Ann. N.Y. Acad. Sci. ISSN 0077-8923
A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S Issue: The Year in Ecology and Conservation Biology
Habitat fragmentation, climate change, and inbreeding in plants Roosa Leimu,1 Philippine Vergeer,2 Francesco Angeloni,2 and N. Joop Ouborg2 1
Department of Plant Sciences, University of Oxford, Oxford, UK. 2 Section Molecular Ecology and Ecological Genomics, IWWR, Radboud University, Nijmegen, the Netherlands Address for correspondence: Roosa Leimu, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, UK.
[email protected]
Habitat fragmentation and climate change are recognized as major threats to biodiversity. The major challenge for present day plant populations is how to adapt and cope with altered abiotic and biotic environments caused by climate change, when at the same time adaptive and evolutionary potential is decreased as habitat fragmentation reduces genetic variation and increases inbreeding. Although the ecological and evolutionary effects of fragmentation and climate change have been investigated separately, their combined effects remained largely unexplored. In this review, we will discuss the individual and joint effects of habitat fragmentation and climate change on plants and how the abilities and ways in which plants can respond and cope with climate change may be compromised due to habitat fragmentation. Keywords: adaptation; climate change; genetic variation; habitat fragmentation; inbreeding; plant fitness
Introduction Rapid environmental changes, caused by human activities, influence both ecological processes and evolutionary trajectories, which can ultimately result in extinctions of populations and species, and loss of global biodiversity.1–3 Habitat fragmentation and climate change are recognized as major threats to biodiversity.3 The number of published studies reporting their separate impacts on plant population viability and extinction risk has increased almost exponentially during the last few years.4–14 Only few recent reviews have outlined the joint impact of habitat fragmentation and climate change on extinction risk.15,16 Fragmentation is considered to reduce species’ abilities to track the rapid climate change mainly due to two reasons. First, dispersal or movement (“range shift”) to habitats with optimal climate conditions is compromised in a fragmented landscape.17–20 Second, reduced genetic variation in fragmented populations is predicted to reduce the adaptive potential of species under climate change.21 Empirical and/or experimental studies supporting these views are still scarce.22 Moreover, the im-
pact of increased inbreeding, another major genetic consequence of fragmentation, on the viability and extinction risk under climate change, and on the ability to cope with climate change, is poorly understood. Hence, understanding the joint consequences of habitat fragmentation and climate change, and especially the mechanisms by which they reduce biodiversity, is a major challenge for ecologists and evolutionary biologists today. These challenges are also recognized as priority by several international bodies.23 In one of its working group reports, IPCC lists “The impacts of interactions between climate change and changes in human use and management of ecosystems, as well as other drivers of global environmental change” as one of the key uncertainties and research priorities of today.23 In this article, we will review the major consequences of habitat fragmentation and climate change and their interactive effects on plant species and their populations. We will discuss the potential mechanisms by which the genetic consequences of habitat fragmentation compromise the ability of plant species to cope with climate change. We will
doi: 10.1111/j.1749-6632.2010.05450.x 84
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focus on the impact of inbreeding on adaptation and on the interactive effects of inbreeding and climate change-driven changes in abiotic and biotic environments. We aim to reveal the gaps of our knowledge and provide guidelines for future research and discuss new avenues. Consequences of habitat fragmentation for plants Habitat fragmentation refers to the loss of suitable habitat of a species and the concurrent separation of individuals into a number of habitat patches, which are isolated from each other by unsuitable habitat types. Due to fragmentation, numerous populations of many plant species have decreased in size and have become more isolated. As a result, they face an increased risk of extinction due to environmental and demographic stochasticity.24–26 The probability of stochastic extinctions is determined by environmental, demographic, and genetic processes, which are all strongly related to habitat fragmentation and population size. Genetic consequences The main predicted genetic consequences of habitat fragmentation are reduced genetic variation and increased inbreeding within populations, and increased genetic differentiation among populations. Reduced population sizes may result in reduced genetic variation and increased levels of inbreeding and, eventually, lower population performance.27,28 These effects are caused by a series of closely connected processes. In small populations the influence of genetic drift increases, leading to increased loss and/or random fixation of alleles.29 This leads to increased homozygosity, which may negatively affect individual fitness.30 Plant performance may also be compromised by accumulation of deleterious mutations in small populations, due to less effective selection.31 Finally, small populations face greater risk of inbreeding simply because individuals are more likely to be related (“bi-parental inbreeding”) or because of higher rates of selfing due, for example, to reproductive assurance.32 Reduced genetic diversity, mutation accumulation, and increased inbreeding may result in reduced fitness in small plant populations.27,28,30 In the long term, these processes may decrease the evolutionary po-
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tential of species and their ability to adapt and cope with changing environments such as climate change.27,33,34 Habitat fragmentation increases isolation between populations, which will lead to increased genetic differentiation between them. Because isolation restricts gene flow, local populations may become independent evolutionary units, with random genetic processes drifting populations apart. There is ample evidence for this effect, often quantified by the population genetic parameter FST .35–38 Evidence for such genetic differentiation has been found particularly in marginal plant populations.39,40 Increased genetic differentiation among populations is important for conservation. It raises the concern of outbreeding depression, that is, reduced fitness or maladaptation of progeny of crosses between individuals of two populations.41–43 In a conservation context, this is important when plants are transplanted between populations or the gene pool mixed for restoration purposes. Moreover, increased genetic differentiation of populations may matter if formerly isolated populations come into contact with each other due to climate change-mediated shifts. Ecological consequences Besides genetic effects, habitat fragmentation will also have clear demographic and ecological effects. Small populations will have higher probabilities of extinction, just because of the lower number of individuals. The increased isolation in a fragmented landscape will also prevent demographic rescue by immigration from individuals out of other populations. The ecological consequences are many. Habitat fragmentation can lead to the disruption of biotic interactions such as plant–pollinator mutualisms.7,44,45 Small fragmented plant populations may be less attractive to pollinators and thus more strongly pollinator or pollen limited, which results in reduced reproductive success.46–48 Habitat fragmentation may also alter the foraging behavior of pollinators and limit their movements.49–51 Furthermore, fragmentation may disrupt interactions between plants and agents of seed dispersal. This may influence the population dynamics and fitness of populations of plants that rely on animals in their seed dispersal.51 Finally, habitat
