Invasive plants and enemy release: evolution of trait means and trait correlations in Ulex europaeus

Several hypotheses that attempt to explain invasive processes are based on the fact that plants have been introduced without their natural enemies. Among them, the EICA (Evolution of Increased Competitive Ability) hypothesis is the most influential. It states that, due to enemy release, exotic plants evolve a shift in resource allocation from defence to reproduction or growth. In the native range of the invasive species Ulex europaeus, traits involved in reproduction and growth have been shown to be highly variable and genetically correlated. Thus, in order to explore the joint evolution of life history traits and susceptibility to seed predation in this species, we investigated changes in both trait means and trait correlations. To do so, we compared plants from native and invaded regions grown in a common garden. According to the expectations of the EICA hypothesis, we observed an increase in seedling height. However, there was little change in other trait means. By contrast, correlations exhibited a clear pattern: the correlations between life history traits and infestation rate by seed predators were always weaker in the invaded range than in the native range. In U. europaeus, the role of enemy release in shaping life history traits thus appeared to imply trait correlations rather than trait means. In the invaded regions studied, the correlations involving infestation rates and key life history traits such as flowering phenology, growth and pod density were reduced, enabling more independent evolution of these key traits and potentially facilitating local adaptation to a wide range of environments. These results led us to hypothesise that a relaxation of genetic correlations may be implied in the expansion of invasive species.     

MULTIVARIATE ADAPTATION BUT NO INCREASE IN COMPETITIVE ABILITY IN INVASIVE GERANIUM CAROLINIANUM L. (GERANIACEAE)

Adaptive evolution can affect the successful establishment of invasive species, but changes in selective pressures, loss of genetic variation in relevant traits, and/or altered trait correlations can make adaptation difficult to predict. We used a common‐garden experiment to assess trait correlations and patterns of adaptation in the invasive plant, Geranium carolinianum, sampled across 20 populations in its native (United States) and invasive (China) ranges. We used multivariate Q_ST – F_ST tests to determine if phenotypic differences between countries are attributable to adaptation. We also compared population‐level variation within each country to assess whether local adaptation resulted in similar multivariate phenotypes in the United States and China. Between countries, most phenotypic differences are indistinguishable from genetic drift, although we detected a signature of adaptation to the colder, drier winters in China. There was no evidence for increases in invasive traits in China. Within countries, strong multivariate adaptation appears to be driven by latitudinal climatic variation in the United States, but not in China. Additionally, adaptive trait combinations as well as their underlying correlations differ between the two countries, indicating that adaptation in invasive populations does not parallel patterns in native populations due to differences in selection pressures, genetic constraints, or both.     

For or against: the importance of variation in growth rate for testing the EICA hypothesis

The evolution of increased competitive ability (EICA) hypothesis proposes that invasive species evolve decreased defense and increased competitive ability following natural enemy release. Previous studies have found evidence both for and against EICA. The resource-enemy release hypothesis (R-ERH) suggests that fast-growing species may experience stronger enemy release than slow-growing species. On the basis of R-ERH, the prediction of EICA will be held true for slow-growing genotypes, i.e., the slow-growing genotypes from the introduced range will be less resistant to herbivory and grow faster than those from the home range; while the EICA will not be held for fast-growing genotypes, i.e., there will be no significant differences in growth and defense traits between the introduced and native fast-growing genotypes. We tested these predictions preliminarily using five populations of the invasive plant Alternanthera philoxeroides. This species has two varieties in its home range, which showed a distinct growth-defense strategy: the northern A. p. var. acutifolia (Apa) had higher growth rate but lower resistance, while the southern A. p. var. obtusifolia (Apo) had lower growth rate but higher resistance level. Our results suggest that the EICA hypothesis is consistent with the slow-growing Apo, but not with the fast-growing Apa. We suggest that evolutionary changes in growth or resistance following enemy release are influenced by variation in growth rate within an invasive alien plant. These findings have important implications for the EICA hypothesis, and may partially explain why previous studies have found evidence both for and against EICA.     

