Plant conservation genetics in a changing world

Review

Special Issue: Plant science research in botanic gardens

Plant conservation genetics in a changing world Andrea T. Kramer1 and Kayri Havens2 1 2

Botanic Gardens Conservation International USA, Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, IL 60022, USA Division of Plant Science and Conservation, Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, IL 60022, USA

Plant conservation genetics provides tools to guide conservation and restoration efforts, measure and monitor success, and ultimately minimize extinction risk by conserving species as dynamic entities capable of evolving in the face of changing conditions. We consider the application of these tools to rare and common species alike, as ongoing threats that increasingly limit their resilience, evolutionary potential and survival. Whereas neutral marker studies have contributed much to conservation genetics, we argue for a renewed focus on quantitative genetic studies to determine how, or if, species will adapt to changing conditions. Because restoration plays an increasingly vital role in conservation, we discuss additional genetic considerations and research questions that must be actively studied now to effectively inform future actions. Genetic aspects of plant conservation Conserving habitat and ecological processes is unarguably the best way to preserve plant species, communities and ecosystems, as the losses of habitat and ecological processes have immediate impacts on species survival. However, because so much habitat has been and continues to be lost, conservation-as-usual is no longer enough to ensure the survival of the world’s plant species. This is certainly true for currently-rare species, but regrettably is also increasingly true for common species. Rapidly increasing habitat fragmentation, degradation, globalization of pests and diseases, and climate change mean that conservation now requires coordinated action on local, regional, national and global scales. And it means that whole-habitat restoration as well as single-species reintroduction and population augmentation will be increasingly important conservation tools. Here, we explore how the growing use of these tools introduces myriad opportunities for genetic factors to affect plant conservation efforts, and consider what can be done to minimize or avoid negative effects. Since its inception, conservation genetics has focused largely on the genetic consequences of small population size that may limit survival of populations and species [1]. Several excellent reviews and textbooks on the genetic aspects of plant conservation have been published over the past two decades [2–8]. We do not attempt to rehash these reviews here. Instead, we consider implicaCorresponding author: Havens, K. ([email protected]).

tions and applications of the latest research, and broaden the discussion to consider ways the genetic aspects of plant conservation must, of necessity, expand to reflect conservation in a rapidly changing world [9] where restoration is a key strategy for species conservation. We discuss the importance of a renewed focus on adaptive genetic diversity (see glossary) and why genetic erosion poses an increasing threat to the long-term survival of rare and common species alike. We argue that artificial (human-mediated) gene flow deserves increasing attention, and end with a discussion of research priorities and applications.

Glossary Adaptive genetic diversity: genetic variation that is under natural selection. Additive genetic variation: a measure of how well quantitative traits are passed from parents to offspring; determines evolutionary potential of a population. Artificial gene flow: human-mediated gene flow, due to deliberate movement of seeds, pollen or plants. Assisted migration (assisted colonization, managed relocation): deliberate movement of individuals to locations outside the native range of the species. We restrict the definition to the movement that facilitates or mimics natural range expansion, as a direct management response to climate change. Co-adapted gene complexes: groups of genes at multiple loci that confer higher fitness when they occur together than apart. Genetic drift: changes in the genetic composition of a population due to chance. Genetic swamping: replacement of local genetic variation by introduced/nonlocal genetic variation due to intra or interspecific hybridization. Hybrid vigor (heterosis): superior performance of hybrid genotypes Quantitative genetic variation: genetic variation in a quantitative (continuous) trait, such as size or reproductive rate. Gene flow: the movement of alleles of genes between populations (e.g. effective seed or pollen dispersal). Genetic erosion: loss of genetic diversity within a population or species. Inbreeding: mating of individuals related by descent. Inbreeding coefficient: a measure of the extent of inbreeding; the probability that two alleles at a locus are identical by descent. Inbreeding depression: a reduction in fitness due to inbreeding. Local adaptation: genetic divergence between populations in response to natural selection for location-specific biotic or abiotic factors (e.g. pathogens or climate). Mating system: the degree to which individuals are self-fertilizing versus outcrossing. Neutral genetic variation: genetic variation that is not under natural selection. Outbreeding depression: a reduction in progeny fitness due to intraspecific mating between genetically dissimilar individuals. Phenotypic plasticity: the ability of an individual to change its phenotype in response to changes in the environment. Seed transfer zones: delineated regions within which restoration efforts can move plant material (e.g. seeds) with the fewest negative impacts on fitness due to maladaptation. Sympatry (incl. artificial sympatry): when populations overlap, partly or fully, geographically. Artificial sympatry can occur when plants are moved to new locations, particularly those outside their native range.