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fragmentation may perturb antagonistic interactions, such as those between plants and herbivores, seed predators, or pathogens.52–54 Habitat fragmentation also causes changes in the physical environment. Small habitat fragments will have a different ratio of core to margin, which will change the biotic and abiotic quality of such fragments. As a result, fluxes of light, wind, water, and nutrients across the landscape are significantly altered. This, in turn, can have important consequences on the remnant individuals.55 Therefore, the differences in habitat quality between the different fragments in which a population is subdivided56,57 might have very different influences on within-fragment dynamics, including both positive and negative effects on life history processes and population viability. Effects of inbreeding on plant performance Inbreeding can have considerable demographic and evolutionary consequences,58 largely because inbred offspring have lower fitness than outcrossed offspring, that is, inbreeding depression.59–62 Laboratory and field studies of plants and animals have shown that inbreeding depression is ubiquitous both in wild25,26,63,64 and captive populations.65,66 Inbreeding depression is a major topic in population biology, which has traditionally been studied in relation to mating system evolution,60,67 dispersal strategies and social behavior,68 artificial breeding of agricultural stocks,59 and later on, in the habitat fragmentation context,28 and in relation to the maintenance of rare and endangered species.69 Inbreeding depression can be expressed in a range of plant traits, including germination,70 biomass,71 survival,61 reproduction,72 and interaction with pollinators, pathogens, and herbivores73–76 Inbreeding depression is predicted to differ between traits of different developmental stages because of differential selection.62 However, studies have reported the absence of correlations between metrics of inbreeding depression and life history stages.77,78 Furthermore, the same trait can be differently influenced by inbreeding in different species and populations70,79 and may show greater inbreeding depression in stressful environments than in controlled environments.80 In general, the ability to face environmental stress is reduced in inbred individuals,81
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and inbreeding depression is often more severe in stressed environments.21,82 Effects of climate change on plants The anthropogenic “greenhouse gas-driven” climate change refers to the recent human-induced increase in global temperature, altered precipitation, and increased CO2 concentrations.23,83 In addition to physiological responses to these changes, biotic changes, including species invasions, have been widely documented as a result of recent climate change.84 Hence, it is not surprising that there is ample evidence of the wide ecological impacts of the recent climate change on a global scale. The reported effects include changes in phenology and physiology, range and distribution of species, composition of communities and interactions between species, and the structure and dynamics of ecosystems.4,84,85,88 Climate change is especially challenging for plants, which, due to their sessile nature, are restricted in their abilities to respond to unsuitable conditions. Increased temperature and CO2 levels and altered precipitation and seasonality are the most important abiotic changes for plants. These changes will influence plant ecophysiology and consequently affect growth and fitness both directly and indirectly.86,87 In addition, climate change can alter levels and distribution of genetic variation. Taken together, both the abiotic and biotic impacts of climate change exert significant selective pressures on plants,86 hence, having not only ecological, but also evolutionary consequences. Since the effects of climate change have been reviewed fairly inclusively and in detail elsewhere,84,85 they will not be reviewed in here. Interactive effects of fragmentation and climate change Studies investigating climate change effects in fragmented populations include reports on compromised migration due to increased distance of populations, or suitable habitat patches, due to fragmentation.15,16 Reduced adaptive potential due to reduced genetic variation of fragmented plant populations is also acknowledged,37 but we still lack detailed studies investigating these effects, especially under natural conditions or conditions related to climate change. Yet, considering the impact of habitat fragmentation and climate change individually,
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as done above, already reveals the main concerns related to the interactive effects. First, we need a better understanding of the impact of reduced genetic variation and inbreeding on the adaptive potential and plasticity under climate change (discussed in more detail below). Second, the mechanisms of inbreeding depression under environmental conditions linked to climate change urgently call for more investigations, especially under field conditions. The genetic and ecological consequences of habitat fragmentation on plants are fairly well understood. Similarly, evidence on the impact of climate change on plant life from gene expression, metabolomics and physiology, to plant fitness, and community responses is increasing rapidly. The challenge of future studies lies in combining the evidence, knowledge, and methodology of the two to investigate in greater detail the joint effects of fragmentation and climate change on plants.
conditions. They found that the expression of heatshock proteins and metabolism genes are affected by the high temperature stress, while genes involved in metabolism are in principal solely affected by inbreeding. Furthermore, Pedersen et al.100 investigated the biochemical effects of inbreeding on inbred and outbred lines of Drosophila, after exposure to benign temperature, heat stress, or cold stress. They found a significant change in metabolite levels between inbred and outbred lines, while, in contrast to the phenotypical and transcriptional observations, no significant difference on the metabolite profile between different temperature treatments could be found. The environmental dependency of the expression of inbreeding implies that inbreeding can change the potential for environmentally induced plasticity, the primary mechanism for sessile organisms to respond to environmental changes.101–102
Effects of environment on inbreeding depression Several studies have suggested that inbreeding depression strongly depends on the environmental conditions, and that the inbreeding load becomes increasingly expressed under more stressful conditions.58,80–82,89–94 This suggests that at least some recessive alleles become more deleterious under stressful conditions. In this case, deleterious recessive alleles can be purged more readily by means of natural selection.66,95,96 Armbruster and Reed,80 however, found that inbreeding depression increased significantly in stressful environments in only 48% of the studies included in their review. More recently, the effect of environment on inbreeding depression has been examined, not only at the phenotypical perspective, but also at the level of gene expression and physiological differences of inbred and outbred individuals.97,98 Genomic, proteomic, and metabolomic approaches are required in order to investigate architecture of inbreeding depression under environmental stress, such as climate-driven changes in environmental conditions.97,98 We still lack studies on inbreeding depression or effects at the different “omic” levels in plants, but investigations have been conducted in other organisms.99,100 Kristensen et al.99 showed that inbred and noninbred lines of Drosophila display a markedly different gene expression after exposure to nonstressful and stressful (heat stress)
Biotic interactions in fragmented plant populations under climate change Both habitat fragmentation and climate change can alter the identity and abundance of competitors, herbivores, pollinators, and pathogens that interact with plants.52,86,103 While habitat fragmentation is more likely to alter the existing communities of organisms interacting with plants, climatic change may also bring plants in contact with novel species as distribution of many species changes. Theoretical work suggests that variation in how interactive species evolve or coevolve is the major force in the organization of biological communities and biodiversity.104–106 Therefore, to understand effects of climate change and fragmentation on populations, their viability, and ultimately on biodiversity, we need to consider biotic interactions in combination with the genetic and abiotic conditions. Effects of habitat fragmentation and climate change on plant–pollinator interactions have been reviewed separately elsewhere (e.g.,107 [fragmentation];108 [climate change]). Moreover, the consequences of mismatches of interactive species due to altered phenologies were briefly discussed above. Here, we focus on discussing antagonistic interactions of plant and their natural enemies in fragmented populations under climate change. Understanding joint effects of habitat fragmentation and climate change on species interactions is also essential considering the spread of invasive species, a phenomenon, which
