.g. water use efficiency, phenology along with the more traditional traits of growth and wood quality, e.g. the Maritime Pine breeding programs in France and Spain, Bouffier et al. 2013), providing an example to follow in other species.

Modern breeding methods based on genomic selection offer great potential for multipurpose breeding programs. Genomic selection has the potential to accelerate breeding in long-generation species, substantially increasing genetic gains while also providing a flexible framework to incorporate changes in breeding targets. It is already widely used in animal and crop selection but has only recently started to be applied to forest trees in species such as eucalypts. Advances are also being made rapidly towards implementation in conifers and other broadleaves such as poplar (Plomion et al. 2015). By genotyping at regular intervals across the genome with a large number of markers (classically over 10 markers/cM, i.e. over 15,000-30,000 markers in forest trees), genomic selection approaches are able to predict phenotypes with variable degrees of accuracy, depending on the effective population size of the base population, linkage disequilibrium, heritability and the genetic architecture of the desired trait (Grattapaglia & Resende 2010).

There are calls from the research community for breeding programs to consider more seriously genetic resources outside the current very few commercial species, to form links with conservation programs and to address traits and uses that have not yet been considered (Fins et al. 2006). For assisted gene flow and ecological restoration for example, breeding for increased genetic diversity and evolvability alone might be a reasonable goal in itself (Alia & Majada 2013, Lefèvre et al. 2013). Benefits from state-of-the-art selection theory and practice can be down-scaled and used in so called low-input breeding programs. Low-input breeding carries both the ideas of selection towards rusticity and a highly cost-effective selection process in terms of direct benefits to users (Dawson et al. 2008). Low input breeding is based on a breeding cycle that ceases early in the selection process, uses information from both wild populations and common gardens, and relies heavily on molecular markers to delineate meaningful geographic zones, track candidate genes and maintain a high effective population size (Lindgren & Wei 2006, El-Kassaby & Lstiburek 2009). Such breeding strategies represent flexible and viable alternatives to complicated and costly (high-input) breeding programs that are designed for high yield situations (Wang et al. 2010).

In conclusion, policy-makers should be aware that breeding programs need to adapt quickly to the challenges of the 21st century while existing ex situ collections and past selection efforts should be rescued and conserved. Whether based on a high or a low input strategy, breeding programs should include the assessment of phenotypic traits that are likely to be important in conferring genetic adaptation to climate change (which may well be found outside usually investigated resources and will require well-organized international collaboration). Low-input breeding strategies represent an opportunity to do so for species that are traditionally under-represented in
breeding programs because of their low market value. This may be useful, as in the future such species (e.g. Mediterranean trees) may become increasingly important under climate change.

686

687

## Challenge 7: What are the socio-economic benefits of genetic conservation and breeding under global change scenarios?

690

In addition to changing perceptions of the importance of genetic resources for better coping with increased disturbances, the views of society are also shifting regarding the role of genetic resources in meeting the demands for forest goods and services.

The two main current drivers of this shifting perception are climate change and expected future demands by end-users.

696

Future demands by European end-users are anticipated to focus on an increase in renewable energy and materials, both to mitigate climate change and to promote trade and economic growth (Farizo et al. 2014, Soliño et al. 2012). This will be accompanied by a need to produce more product per unit of land area as the demands for urbanization, recreation, nature conservation and food production should reduce the amount of land that is available to forestry. There will be pressure to improve the quality of timber (e.g. by increasing stiffness in solid wood or by lowering the lignin content). According to Vanhanen et al. (2007), the maturing forest product markets in Europe will place pressure on the forest sector to restructure through development and adoption of technical and social innovations. At the same time, the demand for recreation and nature conservation is also increasing, and the desirability of a uniform product (which can be more easily achieved via clonal forestry) for the bio-economy has to be balanced against the need to maintain high levels of biodiversity.

710

Forest trees are characterized by a low level of domestication in comparison to other organisms, and consequently, the high levels of intra-specific genetic variation (among and within populations) that most tree species naturally contain has largely been maintained. This variation is essential for the long term adaptability of the tree species themselves as well as the associated species that depend on them. It is also crucial because it serves as the reservoir for breeding resources in the future. However, overall social perceptions of the benefits of biodiversity conservation to forest ecosystem services are usually based on species richness and the importance of intra-specific genetic diversity is generally not accorded the consideration it deserves.

This is possibly because genetic diversity is a component of biodiversity that is not easily visible or accessible to most people. Also, the perceived importance of biodiversity varies with the socio-economic environment (Dominguez-Terrero and Soliño, 2011). Intra-specific genetic diversity has an intrinsic economic value which, despite its importance, is unfortunately poorly recognized in economic valuation scenarios (Thorsen & Kjaer 2007). Highly-diverse forests are also better prepared to response to societal demands for new specialized forest products and increased productivity under climate change.

728

In conclusion, increasing the societal perception of the value of genetic diversity in managed forest ecosystems should be a priority. New methodological developments in forest and landscape genetics could help to assess the socio-economic importance of conservation or breeding activities. Raising awareness in forest managers, policy

730

731

732
makers and conservationists of the essential role of genetic diversity on biodiversity dynamics and adaptability of forests to future conditions is urgently needed. Improvements in knowledge transfer beyond academia are required.

736

737

## Conclusion

738

Climate change will impact natural forests forcing trees, their keystone species, to move, adapt or disappear locally. Climate change is also likely to alter the health of forest trees worldwide. The speed and extent to which these alterations are likely to occur remain difficult to predict accurately. Ultimately, the decision to adopt one management strategy over another is in the hands of managers and policy makers who should be able to make “no regret” decisions. We have shown that genetic diversity will play a vital role in determining the resilience and adaptability of forest tree populations to climate change whatever the management objectives chosen (production, protection or recreation). Genetic knowledge will help managers and policy makers make informed, science-based decisions for prioritizing strategies and it is essential that practitioners keep abreast of scientific advances in this field. Of course, much uncertainty remains and we expect that results from common gardens and the rapid advances that are being made in genomics will soon contribute much needed information for critical issues such as assisted migration and assisted gene flow. This developing understanding will also help tree breeders to apply multi-trait selection approaches to produce the most appropriate phenotypes needed under changed climate conditions. Managing forests and other natural landscapes to conserve and sustainably use genetic diversity is a sensible, practical and risk-reducing strategy under uncertain environmental conditions, that can be applied in production, protection and recreation forests alike.

760

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