1360-1385/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2009.08.005 Available online 10 September 2009

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Review A renewed focus on adaptive genetic diversity Plants cope with threats in three ways: phenotypic plasticity [10], migration to more favourable conditions, or adaptation to new conditions over multiple generations [11]. If any or all of these three strategies fail(s), extinction is the consequence. The best way to gauge the ability of a population to respond effectively to threats is by understanding its underlying quantitative genetic variation, that is, the diversity upon which selection acts. For over two centuries now, researchers have sought to understand how and when quantitative variation and selection interact to drive local adaptation [12]. Some of the most compelling and complete research on this topic is over 60 years old [13,14], and it remains entirely relevant in discussing the genetic aspects of plant conservation that we encounter today [15]. Unfortunately, continued progress has not been as strong as it needs to be to understand and manage species’ responses to new and unprecedented threats. We do know from the past six decades of quantitative genetics research that plant populations are often adapted to local conditions [16] including soil type [17], winter temperature and length [18], water availability and flood tolerance [19–21] local herbivory and pathogen presence [22], and countless other factors. Of course, populations locally adapted to specific biotic or abiotic conditions may experience potentially severe fitness consequences, including poor competitive ability and reduced growth and reproduction [23–26], if transplanted away from their home sites. Current and projected rapid climatic changes mean innumerable populations may find themselves trapped at sites to which they are no longer adapted. Habitat destruction and fragmentation will make natural migration difficult or impossible for many plants in this situation, and if populations do not possess sufficient phenotypic plasticity or quantitative genetic variation, they will be unable to respond to the changes, leaving no alternative to extinction. Unfortunately, by recent accounts, the study of quantitative genetic variation is lagging behind the study of molecular genetic variation, particularly with regard to research aimed at informing plant conservation and restoration actions (Table 1). There has been a steady increase in molecular genetic studies over the past three decades, which has helped advance conservation in many ways [5]. Studies incorporating neutral molecular genetic markers like allozymes and microsatellite markers, combined with increasingly sophisticated analytical approaches like Bayesian analysis and network theory, are helping resolve taxonomic questions, detect hybridization, and quantify patterns of genetic diversity, inbreeding and gene flow within and among populations for numerous species [27– 29]. Although these studies provide valuable information for conservation, when used alone they are inadequate for conservation success in a changing world. This is because neutral molecular variation rarely predicts quantitative genetic variation [30–33], a critical determinant of a population’s evolutionary potential (particularly additive genetic variation). This point has been made in conservation genetics literature for over a decade [34], yet as evidenced by Table 1, neutral molecular studies continue to predominate the realm of published research. 600