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can be enhanced by climate change, but restricted due to fragmentation. Antagonistic interactions in fragmented plant populations under climate change Investigations of climate change effects on plant– herbivore interactions report direct and indirect effects of temperature on insect herbivores,109 effects of elevated O3 and CO2 on leaf chemistry and herbivore performance (reviewed in110 ), and effects of vertebrate herbivory on community response to warming.111 In addition to changing the composition of the interactive communities and abundances of individual species, climate change can affect plant quality for its natural enemies, hence having cascading effects on enemy performance.109,110 As pointed out by Post and Pedersen,111 herbivory can play an important role in determining the abilities of plant communities to respond to climate change, but also the impact of climate change on these communities. To the extent that herbivory constrains plant responses to climate change, or complicates the effects of climate change has been rarely studied. It is, however, clear that conclusions drawn from studies that do not incorporate biotic interactions can be misleading. In addition to altering abundance and composition of herbivore communities, habitat fragmentation can influence plant–herbivore interactions via the genetic effects it has on the interacting species. Since plant responses to natural enemies, such as herbivores, often have a genetic basis,112–116 any changes in levels and distribution of genetic variation are likely to affect plant–enemy interactions. So far relatively few studies have investigated effects of inbreeding on plant resistance or tolerance to herbivore damage,74,76,117–120 or pathogen infection rates.73 Inbreeding effects on plant defense can manifest themselves as altered suitability, resistance, or tolerance to natural enemies.74,119–121 Most studies have found evidence for inbreeding depression in resistance or tolerance,74,76,117–120 while others have not.76,117 A recent study on 17 fragmented Lychnis flos-cuculi populations demonstrated how inbreeding effects on resistance varies among populations depending on their genetic, abiotic, and biotic history.76 Moreover, herbivore damage has been shown to alter inbreeding effects on plant fitness.76 Although the impacts of fragmentation and climate change on plant–herbivore interactions have
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recently been investigated separately, their joint effects remain largely unexplored. Piessens et al.122 investigated how fragmented populations of Anthyllis vulneraria and its specialist herbivore Cupido minimus are influenced by extreme weather conditions. They found that the extinction probability of butterfly populations followed by the extreme conditions was significantly higher for small compared to large populations.122 The authors concluded that higher trophic levels are more susceptible to extinction due to habitat fragmentation and disturbance due to extreme weather conditions.122 It is clear that the impact of habitat fragmentation and climate change on biodiversity reflects their complex and joint effects on species and their interactions. Hence, more studies are needed to investigate, for example, effects of inbreeding and climate change-mediated changes in the abiotic and biotic conditions on species interactions and their ecological and evolutionary dynamics Coping with climate change When plants face new selection pressures, such as those imposed by climate change, there are basically three ways to respond84,123 : First, they can die. Second, they can “escape” the unfavorable conditions by dispersing to other areas. Third, they can stay and face the changing conditions either by means of phenotypic plasticity or via genetic changes through the process of evolution, leading to local genetic adaptations. While the first two options lead to local extinctions and possible colonization elsewhere, the third option, phenotypic plasticity and adaptation, can prevent local extinction. Due to their sessile nature, dispersal capacities in plants are usually very limited.124 Increased interhabitat distances due to habitat fragmentation, colonization of new areas (“range shift”) is not always a possible response to climate change in plants, or it may be too slow. Phenotypic plasticity is considered the primary mechanism for plants to respond to environmental changes.101,102 However, phenotypic plasticity is unlikely to provide a long-term solution for challenges faced by populations experiencing continued directional environmental change and there are limits to phenotypic plasticity.125–127 Hence, adaptive genetic differences may be developed.128,129 However, in many plant populations, the levels of genetic variation are too low for an evolutionary response and therefore
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plasticity remains the essential way of responding to changing environments.34 Adaptation Adaptation is considered as the perquisite for longterm survival under climate change. Today, many plant populations are small and isolated due to habitat fragmentation and at the same time they may face a rapidly changing environment into which they need to adapt. Adaptive potential is, however, likely to be reduced in small populations due to reduced genetic variation.3,34,130 Quantitative genetic theory predicts that potential to respond to selection decreases linearly with population size and an as a consequence the adaptive potential decreases.131,132 The potential and probable levels of adaptation, and how these might be compromised, in fragmented populations under climate change, must be considered from two different perspectives. First, we need to understand the levels and rates of adaptive evolution under climate change and how these are affected by inbreeding and level of genetic variation. Second, we need to know the degree to which plant populations are locally adapted. Adaptive evolution refers to adaptive evolutionary changes that maintain or enhance survival and/or fitness in response to climate change. Local adaptation is, in turn, central as it can determine how well plants perform under altered environmental conditions, or under the novel conditions faced after climate change-mediated dispersal to new areas (“range shift”). Moreover, local adaptation is an important process maintaining phenotypic diversity in the wild.133 Local adaptation can be influenced by fragmentation in two ways. First, if increased isolation leads to reduction in gene flow among population, fragmentation can enhance local adaptation in population occurring in heterogeneous landscapes. In a nonfragmented landscape, gene flow will override the local selection pressures by continuously mixing populations. However, in a fragmented landscape, with low or absent gene flow, local selection will be dominating the population genetic dynamics, and local populations will increasingly become adapted to their local environment34,128,134 Second, if fragmented populations are very small, thus having reduced genetic variation, local adaptation may be less likely.128,135 Numerous studies have investigated levels of local adaptation by comparing population differenti-
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ation in quantitative traits (QST ) to that observed in neutral marker genes (F ST ).For example, 133 Empirical data suggest that the degree of genetic differentiation in quantitative traits among populations commonly exceeds that for marker genes, indicating that quantitative traits are under directional selection and that the magnitude and direction of this selection varies among populations and thus local adaptation.133 The other traditional approach to investigate local adaptations to different habitat types or environmental conditions or across climate gradients, especially in plants, is reciprocal transplant experiments. In a recent meta-analysis of reciprocal transplant experiments Hereford136 demonstrates that local adaptation is common, but that many populations may be prevented from adapting to their local environments. Adaptive divergence was found to depend on environmental differences, limited gene flow, and genetic drift (Hereford136 ). Another recent meta-analysis of transplant experiments in plants found, in turn, that less than half of the investigated populations were locally adapted.135 Moreover, in contrast to predictions128,135,137–139 local adaptations were not influenced by geographic distance of the transplant sites, or by the spatial habitat heterogeneity and temporal variability, or plant life history traits.135 The most important finding in respect to habitat fragmentation and climate change was, however, that evidence for local adaptation was commonly only found for large plant populations and very rarely for small populations.135 Somewhat in contrast to this finding, McKay et al.140 found that populations of the rare and endemic Arabis fecunda are physiologically adapted to the local microclimate despite absence of divergence in marker loci and very small effective population size. Very few studies have investigated genetic adaptation to climate change in plants. Potvin and Tousignant141 investigated genetic adaptation in Brassica juncea in response to simulated global change where both temperature and CO2 levels were increased gradually. After seven generations of selection, evidence for genetic adaptation was found only for one out of the 14 investigated traits, while 11 traits responded plastically to the altered environment.141 The authors concluded that selection was likely to be limited due to inbreeding depression induced by harsh environmental conditions. In another study, Ward and Kelly142 reviewed evidence on
