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Invasive plant species are locally adapted just as frequently and at least as strongly as native plant species
Ayub M. O. Oduor,Roosa Leimu,Mark van Kleunen
Summary Concerns over the ecological impacts of invasive alien plant species have generated great research interest in understanding the mechanisms that underlie the capacity of such plants to occupy a broad range of habitats. It has been repeatedly suggested that rapid evolution of local adaptation to novel environments may enable invasive plants to occupy a broad range of habitats. However, the classical Darwinian view on evolution by natural selection is that the process is slow and gradual, occurring over thousands of years. Invasive plants typically have a relatively short residence time in their introduced ranges (decades or just a few centuries). Besides the time constraint, founder effects (reduction in population size and genetic diversity) may also limit the capacity of invasive plants to rapidly evolve local adaption. Thus, invasive plants may be less likely than native plants to evolve local adaptation. Interestingly, however, an expanding body of literature documents the existence of local adaptation in invasive plant species within their exotic ranges. Here, we did a phylogenetically controlled meta-analysis to compare invasive and native plant species for differences in the frequency and magnitude of local adaptation. The meta-analysis was based on different experiments performed in various habitats including grasslands, steppes, deserts, forests, mountains, wetlands and dunes, and used a total of 134 plant species in 52 families. Forty seven of these species (in 24 families) are alien invaders in the region where the studies were undertaken, while the other 91 species (in 38 families) are native. On average, local plants performed better than foreign plants, and invasive plant species expressed local adaptation just as frequently, and at least as strongly as that exhibited by native plant species. An analysis performed while taking into account different plant life-history traits showed that self-incompatible invasive plants exhibited significantly higher frequencies of local adaptation than native plants characterized by the same breeding system. Synthesis. The present results support the suggestion that rapid evolution of local adaptation may enable invasive plant species to occupy a broad range of novel habitats.
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Cited 185 times
Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America
Invasive species offer excellent model systems for studying rapid evolutionary change. In this context, molecular markers play an important role because they provide information about pathways of introduction, the amount of genetic variation introduced, and the extent to which founder effects and inbreeding after population bottlenecks may have contributed to evolutionary change. Here, we studied microsatellite variation in eight polymorphic loci among and within 27 native and 26 introduced populations of garlic mustard (Alliaria petiolata), a European herb which is a current serious invader in North American deciduous forests. Overall, introduced populations were genetically less diverse. However, considerable variability was present and when compared to the probable source regions, no bottleneck was evident. Observed heterozygosity was very low and resulted in high inbreeding coefficients, which did not differ significantly between native and introduced populations. Thus, selfing seems to be equally dominant in both ranges. Consequently, there was strong population differentiation in the native (F(ST) = 0.704) and the introduced (F(ST) = 0.789) ranges. The high allelic diversity in the introduced range strongly suggests multiple introductions of Alliaria petiolata to North America. Out of six European regions, the British Isles, northern Europe, and central Europe had significantly higher proportions of alleles, which are common to the introduced range, and are therefore the most probable source regions. The genetic diversity established by multiple introductions, and the lack of inbreeding depression in this highly selfing species, may have contributed to the invasion success of Alliaria petiolata.
Cited 724 times
Adaptive population divergence: markers, QTL and traits
Abstract Molecular markers appear to be poor indicators of heritable variation in adaptive traits. Direct comparison of population structure in markers with that in traits is made possible by the measure Q st , which partitions quantitative genetic variation in a manner analogous to F st for single gene markers. A survey of the literature reveals that mean Q st is typically larger than and poorly correlated with mean F st across 29 species. Within species, Q st varies widely among traits; traits experiencing the strongest local selection pressures are expected to be the most divergent from molecular F st . Thus, Q st will be particularly relevant to conservation efforts where preserving extant adaptation to local environments is an important goal. Recent theoretical and simulation studies suggest however that F st is a better predictor of the pattern of allelic differentiation at quantitative trait loci (QTLs) than is Q st in random mating populations, in which case allelic variation at QTLs might be better assessed by molecular markers than will extant variation in the traits themselves.