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When conservation and restoration priorities are based only upon findings from neutral molecular genetic studies, there is great risk that practices they inform will be unsuccessful at creating robust populations capable of adapting to change. This is both ecologically and economically inefficient. For example, populations with little to no measurable difference in neutral alleles may in fact contain important phenotypic plasticity [35] or genetic diversity in ecologically important traits like enhanced dispersal ability [36]. Failure to recognize these important genetic differences could lead to ineffective conservation actions, such as making a decision not to protect populations lacking in neutral genetic diversity that may in fact contain invaluable quantitative genetic variation. For plant populations in a changing world, the difference between long-term adaptation and survival or extinction will be determined by whether they maintain adequate quantitative, not neutral, genetic variation. One of the arguments against quantitative genetics studies is that they take significantly more time and resources than molecular studies. Although often true, particularly for long-lived species, some of the best and most relevant quantitative genetics studies have been carried out by forest geneticists on economically-important timber species [37,38]. Recent studies have proven that, particularly for shorter-lived forbs and grasses, meaningful quantitative genetics and reciprocal transplant studies can be carried out in a short time-frame [26]. If we hope to have the information we need to conserve common and rare species alike, the time to begin these studies is now. When studied in tandem, knowledge about quantitative and neutral genetic variation can provide a powerful picture of a species’ genetic history that can be used to guide future conservation and restoration efforts (Table 1). A recent example comes from Ranunculus reptans (creeping spearwort), where a combination of techniques indicated that genetic drift and natural selection had acted together to exacerbate genetic isolation and adaptive divergence in recently fragmented populations [39]. This information can help guide conservation and restoration practice, from seed collection to reintroduction (Figure 1). Given a growing awareness of the critically important value of quantitative genetic studies and the advent of ecological genomics, at least for a few model plant organisms like Arabidopsis thaliana (rockcress) [40] and Mimulus (monkeyflower) [41], we hope to see more studies of adaptive genetic variation in the coming decade. Population decline and genetic erosion Genetic erosion can limit short term resilience, evolutionary potential for adaptation, and long-term survival of any plant species in the face of rapid environmental change [42,43], thus increasing extinction risk. Concomitant with rapid population decline and genetic erosion, plants residing in small populations may experience increased inbreeding (both selfing and bi-parental), increased homozygosity, and ultimately the negative fitness effects of exposed recessive deleterious mutations, that is, inbreeding depression. Most research on the genetics of small populations has focused on conserving rare species. Today, however, common species are experiencing population

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Table 1. Comparison of techniques to quantify important population genetic parameters, and number of publications for each parameter in conservation journalsa (plants and animals) Population genetic parameter Inbreeding

How knowledge gained is applied for conservation To prioritize and inform conservation activities aimed at avoiding inbreeding and especially inbreeding depression and monitor change over time

Neutral genetic studies (e.g. microsatellites, mitochondrial DNA) Identifies: selfing and bi-parental inbreeding in individuals Con: cannot determine if inbreeding is causing inbreeding depression Number Studies: Plant (23) Animal (51)

Quantitative genetic studies (e.g. common garden, reciprocal transplant, quantitative trait loci) Identifies: the true fitness costs of inbreeding (e.g. inbreeding depression) Con: more time-consuming, labor intensive, often requires destructive sampling Number Studies: Plant (4) Animal (5)

Neutral and quantitative genetic studies together No additional information gained

Withinpopulation genetic diversity

To prioritize and inform conservation activities aimed at maximizing genetic diversity, minimizing erosion and to monitor change over time

Identifies: population-level diversity in neutral alleles Con: cannot identify adaptive genetic diversity Number Studies: Plant (25) Animal (66)

Identifies: potentially adaptive genetic diversity in phenotypes (or quantitative trait loci) Con: more time-consuming, labor intensive, often requires destructive sampling Number Studies: Plant (3) Animal (7)

No additional information gained

Amongpopulation genetic divergence

To prioritize conservation activities aimed at ensuring seed source matches reintroduction or restoration site, such as seed transfer zones and monitor change over time

Identifies: population differentiation in neutral DNA, indicating presence and strength of gene flow, genetic drift Con: cannot identify differentiation in adaptive genetic diversity Number Studies: Plant (23) Animal (59)

Identifies: population differentiation in potentially adaptive genetic diversity Con: without information about gene flow, difficult to identify whether divergence is adaptive or random. Number Studies: Plant (2) Animal (9)

Identifies: adaptive versus random population genetic divergence for selected traits Con: more time-consuming, labor intensive, often requires destructive sampling Number Studies: Plant (4) Animal (8)

Local adaptation

To prioritize conservation activities aimed at ensuring seed source matches reintroduction or restoration site, such as seed transfer zones and monitor change over time

Use of neutral genetic studies cannot identify local adaptation

Identifies: population differentiation in potentially adaptive genetic diversity Con: more time-consuming, labor intensive, requires destructive sampling Number Studies: Plant (2) Animal (2)

No additional information gained

Gene flow

To prioritize conservation activities by understanding species’ life history characteristics and monitor change over time (e.g. increases or decreases in population connectivity with fragmentation, etc.)