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evolutionary responses of plants to elevated CO2 . Altered CO2 concentrations have been found to affect different components of fitness, such as survival and seed production, plant physiology, growth and development, and these effects commonly vary among genotypes.142 This reflects genetic variation in plant responses to altered CO2 concentrations and potential for evolutionary response. More studies investigating the impact of population size, inbreeding, and genetic variation on both local adaptation and adaptive evolution, especially in response to climate change, are urgently needed. When considering effects of fragmentation on adaptive potential or adaptation under climate change it is also important to consider adaptive evolution and local adaptations of interacting species. This is because local adaptation strongly drives adaptive differentiation among species.143,144 Plasticity Phenotypic plasticity refers to the ability of an individual to alter its phenotype in response to changes in environmental conditions.101,102,145,146 Plasticity can be adaptive, but not all plastic responses are adaptive. Moreover, expression of phenotypic plasticity is often limited due to lack of genetic variation, architectural constraints, or resource limitation.145,146 This raises important considerations of plasticity as response to climate change in fragmented plant population. First, we need to understand the effects of genetic variation on plasticity. Plasticity has a genetic basis and genetic variation in plasticity has been widely documented.146 Like any trait, evolutionary changes in plasticity are due to selection, drift, and disruption of the genetic system.145 Plasticity is predicted to correlate negatively with heterozygosity, because of an increase in developmental stability due to deleterious recessive alleles expressed when homozygous.145 Alternatively, a negative correlation between plasticity and heterozygosity may arise if the two represent alternative ways in which to cope with environmental heterogeneity.139 Regardless of these suggested associations of heterozygosity and plasticity, there does not seem to be a consistent link between the two and the existing evidence is contradicting.140 Inbreeding increases developmental instability in predominantly outcrossing plants.147,148 This instability arises due to expression of deleterious recessive alleles, and increased sensitivity to internal environ-
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mental variation due to homozygosity.148 It has been argued that if inbreeding leads to decreased developmental canalization, it is likely that it can also lead to increased developmental phenotypic plasticity in response to external environmental variation.149 Only very few studies have investigated inbreeding effects on plasticity.150 Schlichting and Levin150 found no effects of inbreeding on phenotypic plasticity in cultivated Phlox drummondii. Although the majority of studies focused on reporting effects on mean fitness,28,36 habitat fragmentation can also influence phenotypic variation within and between environments151 and plasticity.152,153 This can arise, because reduced genetic variation in small fragmented populations can prevent nonadaptive phenotypic variation, that is, development instability within individuals.28,153,154 Fischer et al.153 found limited adaptive plasticity in plants from small population of the clonal Ranunculus reptans. Hence, they concluded that reduced adaptive plasticity, due to reduced genetic variation, might lead to reduced fitness of small plant populations in spatially and temporally heterogeneous environments. This is an important consideration for the viability of fragmented plant populations under climate change and clearly calls for further investigations. Range shifts and migration in fragmented landscape Shifts in distribution ranges of numerous species have been documented in response to climate change85,155 and many more are expected to shift with future climate change.156 Evidence supporting the predicted shifts in species’ ranges poleward in latitude and upward in elevation157 has been found across taxa.19,84,158,159 Species move to trace the optimal climate, which reflects their environmental preference (“climate envelope”). Investigations of historic range shifts of species in response to changes in climatic conditions suggest that the rate of the current anthropogenic climate change is too rapid compared to the colonization and establishment rates of many species, which therefore are potentially unable to track the climate to which they are adapted to.160 In addition to being sessile, plants are often poor dispersers, which challenges their ability to respond to climate change by dispersal to new locations, that is, range shifting. Habitat fragmentation is likely to further
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complicate dispersal and range shift. Habitat fragmentation has, indeed, been shown to reduce colonization rates, both the colonization of a new species and recolonization of previously present species, because it increases isolation of populations or suitable habitat patches and decreases their connectivity.161 In addition to the physical challenges fragmentation sets for tracing the optimal climate, the role of the fragmentation-mediated genetic erosion in the colonization process should be better understood. There is a long-standing body of theory and data suggesting that genetic diversity falls as one moves toward the margins of a species’ distribution,162,163 as a result of genetic drift and inbreeding in the generally small and highly fragmented marginal populations. Hence, on the leading edge of the range expansion populations face the same genetic problems as small fragmented populations. As discussed above, reduced genetic variation and increased inbreeding likely reduce the adaptive potential of plants, thus affecting their ability to cope with the new conditions in the new areas. Populations are predicted to be smaller and levels of inbreeding greater in marginal populations, yet, it is still debatable whether and under what conditions this is the case.164 Some studies have found lower levels of neutral genetic variation in marginal populations.165 However, these differences were not always striking and opposite patterns were observed as well. Due to their small population sizes, high degree of isolation and limitation to interpopulation movement, marginal populations may provide vital information on how species might respond to climate change. Furthermore, theory suggests that shifts in marginal populations and changes in their demography could be one of the first and most sensitive signs a species’ response to environmental change.166–168 Finally, if fragmented plant populations that are already genetically eroded serve as source populations for colonization, the founder effects and other genetic consequences of small populations, might have even more severe consequences for population viability. If we are to understand the impact of habitat fragmentation on the range shift in plants as response to climate change we need to consider the effects of inbreeding on traits linked to dispersal, colonization, and establishment. Few studies have investigated inbreeding effects on dispersal traits and found contrasting results: reduced dispersal po-
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tential was found for fragmented populations of Hypochaeris radicata78,169, but not for Tragopogon pratensis.170 More studies are needed on inbreeding effects on dispersal in the field and also under environmental conditions linked to climate change. In addition to affecting dispersal potential, inbreeding can also reduce seed germination70 and seedling establishment. Hence, it is clear that by increasing levels of inbreeding, habitat fragmentation can affect the ability of plants to respond to climate change via dispersal and colonization of new areas. It is, of course, important to understand that, as discussed above, effects of inbreeding depend on population genetic history and environmental conditions and hence these factors should not be neglected in further investigations. Conservation implications, future challenges, and avenues Predicting biodiversity losses due to climate change and habitat fragmentation and to best mitigate their negative impacts, we ought to be able to estimate species’ susceptibility to these threats. This remains a challenging task, because we still lack detailed studies of the combined effects of climate change and fragmentation on population viability and extinction risk. IUCN is developing assessment tools to identify climate change effects on species to better identify those most susceptible and vulnerable.88 The aims include examining to what extent the existing IUCN Red List Criteria could be used for also identifying species most at risk under climate change.88 This provides an opportunity to assess, at least to some degree, the combined risks from climate change and fragmentation. IUCN’s work so far, however, indicates that, although a high number of species that are already threatened are also most susceptible under climate change, the match is not complete. IUCN states that previous assessments of extinctions under climate change did not consider biological differences between species,88 which challenges future assessments, but also research directions. Systematic reviewing by means of meta-analysis could provide a useful tool to reveal among species variation in their responses to climate change and fragmentation. Yet, more case studies covering vast range of species and habitats of most concern are also urgently needed.