¤ Open Access
Cited 2,787 times
Conceptual issues in local adaptation
Studies of local adaptation provide important insights into the power of natural selection relative to gene flow and other evolutionary forces. They are a paradigm for testing evolutionary hypotheses about traits favoured by particular environmental factors. This paper is an attempt to summarize the conceptual framework for local adaptation studies. We first review theoretical work relevant for local adaptation. Then we discuss reciprocal transplant and common garden experiments designed to detect local adaptation in the pattern of deme · habitat interaction for fitness. Finally, we review research questions and approaches to studying the processes of local adaptation ‐ divergent natural selection, dispersal and gene flow, and other processes affecting adaptive differentiation of local demes. We advocate multifaceted approaches to the study of local adaptation, and stress the need for experiments explicitly addressing hypotheses about the role of particular ecological and genetic factors that promote or hinder local adaptation. Experimental evolution of replicated populations in controlled spatially heterogeneous environments allow direct tests of such hypotheses, and thus would be a valuable way to complement research on natural populations.
¤ Open Access
Cited 188 times
Brassicaceae phylogeny inferred from phytochrome A and <i>ndhF</i> sequence data: tribes and trichomes revisited
The family Brassicaceae comprises 3710 species in 338 genera, 25 recently delimited tribes, and three major lineages based on phylogenetic results from the chloroplast gene ndhF. To assess the credibility of the lineages and newly delimited tribes, we sequenced an approximately 1.8-kb region of the nuclear phytochrome A (PHYA) gene for taxa previously sampled for the chloroplast gene ndhF. Using parsimony, likelihood, and Bayesian methods, we reconstructed the phylogeny of the gene and used the approximately unbiased (AU) test to compare phylogenetic results from PHYA with findings from ndhF. We also combined ndhF and PHYA data and used a Bayesian mixed model approach to infer phylogeny. PHYA and combined analyses recovered the same three large lineages as those recovered in ndhF trees, increasing confidence in these lineages. The combined tree confirms the monophyly of most of the recently delimited tribes (only Alysseae, Anchonieae, and Descurainieae are not monophyletic), while 13 of the 23 sampled tribes are monophyletic in PHYA trees. In addition to phylogenetic results, we documented the trichome branching morphology of species across the phylogeny and explored the evolution of different trichome morphologies using the AU test. Our results indicate that dendritic, medifixed, and stellate trichomes likely evolved independently several times in the Brassicaceae.
¤ Open Access
Cited 1,305 times
A meta-analysis of trait differences between invasive and non-invasive plant species
A major aim in ecology is identifying determinants of invasiveness. We performed a meta-analysis of 117 field or experimental-garden studies that measured pair-wise trait differences of a total of 125 invasive and 196 non-invasive plant species in the invasive range of the invasive species. We tested whether invasiveness is associated with performance-related traits (physiology, leaf-area allocation, shoot allocation, growth rate, size and fitness), and whether such associations depend on type of study and on biogeographical or biological factors. Overall, invasive species had significantly higher values than non-invasive species for all six trait categories. More trait differences were significant for invasive vs. native comparisons than for invasive vs. non-invasive alien comparisons. Moreover, for comparisons between invasive species and native species that themselves are invasive elsewhere, no trait differences were significant. Differences in physiology and growth rate were larger in tropical regions than in temperate regions. Trait differences did not depend on whether the invasive alien species originates from Europe, nor did they depend on the test environment. We conclude that invasive alien species had higher values for those traits related to performance than non-invasive species. This suggests that it might become possible to predict future plant invasions from species traits.
Cited 210 times
A Meta‐Analysis of Factors Affecting Local Adaptation between Interacting Species
Adaptive divergence among populations can result in local adaptation, whereby genotypes in native environments exhibit greater fitness than genotypes in novel environments. A body of theory has developed that predicts how different species traits, such as rates of gene flow and generation times, influence local adaptation in coevolutionary species interactions. We used a meta-analysis of local-adaptation studies across a broad range of host-parasite interactions to evaluate predictions about the effect of species traits on local adaptation. We also evaluated how experimental design influences the outcome of local adaptation experiments. In reciprocally designed experiments, the relative gene flow rate of hosts versus parasites was the strongest predictor of local adaptation, with significant parasite local adaptation only in the studies in which parasites had greater gene flow rates than their hosts. When nonreciprocal studies were included in analyses, species traits did not explain significant variation in local adaptation, although the overall level of local adaptation observed was lower in the nonreciprocal than in the reciprocal studies. This formal meta-analysis across a diversity of host-parasite systems lends insight into the role of both biology (species traits) and biologists (experimental design) in detecting local adaptation in coevolving species interactions.