Identifies: historical and current movement and mixing of populations; use of multiple markers can distinguish movement via seed and pollen. Con: presence of gene flow does not preclude divergence in adaptive genetic diversity Number Studies: Plant (13) Animal (50)

Use of quantitative genetic studies cannot identify gene flow

No additional information gained

a Results of a search on ‘‘population genetics’’ for all articles published in Conservation Genetics, Conservation Biology, and Biological Conservation in 2008, manually searched and grouped by category and organism (plant vs. animal).

declines due to habitat destruction, fragmentation, climate change and restoration efforts that fail to establish large, genetically diverse and genetically appropriate populations. Thus the same genetic concerns are valid and applicable to both rare and currently common species, and there is an urgent need to understand how rapid declines in population size impact genetics and negatively affect population persistence. Although there has been considerable debate over the role of genetics in species extinction, there is significant support for the hypothesis that extinction does not occur before genetic factors come into play [44]. For example, a meta-analysis of genetic studies for 95 rare plant species

and 152 taxonomically related common species found significantly lower genetic variation in the rare species [45]. Looking beyond the results of genetic studies that incorporate only neutral molecular markers, two additional meta-analyses identified significant positive correlations between fitness and genetic erosion in selfincompatible plant species, and remarkably significant correlations between population size, genetic erosion and fitness [46,47]. It is clearly counterproductive to disregard genetic factors in conservation activities focused on establishing or maintaining populations capable of evolving and persisting into the future; we outline specific concerns below. 601

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Figure 1. Illustration of six stages at which genetic information has been used and is increasingly needed to guide large-scale native plant restoration efforts. This includes: 1. Seed collection: it is important to capture intra and interpopulation quantitative genetic variation and phenotypic plasticity (including small and peripheral populations, as long as they do not exhibit inbreeding depression). Genetic sampling guidelines have been developed for rare species [115], and molecular [116,117] and quantitative genetic studies [118,119] have been used to guide and gauge success of work at this stage in many species. 2. Research: collection of multiple seed sources provides a valuable opportunity to incorporate molecular and quantitative genetic studies on collected seeds to learn more about the species’ biology and underlying adaptive genetic diversity in order to delineate seed transfer zones. Examples come from forest genetics {106] and others [120,121]. Because little is known about most species, this stage is often critical to guiding effective species restoration, and there is room for a significant expansion of genetics work in this realm. 3 and 4. Seed bulking via field establishment and seed production: native plant community restoration is increasingly performed on a large scale, requiring ample seed supplies. During grow-out it is important to ensure maximum quantitative genetic variation is maintained, yet limit the potential for inappropriate inbreeding as well as inappropriate intrapopulation gene flow or interspecific hybridization. Genetics research has helped identify when and where these genetic factors are a concern [122–124]. 5. Seed storage: It is important to clean, dry and store seeds to ensure the storage and equal survival of genetic diversity [125]. 6. Restoration: all restoration practices will benefit from incorporating genetic considerations, including choosing the best seed source (guided by research in stage 2), species mix, and restoration technique to maximize appropriate quantitative genetic variation and population size.

One of the most straightforward ways genetic erosion reduces population viability is demonstrated in self-incompatible species, where a loss of diversity in self-incompatibility alleles can lead to pollen-limitation and reduced seed set, ultimately increasing extinction risk. An extreme example was provided by Hymenoxys acaulis var. glabra (lakeside daisy) [48], where the one remaining population in Illinois became effectively extinct because it contained plants of just one mating type. Plants were only capable of seed production when crossed with pollen from the nearest population, over 450 km away. However, more subtle extinction risk in self-incompatible species has been found in fragmented or shrinking populations, with declines in seed production attributed to lack of genetically appropriate pollen [49]. This can be of particular concern for species often used in restoration efforts that were once widespread and common but that now occur in fragmented populations unconnected by gene flow. For instance, in Echinacea angustifolia (narrow-leaved coneflower) genetically-based pollen limitation increased while seed set and fecundity decreased with isolation of individual plants, and to a lesser extent with population size [50]. A growing number of experimental studies have helped demonstrate other more cryptic effects of genetic erosion 602