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IUCN has identified five groups of traits that are believed to be associated with increased susceptibility to climate change.88 These include specialized habitat and/or microhabitat requirements; Narrow environmental tolerances or thresholds that are likely to be exceeded due to climate change at any stage in the life cycle; Dependence on specific environmental triggers or cues that are likely to be disrupted by climate change; Dependence on interspecific interactions that are likely to be disrupted by climate change; and Poor ability to disperse to or colonize a new or more suitable range. To better understand how susceptibility to climate change is modified by habitat fragmentation, we need more investigations on how the traits associated with susceptibility are influenced by the genetic and environmental consequences of fragmentation. Climate change is influencing physical and biological environments globally, but the impacts vary among different areas and habitats.23 While some areas suffer from drought and decreased precipitation, others experience higher annual rainfall.23,83 Similarly, the local temperature changes and variability in weather conditions are very different across areas.23,83 Details of the observed and predicted changes on a global scale are reported in the recent synthesis report of IPCC.23 It is clear that natural ecosystems and biodiversity will be sustainably affected by climate change (“very high confidence”) and that the majority of organisms and ecosystems are likely to have difficulties in adapting to climate change (“high confidence”). The same IPCC report lists the following major impact of climate change on ecosystems: “Ecosystem resilience is likely to be exceeded by an unprecedented combination of climate change, associated disturbances (e.g., flooding, drought, wildfire, insects, ocean acidification), and other global change drivers (e.g., land-use change, pollution, fragmentation of natural systems, overexploitation of resources); Net carbon uptake by terrestrial ecosystems is likely to peak before midcentury and then weaken or even reverse, thus amplifying climate change; Approximately 20% to 30% of plant and animal species assessed so far are likely to be at increased risk of extinction if increases in global average temperature exceed 1.5 to 2.5◦ C (“medium confidence”); and Climate change is projected to result in major changes in ecosystem structure and function, species’ ecological interactions,
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and shifts in species’ geographical ranges, with predominantly negative consequences for biodiversity and ecosystem goods and services, for example, water and food supply.23 Systems and regions that are predicted to be especially affected by climate change include particular ecosystems, such as tundra, boreal forest and mountain regions, Mediterranean-type ecosystems, tropical rain forests, mangroves, and salt marshes.23 This information together with the knowledge on types of species most susceptible should be further combined with information on the distribution of other anthropogenic threats, such as habitat fragmentation. We need to know more about the distribution and levels of genetic variation and how the underlying genetic structure of populations compromise or influence abilities to respond to climate change in different areas where the challenges can be very different. Conclusions and research avenues Climate is changing at a greater rate than ever before and we have now reached a point where climate change may outpace the ability of many plants to either migrate or adapt.16 Furthermore, some species adapt much more rapidly to new conditions than others, which results in changes in species’ composition and dominance of these better adapted species. The abilities of plants to respond to climate change are, however, to an increasing degree compromised due to the genetic problems associated with the increased fragmentation of habitats. Therefore, we need more investigations of the interactive effects of the fragmentation-mediated genetic erosion and climate change on population viability and extinction risk. The focus should be on the areas, habitats, and species of most concern, taking into account the specific observed and predicted physiological and biological changes at the given area. More mechanistic studies on inbreeding, climate change, and their interaction should be performed. A promising avenue seems to be to adopt an ecogenomic approach, in which gene expression as function of environmental and genetic stress is investigated.171 Many environmental stress factors elicit specific transcription profiles.172 These profiles can be studied in individuals of genetically eroded populations, in inbred and outbred individuals, and in progeny of crosses between populations, under climate change and control conditions. In
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addition, phenotypic trait studies of inbred and outbred individuals under climate change and control conditions can tell us how inbreeding would limit fitness as a function of climate change. Conflicts of interest The authors declare no conflicts of interest. References 1. Palumbi, S.R. 2001. Humans as the world’s greatest evolutionary force. Science 293: 1786–1790. 2. Tilman, D. & C. Lehman. 2001. Human-caused environmental change: impacts on plant diversity and evolution. PNAS 98: 5433–5440. 3. Stockwell, C.A., A.P. Hendry & M.T. Kinnison. 2003. Contemporary evolution meets conservation. Trends Ecol. Evol. 18: 94–101. 4. Walther, G.-R., E. Post, P. Convey, et al. 2002. Ecological responses to recent climate change. Nature 416: 389– 395. 5. Thuiller, W., S. Lavorel, M.B. Araujo, et al. 2005 Climate change threats to plant diversity in Europe. PNAS 102: 8245–8250. 6. Honnay, O., H. Jacquemin, B. Bossuit & M. Hermy. 2005. Forest fragmentation effects on patch occupancy and population viability of herbaceous plant species. New Phytologist 166: 723–736. 7. Aguilar, R., L. Ashworth, L. Galetto & M.A. Aizen. 2006. Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol. Lett. 9: 968–980. 8. Lawson, D.M., C.K. Lamar & M.W. Schwartz. 2008. Quantifying plant population persistence in humandominated landscapes. Conservation Biol. 22: 922– 928. 9. Schleuning, M., N. Niggeman, U. Becker & D. Matthies. 2009. Negative effects of habitat degradation and fragmentation on the declining grassland plant Trifolium montanum. Basic Appl. Ecol. 10: 61–69. 10. Bruna, E.M., I.J. Fiske & M.D. Trager. 2009. Habitat fragmentation and plant populations: is what we know demographically relevant? J. Vegetational Sci. 20: 569– 576. 11. Cousins, S.A.O. 2009. Extinction debt in fragmented grasslands: paid or not? J. Vegetation Sci. 20: 3–7 12. Feehan, J., M. Harley & J. van Minnen. 2009. Climate change in Europe 1. Impact on terrestrial ecosystems and biodiversity. A review. Agron. Sustain. Dev. 29: 409– 421
Habitat fragmentation, climate change and inbreeding in plants
13. Fratterigo, J.M., S.M. Pearson & M.G. Turner. 2009. Joint effects of habitat configuration and temporal stochasticity on population dynamics. Landscape Ecol. 24: 863–877 14. Randin, C.F., R. Engler, S. Normand, et al. 2009. Climate change and plant distribution: local models predict high-elevation persistence. Glob. Change Biol. 15: 1557–1569. 15. Opdam, P. & D. Wascher. 2004. Climate change meets habitat fragmentation: linking landscape and biogeographical scale levels in research and conservation. Biol. Conserv. 117: 285–297. 16. Jump, A.S. & J. Penuelas. 2005. Running to stand still: adaptation and the response of plants to rapid climate change. Ecol. Lett. 8: 1010–1020. 17. Sork, V.L., J. Nason, D.R. Campbell & J.F. Fernandez. 1999. Landscape approaches to historical and contemporary gene flow in plants. TREE 14: 219– 224 18. Sork, V.L. & P.E. Smouse. 2006. Genetic analysis of landscape connectivity in tree populations. Landscape Ecol. 21: 821–836. 19. Honnay, O., K. Verheyen, J. Butaye, et al. 2002. Possible effects of habitat fragmentation and climate change on the range of forest plant species. Ecol. Lett. 5: 525– 530. 20. Thuiller, W., C. Albert, M.B. Araujo, et al. 2008. Predicting global change impacts on plant species’distributions: future challenges. Perspect. Plant Ecol. Evol. Syst. 9: 137–152. 21. Frankham, R., J.D. Ballou & D.A. Briscoe. 2002. Introduction to Conservation Genetics. Cambridge University Press. Cambridge, UK. 22. Ceriani, R.M., S. Pierce & B. Cerabolini. 2009. The survival strategy of the alpine Primula glaucescens is fundamentally unchanged throughout its climate envelope despite superficial phenotypic variability. Plant Ecol. 204: 1–10 23. IPCC. Climate Change. 2007. Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Core Writing Team, Pachauri, R.K. and Reisinger, A. Eds.: pp 104. IPCC, Geneva, Switzerland. 24. Lande, R. 1993. Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Nat. 142: 911–927 25. Saccheri, I., M. Kuussaari, M. Kankare, et al. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392: 491–494.
c 2010 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1195 (2010) 84–98
93
Leimu et al .
Habitat fragmentation, climate change and inbreeding in plants