Cited 150 times
Invasive plants do not display greater phenotypic plasticity than their native or non-invasive counterparts: a meta-analysis
Phenotypic plasticity is commonly considered as a trait associated with invasiveness in alien plants because it may enhance the ability of plants to occupy a wide range of environments. Although the evidence of greater phenotypic plasticity in invasive plants is considerable, it is not yet conclusive. We used a meta-analysis approach to evaluate whether invasive plant species show greater phenotypic plasticity than their native or non-invasive counterparts. Th e outcome of such interspecifi c comparisons may be biased when phylogenetic relatedness is not taken into account. Consequently, species pairs belonged to the same genus, tribe or family. Th e meta-analysis included 93 records from 35 studies reporting plastic responses to light, nutrients, water, CO 2 , herbivory and support availability. Contrary to what is often assumed, overall, phenotypic plasticity was similar between invasive plants and native or non-invasive closely related species. Th e same result was found when separate analyses were conducted for trait plasticity to nutrients, light and water availability. Th us, invasive plant species and their native or non-invasive counterparts are equally capable of displaying functional responses to environmental heterogeneity. Th e colonization of a wide range of environments by invasive plants could be due to their capacity to undergo adaptive ecotypic diff erentiation rather than to their ability to display plastic responses. Alternatively, phenotypic plasticity might play a role in plant invasion, but only during the initial phases, when tolerance of the novel environment is essential for plant survival. Afterwards, once alien plants are identifi ed as invaders, the magnitude of phenotypic plasticity might be reduced after selection of the optimum phenotypes in each habitat. Th e identifi cation of plant traits that consistently predict invasiveness might be a futile task because diff erent traits favor invasiveness in diff erent environments. Approaches at the local scale, focusing on the ecology of specifi c invasive plants, could be more fruitful than global macro-analyses.
Cited 1,266 times
MATERNAL EFFECTS IN PLANTS
Maternal effects in plants were recognized as long ago as 1909 (32). Recent evidence, primarily over the last 15-20 years, shows that maternal effects can contribute substantially to the phenotype of an individual, and as we show, this has important consequences for the interpretation and' design of both ecofogical and genetic studies. Following a discussion of the consequences of maternal effects and an analysis of the different ways these effects can be estimated, we review the evidence for maternal effects from the fields of physiological ecology, crop science, and quantitative genetics. We do not review all of the literature because that would be a monumental task; rather, we focus on representative studies from each of these fields. It is our contention that despite evidence that maternal effects can have a large in fluence on offspring phenotype, few detailed studies have identified the specific causes of maternal effects, particularly in natural populations.
Cited 673 times
Paradox lost: genetic diversity and the success of aquatic invasions
There is mounting evidence that reduced genetic diversity in invasive populations is not as commonplace as expected. Recent studies indicate that high propagule vectors, such as ballast water and shellfish transplantations, and multiple introductions contribute to the elimination of founder effects in the majority of successful aquatic invasions. Multiple introductions, in particular, can promote range expansion of introduced populations through both genetic and demographic mechanisms. Closely related to vectors and corridors of introduction, propagule pressure can play an important role in determining the genetic outcome of introduction events. Even low-diversity introductions have numerous means of avoiding the negative impact of diversity loss. The interaction of high propagule vectors and multiple introductions reveal important patterns associated with invasion success and deserve closer scrutiny.