Decreased indirect defense in the invasive tree, Triadica sebifera

In the absence of coevolved natural enemies, plants are expected to experience selection away from costly herbivore defenses toward growth and reproduction [evolution of increased competitive ability hypothesis (EICA)], yet no one has demonstrated EICA for an indirect defense trait. Likewise, we have little understanding of how constitutive and induced levels of defense vary among native and invasive plant populations. We conducted a greenhouse experiment in the introduced range to test whether invasive populations have reduced constitutive and induced investment in an indirect defense trait, extrafloral nectar (EFN) production, compared to native populations of Chinese tallow tree, Triadica sebifera, through an experimental leaf damage treatment. Overall, native populations invested more in indirect defense: Native populations had a greater number (+16?%) and percentage of leaves producing EFN (35 vs. 28?%), produced more EFN (63?% greater volume), and produced more sugar (+33?%) compared to invasive populations, independent of damage treatment. Of these traits, number of leaves producing EFN and volume of EFN exhibited a trade-off between constitutive and induced investment but these did not depend on plant origin. Our results are the first to support the EICA hypothesis for an indirect defense trait. This suggests that tri-trophic interactions such as indirect defense are under similar selection as direct defense traits within introduced populations. Despite reduced investment in EFN production, invasive populations still retain the ability to produce EFN, which may enable invasive plants to defend against herbivores in the introduced range.     

Plasticity and evolution in correlated suites of traits

When organisms are faced with new or changing environments, a central challenge is the coordination of adaptive shifts in many different phenotypic traits. Relationships among traits may facilitate or constrain evolutionary responses to selection, depending on whether the direction of selection is aligned or opposed to the pattern of trait correlations. Attempts to predict evolutionary potential in correlated traits generally assume that correlations are stable across time and space; however, increasing evidence suggests that this may not be the case, and flexibility in trait correlations could bias evolutionary trajectories. We examined genetic and environmental influences on variation and covariation in a suite of behavioural traits to understand if and how flexibility in trait correlations influences adaptation to novel environments. We tested the role of genetic and environmental influences on behavioural trait correlations by comparing Trinidadian guppies (Poecilia reticulata) historically adapted to high‐ and low‐predation environments that were reared under native and non‐native environmental conditions. Both high‐ and low‐predation fish exhibited increased behavioural variance when reared under non‐native vs. native environmental conditions, and rearing in the non‐native environment shifted the major axis of variation among behaviours. Our findings emphasize that trait correlations observed in one population or environment may not predict correlations in another and that environmentally induced plasticity in correlations may bias evolutionary divergence in novel environments.     

Interactive effects of habitat productivity and herbivore pressure on the evolution of anti-herbivore defense in invasive plant populations

The evolution of increased competitive ability (EICA) hypothesis predicts that plants released from natural enemies should evolve to become more invasive through a shift in resource allocation from defense to growth. Resource availability in the environment is widely regarded as a major determinant of defense investment and invasiveness, and thus should be incorporated into the conceptual framework of EICA. Analysis of a simple model from the optimal defense literature demonstrates that, in contrast to the EICA hypothesis, enemy release is neither sufficient nor necessary for evolution of reduced resistance among introduced plants when habitat productivity co-varies. In particular, if the invasive range is more nutrient-poor than the native range, there could be selection for more plant defenses even with enemy release.     

Comparison of the herbivore defense and competitive ability of ancestral and modern genotypes of an invasive plant,Lespedeza cuneata

The evolution of increased competitive ability (EICA) hypothesis provides a compelling explanation for the success of invasive species. It contends that because alien plants have escaped their coevolved natural enemies, selection pressures favor a diversion of resources from herbivore defense to traits that confer increased competitive ability. Here, we provide evidence for EICA in the noxious grassland invader Lespedeza cuneata, by comparing the ancestral genotype introduced to North America in 1930 with modern‐day invasive (North American) and native (Japanese) genotypes. We found that the invasive genotype was a better competitor than either the native or the ancestral genotype. Further, the invasive genotype exhibited greater induced resistance but lower constitutive resistance than the ancestral and native genotypes. Our results suggest that selection has played a pivotal role in shaping this invasive plant species into a more aggressive, but less constitutively defended competitor.     