26. Westemeier, R.L., J.D. Brown, S.A. Simpson, et al. 1998. Tracking the long-term decline and recovery of an isolated population. Science 282: 1695–1698. 27. Ellstrand, N.C. & D.R. Elam. 1993. Population genetic consequences of small population size: implications for plant conservation. Annu. Rev. Ecol. Syst. 24: 217–243. 28. Young, A., T. Boyle & T. Brown. 1996. The population genetic consequences of habitat fragmentation for plants. Trends Ecol. Evol. 11: 413–418. 29. Lande, R. 1995. Mutation and conservation. Conservation Biol. 9: 782–791. 30. Leimu, R., P. Mutikainen, J. Koricheva & M. Fischer. 2006. How general are positive relationships between plant population size, fitness and genetic variation? J. Ecol. 94: 942–952. 31. Lynch, M., J. Conery & R. B¨urger. 1995. Mutation accumulation and the extinction of small populations. Am. Nat. 146: 489–518. 32. Barrett, S.C. & J.R. Kohn. 1991. Genetic and evolutionary consequences of small population size in plants: implications for conservation. In Genetics and Conservation of Rare Plants. D.A. Falk & K.E. Holsinger, Eds.: 3–30. Oxford University Press. New York.. 33. Lynch, M. 1996. A quantitative-genetic perspective on conservation issues. In Conservation Genetics. Case Histories from Nature. J.C. Avise & J.L. Hamrick, Eds.: 471– 501. Chapman & Hall. New York. 34. Pertoldi, C., R. Bijlsma & V. Loeschcke. 2007. Conservation genetics in a globally changing environment: present problems, paradoxes and future challenges. Biodiv. Conserv. 16: 4147–4163. 35. Wright, S. 1978. Evolution and the Genetics of Populations Volume 4–Variability within and among Natural Populations. University of Chicago Press. Chicago, IL. 36. Slatkin, M. 1985. Rare alleles as indicators of gene flow. Evolution 39: 53–65. 37. Cain, M.L., B.G. Milligan & A.E. Strand. 2000. Longdistance dispersal in plant populations. Am. J. Bot. 87: 1217–1227. 38. Raybould, A.F., R.T. Clarke, J.M. Bond, et al. 2002. Inferring patterns of dispersal from allele frequency data. In: Dispersal Ecology. 42nd Symposium of the British Ecological Society. J. M. Bullock, R.E. Kenward & R.S. Hails, Eds.: 89–110. Blackwell. Malden, MA. 39. Eckstein, R.L., R.A. O’Neill, J. Danihelka, et al. 2006 Genetic structure among and within peripheral and central populations of three endangered floodplain violets. Mol. Ecol. 15: 2367–2379. 40. Kunin, W.E., P. Vergeer, T. Kenta, et al. 2009. Variation at range margins across multiple spatial scales: environ-
94
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
mental temperature, population genetics and metabolic phenotype. Proc. R. Soc. B 276: 1495–1506. Templeton, A.R. 1986. Coadaptation and outbreeding depression. In Conservation Biology: The Science of Scarcity and Diversity. M.E. Soul´e, Ed.: 105–116. Sinauer. Sunderland, UK. Fischer, M. & D. Matthies. 1997. Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae). Am. J. Bot. 84: 1685–1692. Hufford, K.M. & S.J. Mazer. 2003. Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol. Evol. 18: 147–155.. Rathcke, B.J & E.S. Jules. 1993. Habitat fragmentation and plant-pollinator interactions. Curr. Sci. 65: 273– 278. Olesen, J.M. & S.K. Jain. 1994. Fragmented plant populations and their lost interactions. In: Conservation Genetics. V. Loeschcke, J. Tomiuk & S.K. Jain, Eds.: 417–426. Birkhauser. ˚ Agren, J. 1996. Population size, pollination limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77: 1779–1790. Waites, A.R. & J. Agren. 2004. Pollinator visitation, stigmatic pollen loads and among-population variation in seed set in Lythrum salicaria. J. Ecol. 92: 512–526. Kolb, A. 2005. Reduced reproductive success and offspring survival in fragmented populations of the forest herb Phyteuma spicatum. J. Ecol. 93: 1226–1237. Sih, A. & M.S. Baltus. 1987. Patch size, pollinator behavior, and pollinator limitation in catnip. Ecology 68: 1679–1690. Jennersten, O. 1988. Pollination in Dianthus deltoids (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conservation Biol. 2: 359–366. Lennartsson, T. 2002. Extinction thresholds and disrupted plant-pollinator interactions in fragmented plant populations. Ecology 83: 3060–3072. K´ery, M., D. Matthies & M. Fischer. 2001. The effect of plant population size on the interactions between a rare plant Gentiana cruciata and its specialist herbivore Maculinea rebeli. J. Ecol. 89: 418–427. Colling, G. & D. Matthies. 2004. The effects of plant population size on the interactions between the endangered plant Scorzonera humilis, a specialised herbivore, and a phytopathogenic fungus. Oikos 105: 71–78. Von Zeipel, H., O. Eriksson & J. Ehrlen. 2006. Host plant population size determines cascading effects in a plant–herbivore–parasitoid system. Basic Appl. Ecol. 7: 191–200.
c 2010 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1195 (2010) 84–98
Leimu et al .
55. Saunders, D.A., R.J. Hobbs & C.R. Margules. 1991. Biological consequences of ecosystem fragmentation. Conservation Biol. 5: 18–32. 56. Jules, E.S. & P. Shahani. 2003. A broader ecological context to habitat fragmentation: why matrix habitat is more important than we thought. J. Vegetation Sci. 14: 459–464. 57. Arroyo-Rodr´ıguez, V. & S. Mandujano. 2006. The importance of tropical rain forest fragments to the conservation of plant species diversity in Los Tuxtlas, Mexico. Biodiv. Conserv. 15: 4159–4179. 58. Keller, L.F. & D.M. Waller. 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17: 230–241. 59. Falconer, D.S. 1981. Introduction to Quantitative Genetics. 2nd ed. Longman. London. 60. Charlesworth, D. & B. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 1: 237–268. 61. Husband, B.C. & D.W. Schemske. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54–70. 62. Charlesworth, D. & J.H. Willis. 2009. The genetics of inbreeding depression. Nat. Rev. Genet. 10: 783–796. 63. Crnokrak, P. & D.A. Roff. 1999. Inbreeding depression in the wild. Heredity 83: 260–270. 64. O’Grady, J.J., B.W. Brook, D.H. Reed, et al. 2006. Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol. Conserv. 133: 42–51. 65. Bijlsma, R., J. Bundgaard & A.C. Boerema. 2000. Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J. Evol. Biol. 13: 502–514. 66. Reed, D.H., E.H. Lowe, D.A. Briscoe & R. Frankham. 2003. Inbreeding and extinction: effects of rate of inbreeding. Conservation Genet. 4: 405–410. 67. Uyenoyama, M.K., K.E. Holsinger & D.M. Waller. 1993. Ecological and genetic factors directing the evolution of self- fertilization. Oxford surv. Evol. Biol. 9: 327–381. 68. Thornhill, N.W. 1993. The Natural History of Inbreeding and Outbreeding. University of Chicago Press. Chicago, IL. 69. Frankham, R. 1995. Inbreeding and extinction: a threshold effect. Conservation Biol. 9: 792–799. 70. Sheridan, P.M. & D.N. Karowe. 2000. Inbreeding, outbreeding and heterosis in the yellow pitcher plant, Sarracenia flava (Sarraceniaceae), in Virginia. Am. J. Bot. 87: 1628–1633. 71. Galloway, L.F., J.R. Etterson & J.L. Hamrick. 2003. Outcrossing rate and inbreeding depression in the herba-
Habitat fragmentation, climate change and inbreeding in plants
72.
73.
74.
75.
76.
77.
78.
79.
80.
81.
82.
83.
c 2010 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1195 (2010) 84–98
ceous autotetraploid, Campanula americana. Heredity 90: 308–315. Husband, B.C. & D.W. Schemske. 1997. The effect of inbreeding in diploid and tetraploid populations of Epilobium angustifolium (Onagraceae): implications for the genetic basis of inbreeding depression. Evolution 51: 737–746. Ouborg, N.J., A. Biere & C.L. Mudde. 2000. Inbreeding effects on resistance and transmission-related traits in the Silene-Microbotryum pathosystem. Ecology 81: 520–531. Carr, D.E. & M.D. Eubanks. 2002. Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae). Evolution 56: 22–30. Ouborg, N.J. & A. Biere. 2003. The relationship between plant-pathogen and plant–herbivore interactions and plant population persistence in a fragmented landscape. In PopulationViability Analysis in Plants. C.A. Brigham & M.W. Schwartz, Eds.: 99–116. SpringerVerlag. Berlin. Leimu, R., L. Kloss & M. Fischer. 2008. Effects of experimental inbreeding on herbivore resistance and plant fitness: the role of history of inbreeding, herbivory and abiotic factors. Ecol. Lett. 11: 1101–1110. ˚ Agren, J. & D.W. Schemske. 1993. Outcrossing rate and inbreeding depression in two monoecious herbs, Begonia hirsuta and B. semiovata. Evolution 47: 125– 135. ´ F.X., N.J. Ouborg & J.M. Van Groenendael. 2004. Pico, Evaluation of the extent of among-family variation in inbreeding depression in the perennial herb Scabiosa calumbaria (Dipsacaceae). Am. J. Bot. 91: 1183–1189. Dudash, M.R. & C.B. Fenster 2001. The role of breeding system and inbreeding depression in the maintenance of an outcrossing mating strategy in Silene virginica (Caryophyllaceae). Am. J. Bot. 88: 1953–1959. Armbruster, P. & D.H. Reed. 2005. Inbreeding depression in benign and stressful environments. Heredity 95: 235–242. Bijlsma, R., J. Bundgaard & W.F. Van Putten. 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J. Evol. Biol. 12: 1125–1137. Dudash, M.R. 1990. Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44: 1129–1139. IPCC. 2007: Climate change 2007: impacts, adaptation and vulnerability. In Contribution of Working Group II
95
Habitat fragmentation, climate change and inbreeding in plants
84.
85.
86.
87.
88.
89. 90.
91. 92.
93.