Cited 153 times
Multispecies comparison reveals that invasive and native plants differ in their traits but not in their plasticity
Summary 1. Plastic responses to spatiotemporal environmental variation strongly influence species distribution, with widespread species expected to have high phenotypic plasticity. Theoretically, high phenotypic plasticity has been linked to plant invasiveness because it facilitates colonization and rapid spreading over large and environmentally heterogeneous new areas. 2. To determine the importance of phenotypic plasticity for plant invasiveness, we compare well-known exotic invasive species with widespread native congeners. First, we characterized the phenotype of 20 invasive–native ecologically and phylogenetically related pairs from the Mediterranean region by measuring 20 different traits involved in resource acquisition, plant competition ability and stress tolerance. Second, we estimated their plasticity across nutrient and light gradients. 3. On average, invasive species had greater capacity for carbon gain and enhanced performance over a range of limiting to saturating resource availabilities than natives. However, both groups responded to environmental variations with high albeit similar levels of trait plasticity. Therefore, contrary to the theory, the extent of phenotypic plasticity was not significantly higher for invasive plants. 4. We argue that the combination of studying mean values of a trait with its plasticity can render insightful conclusions on functional comparisons of species such as those exploring the performance of species coexisting in heterogeneous and changing environments.
Cited 905 times
A Quantitative Survey of Local Adaptation and Fitness Trade‐Offs
The long history of reciprocal transplant studies testing the hypothesis of local adaptation has shown that populations are often adapted to their local environments. Yet many studies have not demonstrated local adaptation, suggesting that sometimes native populations are no better adapted than are genotypes from foreign environments. Local adaptation may also lead to trade‐offs, in which adaptation to one environment comes at a cost of adaptation to another environment. I conducted a survey of published studies of local adaptation to quantify its frequency and magnitude and the costs associated with local adaptation. I also quantified the relationship between local adaptation and environmental differences and the relationship between local adaptation and phenotypic divergence. The overall frequency of local adaptation was 0.71, and the magnitude of the native population advantage in relative fitness was 45%. Divergence between home site environments was positively associated with the magnitude of local adaptation, but phenotypic divergence was not. I found a small negative correlation between a population’s relative fitness in its native environment and its fitness in a foreign environment, indicating weak trade‐offs associated with local adaptation. These results suggest that populations are often locally adapted but stochastic processes such as genetic drift may limit the efficacy of divergent selection.
Cited 1,127 times
EVOLUTIONARY SIGNIFICANCE OF LOCAL GENETIC DIFFERENTIATION IN PLANTS
▪ Abstract The study of natural plant populations has provided some of the strongest and most convincing cases of the operation of natural selection currently known, partly because of amenability to reciprocal transplant experiments, common garden work, and long-term in situ manipulation. Genetic differentiation among plant populations over small scales (a few cm to a few hundred cm) has been documented and is reviewed here, in herbaceous annuals and perennials, woody perennials, aquatics, terrestrials, narrow endemics, and widely distributed species. Character differentiation has been documented for most important features of plant structure and function. Examples are known for seed characters, leaf traits, phenology, physiological and biochemical activities, heavy metal tolerance, herbicide resistance, parasite resistance, competitive ability, organellar characters, breeding systems, and life history. Among the forces that have shaped these patterns of differentiation are toxic soils, fertilizers, mowing and grazing, soil moisture, temperature, light intensity, pollinating vectors, parasitism, gene flow, and natural dynamics. The breadth and depth of the evidence reviewed here strongly support the idea that natural selection is the principal force shaping genetic architecture in natural plant populations; that view needs to be more widely appreciated than it is at present.
Cited 267 times
Plant reproductive systems and evolution during biological invasion
Recent biological invasions provide opportunities to investigate microevolution during contemporary timescales. The tempo and scope of local adaptation will be determined by the intensity of natural selection and the amounts and kinds of genetic variation within populations. In flowering plants, genetic diversity is strongly affected by interactions between reproductive systems and stochastic forces associated with immigration history and range expansion. Here, we explore the significance of reproductive system diversity for contemporary evolution during plant invasion. We focus in particular on how reproductive modes influence the genetic consequences of long-distance colonization and determine the likelihood of adaptive responses during invasion. In many clonal invaders, strong founder effects and restrictions on sexual reproduction limit opportunities for local adaptation. In contrast, adaptive changes to life-history traits should be a general expectation in both outbreeding and inbreeding species. We provide evidence that evolutionary modifications to reproductive systems promote the colonizing ability of invading populations and that reproductive timing is an important target of selection during range expansion. Knowledge of the likelihood and speed at which local adaptation evolves in invasive plants will be particularly important for management practices when evolutionary changes enhance ecological opportunities and invasive spread.