and inbreeding on fitness (e.g. inbreeding depression) and long-term population viability. A striking example comes from Clarkia pulchella (pinkfairies) [51], where experimental populations with slightly elevated inbreeding coefficients (F = 4% versus F = 8–9%) experienced significantly greater extinction rates over three generations in a natural environment (25% versus 69%, respectively). Similar correlations between genetic erosion and measures of population fitness and viability were found in demographic studies of Silene regia (royal catchfly) [52], Primula vulgaris (English primrose) [53], and Zostera marina (eelgrass) [54]. In addition, population viability analyses (e.g. demographic modelling) for Astragalus cremnophylax (sentry milkvetch) and Calochortus tiburonensis (Tiburon mariposa lily) found that modest levels of inbreeding depression led to faster median times to extinction for each species (up to 21% and 84%, respectively) [55]. A follow-up study suggested that the negative impacts of inbreeding depression on median time to extinction identified in these models may have been up to four times greater than reported [56]. Clearly, population viability analyses should strive to incorporate reasonable measures of inbreeding depression effects. Unfortunately, getting accurate estimates of lifetime inbreeding depression effects, particularly in plants, is still an area of significant

Review research opportunity. This is because the expression of inbreeding depression varies not only by species, but also by trait, genotype, population, and environment [4,57,58]. Finally, genetic erosion limits the ability of evolution via natural selection to provide species with the capacity to adapt to a changing environment [43,59–63]. Populations with sufficient additive genetic variation for ecologically important traits will be best equipped to adapt to today’s rapidly changing environment, and this must be increasingly incorporated in conservation and restoration activities. Although there are certainly constraints to evolution of a trait or suite of traits even if ample additive genetic variation is present [64], there are numerous documented cases of rapid trait evolution that provide hope for adaptation as an option for long-term survival. One example comes from the annual Brassica rapa (field mustard), where natural selection for drought escape via early flowering occurred over the course of just a few generations [65]. Management and conservation practices must ensure that populations of rare as well as common plant species do not lose important additive genetic variation, and restoration practices will be most effective if they are geared toward establishing populations with adequate and appropriate genetic variation. Effects of artificial gene flow Human activities, such as horticulture and agriculture, revegetation projects, ex situ conservation programs, and habitat alterations are increasingly bringing previously isolated populations and species into contact, as are range expansion or change of both native and invasive species due to climate change. This artificial gene flow can contribute to species decline or loss via outbreeding depression and genetic swamping. Outbreeding depression is a decline in offspring fitness when parents are genetically dissimilar [66]. Although it has received much less research and management attention than inbreeding depression [67], outbreeding depression has been documented in a growing number of plant [68–71] and animal [72,73] species, and has significant potential for large and long-lasting generational effects [74] on population viability. Indeed, a recent review [67] suggests that the negative effects of outbreeding depression on population persistence may be on par with the risks from inbreeding depression. Until the last decade, outbreeding depression had rarely been empirically detected because it was rarely studied, and because its negative fitness effects are difficult to measure and often take more than one generation to manifest [75]. Indeed, the first generation of a cross between genetically dissimilar parents may produce offspring with hybrid vigor (particularly if the parents are inbred) as deleterious recessive alleles are masked [76]. Yet following generations of this same cross may experience significant outbreeding depression as co-adapted gene complexes are recombined through at least the second [77] or even sixth generation [71]. We do not yet know enough to predict which species and crossing scenarios will produce offspring most at risk for outbreeding depression, but it is a growing concern as restoration practices often entail moving, and in some cases mixing, disparate populations.