94.
95.
96.
97.
96
to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. M.L. Parry, O.F. Canziani, J.P. Palutikof, P.J. van der Linden & C.E. Hanson, Eds.: 976. Cambridge University Press. Cambridge, UK. Parmesan, C. & G. Yohe. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42. Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Syst. 37: 637–669. Geber, M.A. & T.E. Dawson. 1993. Evolutionary responses of plants to global change. In: Biotic Interactions and Global Change. P. Kareiva, J.G. Kingsolver & R.B. Huey, Eds.: 179–197. Sinauer Associates Inc. Sunderland, MA. Korner, C.H. Plant CO2 responses: an issue of definition, time and resource supply. New Phytologist 172: 393–411. Foden, W.B., G.M. Mace, J.-C. Vie, et al. 2008. Species susceptibility to climate change impacts. IUCN, Species Survival Commission. Coman, N. & B. Wallace. 1973. Inbreeding depression and environmental stress. Genetika 5: 157–166. Hayes, C.N., J.A. Winsor, & A.G. Stephenson. 2005. Environmental variation influences the magnitude of inbreeding depression in Cucurbita pepo ssp. texana (Cucurbitaceae). J. Evol. Biol. 18: 147–155. Miller, P.S. 1994. Is inbreeding depression more severe in a stressful environment? Zool. Biol. 13: 195–208. Dahlgaard, J., R.A. Krebs & V. Loeschcke. 1995. Heatshock tolerance and inbreeding in Drosophila buzzatii. Heredity 74: 157–163. Bijlsma, R., J. Bundgaard, A.C. Boerema & W.F. Van Putten. 1997. Genetics and environmental stress, and the persistence of populations. In: Environmental Stress, Adaptation and Evolution. R. Bijlsma & V. Loeschcke, Eds.: 193–207. Birkhauser. Basel. Loeschcke, V., R.A. Krebs, J. Dahlgaard & P. Michalak. 1997. High-temperature stress and the evolution of thermal resistance in Drosophila. In: Environmental Stress, Adaptation and Evolution. R. Bijlsma & V. Loeschcke, Eds.: 175–190. Birkh.auser Verlag. Basel. Wool, D. & E. Sverdlov. 1976. Sib-mating populations in an unpredictable environment: effects on components of fitness. Evolution 30: 119–129. Armbruster, W.S. & D.G. Rogers. 2004. Does pollen competition reduce the cost of inbreeding? Am. J. Bot. 91: 1939–1943. Holloway, A.J., R.K. Van Laar, R.W. Tothil & D.D.L. Bowtell. 2002. Options available—from start to
Leimu et al .
finish—for obtaining data from DNA microarrays II. Nat. Genet. 32: 481–489. 98. MacBeath, G. 2002. Protein microarrays and proteomics. Nat. Genet. 32: 526–532. 99. Kristensen, T.N., J.G. Sørensen, K.S. Pedersen, et al. 2006. Inbreeding by environmental interactions affect gene expression in Drosophila melanogaster. Genetics 173: 1329–1336. 100. Pedersen, K.S., T.N. Kristensen, V. Loeschcke, et al. 2008. Metabolomic signatures of inbreeding at bening and stressful temperatures in Drosophila melanogaster. Genetics 180: 1233–1243. 101. Dudley, S.A. & J. Schmitt. 1996. Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. Am. Nat. 147: 445–465. 102. Bell, D.L. & L.F. Galloway. 2007. Plasticity to neighbor shade: fitness consequences and allometry. Funct. Ecol. 21: 1145–1152. 103. Steffan-Dewenter, I. & T. Tscharntke. 2002. Insect communities and biotic interactions in fragmented calcareous grasslands – a mini review. Biol. Conserv. 104: 274– 284. 104. Janzen, D.H. 1980. When is it coevolution? Evolution 34: 611–612. 104a. Jentsch, A., J. Kreyling, J. Bottcher-Treschkow & Beierkuhnlein. 2008. Beyond gradual warming – extreme weather events alter flower phenology of European grassland and heath species. Glob. Change Biol. doi: 10.1111/j.13652486.2008.01690.x. 105. Thompson, J.N. 1994. The Coevolutionary Process. University of Chicago Press. Chicago, IL. 106. Thompson, J.N. 1999. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 153(Suppl.): S1–S14. 107. Kearns, C.A., D.W. Inouye & N.W. Waser. 1998. Endangered mutualisms: the conservation of plant-pollinator interactions. Annu. Rev. Ecol. Syst. 29: 83–112. 108. Hegland, S.J., A. Nielsen, A. Lazaro, et al. 2009. How does climate warming affect plant–pollinator interactions? Ecol. Lett. 12: 184–195. 109. Bale, J.S., G.J. Masters & I.D. Hodkinson. 2002. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob. Change Biol. 8: 1–16 110. Valkama, E, J. Koricheva & E. Oksanen. 2007. Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob. Change Biol. 13: 184– 201.
c 2010 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1195 (2010) 84–98
Leimu et al .
111. Post, E. & C. Pedersen. 2008. Opposing plant community responses to warming with and without herbivores. PNAS 105: 12353–12358. 112. Marquis, R.J. 1984. Leaf herbivores decrease fitness of a tropical plant. Science 226: 537–539. 113. Marquis, R.J. 1990. Genotypic variation in leaf damage in Piper arieianum (Piperaceae) by a multispecies assemblage of herbivores. Evolution 44: 104–120. 114. Berenbaum, M.R., A.R. Zangerl & J.K. Nitao. 1986. Constraints on chemical coevolution: wild parsnip and the parsnip webworm. Evolution 40: 1215–1228. 115. Simms, E.L. & M.D. Rausher. 1987. Costs and benefits of plant defence to herbivory. Am. Nat. 130: 570–581. 116. Simms, E.L. & M.D. Rausher. 1989. The evolution of resistance to herbivory in Ipomoea purpurea. II. Natural selection by insects and costs of resistance. Evolution 43: 573–585. 117. Nunezfaran, J., R.A. Cabralesvargas & R. Dirzo. 1996. Mating system consequences on resistance to herbivory and life history traits in Datura stramonium. Am. J. Bot. 83: 1041–1049. 118. Hayes, C.N., J.A. Winsor & A.G. Stephenson. 2004. Inbreeding influences herbivory in Cucurbita pepo ssp. texana (Cucurbitaceae). Oecologia 140: 601–608. 119. Ivey, C.T., D.E. Carr & M.D. Eubanks. 2004. Effects of inbreeding in Mimulus guttatus on tolerance to herbivory in natural environments. Ecology 85: 567– 574. 120. Stephenson, A.G., B. Leyshon, S.E. Travers, et al. 2004. Interrelationships among inbreeding, herbivory, and disease on reproduction in a wild gourd. Ecology 85: 3023–3034. 121. Strauss, S.Y. & R. Karban. 1994. The significance of outcrossing in an intimate plant-herbivore relationship. I. Does outcrossing provide an escape from herbivores adapted to the parent plant? Evolution 48: 454– 464. 122. Piessens, K., D. Adriaens, H. Jacquemyn & O. Honnay. 2009. Synergistic effects of an extreme weather event and habitat fragmentation on a specialised insect herbivore. Oecologia DOI 10.1007/s00442–008-1204-x. 123. Brook, B.W., N.S. Sodhi & C.J.A. Bradshaw. 2008. Synergies among extinction drivers under global change. Trends Ecol. Evol. 23: 453–460. 124. Soons, M.B. & J.M. Bullock. 2008. Non-random seed abscission, long-distance wind dispersal and plant migration rates. J. Ecol. 96: 581–590. 125. de Jong, G. 2005. Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytologist 166: 101–118.