Cited 374 times
High genetic diversity in French invasive populations of common ragweed, Ambrosia artemisiifolia, as a result of multiple sources of introduction
Ambrosia artemisiifolia is an aggressive North American annual weed, found particularly in sunflower and corn fields. Besides its economic impact on crop yield, it represents a major health problem because of its strongly allergenic pollen. Ragweed was imported inadvertently to Europe in the 18th century and has become invasive in several countries, notably in the Rhône Valley of France. It has recently expanded in both the Provence-Alpes-Côte-d'Azur and Bourgogne regions. As first steps towards understanding the causes and mechanisms of ragweed invasion, genetic variability of French and North American populations was analysed using microsatellites. Overall genetic variability was similar in North America and in the Rhône-Alpes region, but within-population levels of genetic variability were surprisingly lower in native than in invasive French populations. French populations also exhibited lower among-population differentiation. A significant pattern of isolation by distance was detected among North American populations but not among French populations. Assignment tests and distribution of rare alleles did not point to a single origin for all French populations, nor for all individuals within populations and private alleles from different North American populations were found in the same French populations. Indeed, within all French populations, individual plants were roughly equally assigned to the different North American populations. Altogether, these results suggest that the French invasive populations include plants from a mixture of sources. Reduced diversity in populations distant from the original area of introduction indicated that ragweed range expansion probably occurred through sequential bottlenecks from the original populations, and not from subsequent new introductions.
¤ Open Access
Cited 67 times
PHENOTYPIC PLASTICITY OF NATIVE VS. INVASIVE PURPLE LOOSESTRIFE: A TWO-STATE MULTIVARIATE APPROACH
The differences in phenotypic plasticity between invasive (North American) and native (German) provenances of the invasive plant Lythrum salicaria (purple loosestrife) were examined using a multivariate reaction norm approach testing two important attributes of reaction norms described by multivariate vectors of phenotypic change: the magnitude and direction of mean trait differences between environments. Data were collected for six life history traits from native and invasive plants using a split-plot design with experimentally manipulated water and nutrient levels. We found significant differences between native and invasive plants in multivariate phenotypic plasticity for comparisons between low and high water treatments within low nutrient levels, between low and high nutrient levels within high water treatments, and for comparisons that included both a water and nutrient level change. The significant genotype x environment (G x E) effects support the argument that invasiveness of purple loosestrife is closely associated with the interaction of high levels of soil nutrient and flooding water regime. Our results indicate that native and invasive plants take different strategies for growth and reproduction; native plants flowered earlier and allocated more to flower production, while invasive plants exhibited an extended period of vegetative growth before flowering to increase height and allocation to clonal reproduction, which may contribute to increased fitness and invasiveness in subsequent years.
¤ Open Access
Cited 1,003 times
Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions
Invasion biologists often suggest that phenotypic plasticity plays an important role in successful plant invasions. Assuming that plasticity enhances ecological niche breadth and therefore confers a fitness advantage, recent studies have posed two main hypotheses: (1) invasive species are more plastic than non-invasive or native ones; (2) populations in the introduced range of an invasive species have evolved greater plasticity than populations in the native range. These two hypotheses largely reflect the disparate interests of ecologists and evolutionary biologists. Because these sciences are typically interested in different temporal and spatial scales, we describe what is required to assess phenotypic plasticity at different levels. We explore the inevitable tradeoffs of experiments conducted at the genotype vs. species level, outline components of experimental design required to identify plasticity at different levels, and review some examples from the recent literature. Moreover, we suggest that a successful invader may benefit from plasticity as either (1) a Jack-of-all-trades, better able to maintain fitness in unfavourable environments; (2) a Master-of-some, better able to increase fitness in favourable environments; or (3) a Jack-and-master that combines some level of both abilities. This new framework can be applied when testing both ecological or evolutionary oriented hypotheses, and therefore promises to bridge the gap between the two perspectives.
“Invasive plant species are locally adapted just as frequently and at least as strongly as native plant species” is a paper by Ayub M. O. Oduor Roosa Leimu Mark van Kleunen published in the journal Journal of Ecology in 2016. It was published by Wiley. It has an Open Access status of “green”. You can read and download a PDF Full Text of this paper here.