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Another potential effect of artificial gene flow produced through human activities is genetic swamping via hybridization. Hybridization, or crossing between species, can be considered an extreme case of outbreeding, with potentially equally negative impacts on the long-term survival of a species. Hybridization is a concern because formerly isolated species are increasingly becoming sympatric and the more common congener can genetically swamp the rarer species, leading to the loss of valuable local ecotypes and, in extreme cases, extinction [78–82]. Important ecological and species considerations Community and ecosystem genetics bridges the fields of population genetics, evolutionary biology, and community ecology [83,84]. Studies under this umbrella are beginning to identify how single-species genetic diversity can impact not only the persistence and resilience of individual plant populations and species [85], but also key ecological processes and patterns in the systems they inhabit [86,87]. For example, experimental grassland plant communities in Europe with higher intraspecific genetic diversity maintained greater species diversity over time [88]. This is because interactions between different genotypes of different plant species resulted in a variety of competitive outcomes, allowing more plant species to persist in the same space [89]. Studies on Solidago altissima (tall goldenrod) reveal how genetic erosion in dominant plant species can lead to lower aboveground net primary productivity, increased susceptibility to invasion by other plant species, and altered diversity and structure of other trophic levels (e.g. arthropod species) [90,91]. Similar effects of genetic erosion, as well as inter- and intra-species introgression, on community and ecosystem structure and function have been documented in poplar trees (Populus spp.) [92–94]. Clearly, we are only beginning to understand the enormity of what is lost when intact habitat is destroyed, and its conservation must be an urgent priority. Yet given all that has been lost already, ecological restoration is also a pressing need. Restoration efforts that disregard the importance of establishing and maintaining genetic as well as species diversity do so at their own peril. Ecological context on a species and landscape basis is also probably important in determining conservation success. Much of today’s conservation theory has developed from empirical work on species in the United States and Europe in relatively young, post-glacial temperate species assemblages. Patterns of genetic diversity and the consequent applications for conservation may be much different in ancient species assemblages such as those found in the Cape Floristic Region of South Africa or in Southwestern Australia. One might expect a greater degree of local adaptation and partitioning of genetic diversity between populations in the floras of ancient, climatically-stable landscapes [95] than in their younger counterparts, but this remains to be tested on a broad scale. Finally, it is important to understand how speciesspecific characteristics can contribute to or hinder species survival in a changing world. For example, higher levels of ploidy moderate the expression of inbreeding depression by masking deleterious alleles, but can also elevate 603

Review outbreeding depression risk due to the presence of coadapted gene complexes [70,96]. We also know that life history characteristics, such as breeding system, mating system and mode of dispersal, influence the amount and pattern of genetic diversity in populations and species. Indeed, numerous generalizations are now possible with respect to neutral genetic variation [97,98], and this is helpful in considering how different species will respond to threats. For example, species with long-distance pollination or dispersal abilities may experience few measurable genetic impacts of habitat fragmentation, because they can maintain larger effective population sizes via gene flow among multiple fragments [99]. Unfortunately, we know much less about adaptive genetic variation [100]. Significant growth in this area is needed if we hope to conserve species effectively in light of current and future threats. Applications to restoration Genetic considerations and concerns of small populations have important applications for restoration practices, and should be kept in mind at all stages of native plant community restoration efforts [101]. Figure 1 depicts the cycle of activities required for large-scale native plant restoration, and illustrates the many stages at which genetic information has been used to guide restoration efforts and evaluate effectiveness. It also highlights areas that require additional genetics research and consideration to help guide appropriate application. One area in particular that needs significant focus, particularly in light of rapidly changing climates, is the development and application of seed transfer zones for species of restoration value. Dynamic seed transfer zones Given that plant populations are often adapted to local site conditions, identifying genetically appropriate seed sources is a crucial consideration in any restoration. Failure to do so may lead to either immediate failure (e.g. seed source conditions do not match site conditions and all seeds fail to germinate or seedlings die), or longer-term collapse if the population does not possess phenotypes that allow it to survive and adapt to current and changing conditions over time. An example comes from the U.S. Forest Service, where Douglas fir (Pseudotsuga menziesii) trees from numerous sources were planted in Oregon in 1915. Trees performed well until 1955, when a prolonged cold spell seriously damaged or killed trees from off-site sources while causing only minor damage to trees from local sources [102,103]. Losses like this led the forestry community to research adaptive genetic diversity in order to delineate ecologically and economically appropriate transfer zones for large-scale reforestation of commercial tree species, beginning in the 1960s and continuing today. Similar research for native herbaceous species has lagged significantly behind research on timber species, and in general much less is known about their biology and underlying adaptive genetic diversity. As a result, the appropriate movement of seeds for restoration is often either not considered, or is very conservatively circumscribed by distance from a source site, resting on the 604