Habitat fragmentation, climate change and inbreeding in plants
126. Pigliucci, M. 1996. How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). Trends Ecol. Evol. 11: 168–173. 127. DeWitt, TJ, A. Sih & D.S. Wilson. 1998. Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13: 77–81. 128. Kawecki, T.J. & D. Ebert. 2004. Conceptual issues in local adaptation. Ecol. Lett. 7: 1225–1241. 129. Van Tienderen, P.H. 1997. Generalists, specialists, and the evolution of phenotypic plasticity in sympatric populations of distinct species. Evolution 51: 1372– 1380. 130. Antonovics, J. 1976. The nature of limits to natural selection. Ann. Miss Bot. Garden 63: 224–247. 131. Robertson, A. 1960. A theory of limits in artificial selection. Proc. R. Soc. Lond. B 153: 234–249. 132. Hill, W.G. 1982. Rates of changes in quantitative traits from fixation of new mutations. Proc. Nat. Aca. Sci. USA 79: 142–145. 133. Meril¨a, J. & P. Crnokrak. 2001. Comparison of genetic differentiation at marker loci and quantitative traits. J. Evol. Biol. 14: 892–903. 134. Antonovics, J. 1968. Evolution in closely adjacent plant populations. 4. Manifold effects of gene flow. Heredity 23: 507–524. 135. Leimu, R. & M. Fisher. 2008. A meta-analyses of local adaptations in plants. PLoS ONE 3: e4010. 136. Hereford, J. 2009. A quantitative survey of local adaptation and fitness trade-offs. Am. Nat. 173: 579–588. 137. Linhart, Y.B. & M.C. Grant. 1996. Evolutionary significance of local genetic differentiation in plants. Annu. Rev. Ecol. Syst. 27: 237–277. 138. Schmid, B. 1985. Clonal growth in grassland perennials. III. Genetic variation and plasticity between and within populations of Bellis perennis and Prunella vulgaris. J. Ecol. 73: 819–830. 139. Hastings, A. 1983. Can spatial variation alone lead to selection for dispersal? Theor. Pop. Biol. 24: 244–251. 140. McKay, J., J.G. Bishop, L. Jing-Zhong, et al. 2001. Local adaptation across a climate gradient despite small effective population size in the rare sapphire rockcress. Proc. R. Soc. Lond. B 268: 1715–1721. 141. Potvin, C. & D. Tousignant. 1996. Evolutionary consequences of simulated global change: genetic adaptation or adaptive phenotypic plasticity. Oecologia 108: 683– 693. 142. Ward, J.K. & J.K. Kelly. 2004. Scaling up evolutionary responses to elevated CO2 : lessons from Arabidopsis. Ecol. Lett. 7: 427–440. 143. Thompson, J.N. 2005. The Geographic Mosaic of Coevolution. University of Chicago Press.
c 2010 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1195 (2010) 84–98
97
Leimu et al .
Habitat fragmentation, climate change and inbreeding in plants
144. Hoeksema, J.D. & S.E. Forde. 2008. A meta-analysis of factors affecting local adaptation between interacting species. Am. Nat. 171: 275–290. 145. Schlichting, C.D. 1986. The evolutions of phenotypic plasticity in plants. Annu. Rev. Ecol. Syst. 17: 667–693. 146. Pigliucci, M. 2001. Phenotypic Plasticity: Beyond Nature and Nurture. The John Hopkins University Press. Baltimore and London. 147. Levin, D.A. 1970. Developmental instability and evolution in peripheral isolates. Am. Nat. 104: 343– 353. 148. Soul`e, M.E. 1982. Allometric variation. 1. The theory and some consequences. Am. Nat. 120: 751–764. 149. Bradshaw, A.D. 1965. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13: 115–155 150. Schlichting, C.D. & D.A. Levin. 1986. Effects of inbreeding on phenotypic plasticity in cultivated Phlox. Theor. Appl. Genet. 72: 114–119. 151. Siikamaki, P. & A. Lammi. 1998. Fluctuating asymmetry in central and marginal populations of Lychnis viscaria in relation to genetic and environmental factors. Evolution 52: 1285–1292. 152. K´ery, M., D. Matthies & H.H. Spillmann. 2000. Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J. Ecol. 88: 17–30. 153. Fischer, M., M. van Kleunen & B. Schmid. 2000. Genetic Allee effects on performance, plasticity and developmental stability in a clonal plant. Ecol. Lett. 3: 530–539. 154. Fowler, K. & M.C. Whitlock. 1999. The variance in inbreeding depression and the recovery of fitness in bottlenecked populations. Proc. R. Soc. Lond. B 266: 2061–2066. 155. Rosenzweig, C, D. Karoly, M. Vicarelli, et al. 2008. Attributing physical and biological impacts to anthropogenic climate change. Nature 453: 353–358. 156. Thomas, C.D., A. Cameron, R.E. Green, et al. 2004. Extinction risk from climate change. Nature 427: 145– 148. 157. Peters, R.L. & J.D.S. Darling. 1985. The greenhouse effect and nature reserves. BioScience 35: 707–717. 158. Parmesan, C. 1996. Climate and species’ range. Nature 382: 765–766. 159. Penuelas, J. & M. Boada. 2003. A global change-induced
98
160.
161.
162. 163.
164.
165.
166. 167.
168.
169.
170.
171.
172.
biome shift in the Montseny Mountains (NE Spain). Glob. Change Biol. 9: 131–140. Davis, M.B. & R.G. Shaw. 2001. Range shifts and adaptive responses to quaternary climate change. Science 292: 673–679. Joshi, J., P. Stoll, H. Rusterholz, et al. 2006. Small-scale experimental habitat fragmentation reduces colonization rates in species-rich grasslands. Oecologia 148: 144–152. Lewontin, R.C. 1974. The Genetic Basis of Evolutionary Change. Columbia University Press. New York. Lesica, P. & F.W. Allendorf. 1995. When are peripheral populations valuable for conservation? Conservation Biol. 9: 753–760. Sagarin, R. & S. Gaines. 2002. The ‘abundant centre’ distribution: to what extent is it a biogeographic rule? Ecol. Lett. 5: 137–147. Eckert, C.G., K.E. Samis & S.C. Lougheed. 2008. Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol. Ecol. 17: 1170–1188. Caughley, G., D. Grice, R. Barker & B. Brown. 1988. The edge of the range. J. Anim. Ecol. 57: 771–785. Hanski, I. & C.D. Thomas. 1994. Metapopulation dynamics and conservation biology: a spatially explicit model applied to butterflies. Biol. Conserv. 68: 67–80. Keitt, T.H., M.A. Lewis & R.D. Holt. 2001. Allee effects, invasion pinning, and species borders. Am. Nat. 157: 203–216. Mix, C., F.X. Pico, J.M. van Groenendael & N.J. Ouborg. 2006. Inbreeding and soil conditions affect dispersal and components of performance of two plant species in fragmented landscapes. Basic Appl. Ecol. 7: 59–69. ` F.X., N.J. Ouborg & J.M. van Groenendael. 2003. Pico, Fitness traits and dispersal ability in the herb Tragopogon pratensis (Asteraceae): decoupling the role of inbreeding depression and maternal effects. Plant Biol. 5: 522–530. Ouborg, N.J., F. Angeloni & P. Vergeer. 2010. An essay on the necessity and feasibility of conservation genomics. Conservation Genet. In press. Roelofs, D., M.G.M. Aarts, H. Schat & N.M. Van Straalen. 2008. Functional ecological genomics to demonstrate general and specific responses to abiotic stress. Funct. Ecol. 22: 8–18.
c 2010 New York Academy of Sciences. Ann. N.Y. Acad. Sci. 1195 (2010) 84–98