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assumption that biotic and abiotic factors are likely to be similar between populations in close proximity. Neither of these approaches is likely to result in the establishment of populations that are genetically equipped to thrive into the future. Fortunately, research-based seed transfer zones similar to those used for trees are beginning to be defined for species commonly used in restoration [103,104]. We hope to see more research focused on understanding adaptive genetic diversity within and among populations [105,106] to help guide the development of seed transfer zones. Finally, climate change scenarios mean that the static notion of seed transfer zones must become more dynamic, as many plant populations may no longer be optimally adapted to local conditions. The forest genetics community continues to lead research efforts in this area, and has been addressing the implications of climate change for seed transfer zones for nearly two decades [37,107–109] This research has improved the matching of source material to restoration and revegetation sites, leading to the development of dynamic or ‘floating’ seed transfer zones [110] that incorporate both geography and shifting climates. With additional research and consideration, we will be increasingly able to avoid creating populations and communities that suffer from the negative effects of genetic erosion, inbreeding depression, outbreeding depression, or maladaptation. This will be critical to the long-term success of all future restoration efforts in our changing world. Conclusions and genetic research priorities for the future Much of the conservation genetics research and many resultant management prescriptions to date have assumed a stable environment. It is increasingly clear that our environment, particularly our climate, is anything but stable. Some of the most pressing research questions for the near future involve understanding the response of plant populations and communities to climate change and their genetic consequences. Common is the new rare The continued survival of many of the world’s plant species, including those not currently considered vulnerable, is increasingly threatened by a rapidly changing climate [111]. Species that have thus far been able to cope with human-imposed changes such as habitat loss, habitat fragmentation, and invasive species, might not be able to cope with climate change. The likely ‘‘losers’’ in a rapidly changing climate are species with long generation times, limited ecological amplitudes due to plasticity, or low levels of additive genetic variation. As restoration is increasingly used as a conservation option, species will be exposed to the genetic aspects and impacts of manipulations or interventions by humans through the practice of ecological restoration and possible assisted migration. These actions will increasingly come into play in determining their survival [60]. Research priorities related to restoration and assisted migration go beyond developing the dynamic seed transfer zones discussed above. For instance, do some life history traits make a species more or less likely to adapt or migrate

Review appropriately on their own? Should seed production be limited to the first generation produced by wild collected plants to preserve the genetic composition of the source population, or should we establish seed beds at the latitudes to which we are likely to be moving a species (or population) to allow a few generations to adapt to the local environment before using them for restoration? Changing relationships Phenological changes induced by climate change may affect plants and animals differently leading to shifting pollinator [112] and herbivore [113] communities. New diseases brought by novel or phenologically-shifted vectors may affect evolution of resistance and population dynamics. Climate change can increase likelihood of hybridization by driving range shifts of previously spatially isolated species or changing phenologies of temporally isolated species. Understanding the genetic consequences of these new plant-animal and plant-plant interactions is an important area of research. One size does not fit all Species assemblages, and the ecological context in which species reside, are highly variable. Management prescriptions and rules of thumb based on research in young, temperate landscapes may not be appropriate for species from ancient landscapes, the tropics, or islands. It is crucial that we begin to understand the genetic differences between species that reflect their different evolutionary and ecological histories. A meta-analysis comparing patterns of genetic variation between species in young landscapes, such as the tallgrass prairie, and ancient landscapes, such as the southwest Australia floristic region, could illuminate how genetic management may need to differ between these floras. For instance, are species in old, stable landscapes more resistant to habitat fragmentation and/or more threatened by climate change as a result of a long history of evolution in relatively small, isolated populations [114]? In this era of environmental uncertainty, maintaining and restoring resilient plant populations have never been more important. Undoubtedly conservation genetics will continue to provide information to improve the understanding and appropriate management of plant populations, but this avenue of research will be most fruitful if we consider the interplay of genetics with ecology, demography and evolutionary history. A unified approach will be necessary to maximize the chances of plant population persistence in the face of a volatile climate and myriad other anthropogenic threats. Acknowledgements The authors’ research on seed transfer zones and genetic considerations in ecological restoration was supported by the U.S. Bureau of Land Management, the Center for Plant Conservation, and an EPA STAR Fellowship to ATK. We thank Peggy Olwell for providing Figure 1, and Jeremie Fant, Pati Vitt, Stuart Wagenius and three anonymous reviewers for their thoughtful comments on an earlier draft of this paper.

References 1 Frankel, O.H. (1974) Genetic conservation: our evolutionary responsibility. Genetics 78, 53–65

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