DISENTANGLING THE ROLE OF PHENOTYPIC PLASTICITY AND GENETIC DIVERGENCE IN CONTEMPORARY ECOTYPE FORMATION DURING A BIOLOGICAL INVASION

The occurrence of contemporary ecotype formation through adaptive divergence of populations within the range of an invasive species typically requires standing genetic variation but can be facilitated by phenotypic plasticity. The relative contributions of both of these to adaptive trait differentiation have rarely been simultaneously quantified in recently diverging vertebrate populations. Here we study a case of intraspecific divergence into distinct lake and stream ecotypes of threespine stickleback that evolved in the past 140 years within the invasive range in Switzerland. Using a controlled laboratory experiment with full‐sib crosses and treatments mimicking a key feature of ecotypic niche divergence, we test if the phenotypic divergence that we observe in the wild results from phenotypic plasticity or divergent genetic predisposition. Our experimental groups show qualitatively similar phenotypic divergence as those observed among wild adults. The relative contribution of plasticity and divergent genetic predisposition differs among the traits studied, with traits related to the biomechanics of feeding showing a stronger genetic predisposition, whereas traits related to locomotion are mainly plastic. These results implicate that phenotypic plasticity and standing genetic variation interacted during contemporary ecotype formation in this case.     

Phenotypic and genetic differentiation between native and introduced plant populations

Plant invasions often involve rapid evolutionary change. Founder effects, hybridization, and adaptation to novel environments cause genetic differentiation between native and introduced populations and may contribute to the success of invaders. An influential idea in this context has been the Evolution of Increased Competitive Ability (EICA) hypothesis. It proposes that after enemy release plants rapidly evolve to be less defended but more competitive, thereby increasing plant vigour in introduced populations. To detect evolutionary change in invaders, comparative studies of native versus introduced populations are needed. Here, we review the current empirical evidence from: (1) comparisons of phenotypic variation in natural populations; (2) comparisons of molecular variation with neutral genetic markers; (3) comparisons of quantitative genetic variation in a common environment; and (4) comparisons of phenotypic plasticity across different environments. Field data suggest that increased vigour and reduced herbivory are common in introduced plant populations. In molecular studies, the genetic diversity of introduced populations was not consistently different from that of native populations. Multiple introductions of invasive plants appear to be the rule rather than the exception. In tests of the EICA hypothesis in a common environment, several found increased growth or decreased resistance in introduced populations. However, few provided a full test of the EICA hypothesis by addressing growth and defence in the same species. Overall, there is reasonable empirical evidence to suggest that genetic differentiation through rapid evolutionary change is important in plant invasions. We discuss conceptual and methodological issues associated with cross-continental comparisons and make recommendations for future research. When testing for EICA, greater emphasis should be put on competitive ability and plant tolerance. Moreover, it is important to address evolutionary change in characteristics other than defence and growth that could play a role in plant invasions.     

Phylogenetic patterns of trait and trait plasticity evolution: Insights from amphibian embryos

Environmental variation favors the evolution of phenotypic plasticity. For many species, we understand the costs and benefits of different phenotypes, but we lack a broad understanding of how plastic traits evolve across large clades. Using identical experiments conducted across North America, we examined prey responses to predator cues. We quantified five life‐history traits and the magnitude of their plasticity for 23 amphibian species/populations (spanning three families and five genera) when exposed to no cues, crushed‐egg cues, and predatory crayfish cues. Embryonic responses varied considerably among species and phylogenetic signal was common among the traits, whereas phylogenetic signal was rare for trait plasticities. Among trait‐evolution models, the Ornstein–Uhlenbeck (OU) model provided the best fit or was essentially tied with Brownian motion. Using the best fitting model, evolutionary rates for plasticities were higher than traits for three life‐history traits and lower for two. These data suggest that the evolution of life‐history traits in amphibian embryos is more constrained by a species’ position in the phylogeny than is the evolution of life history plasticities. The fact that an OU model of trait evolution was often a good fit to patterns of trait variation may indicate adaptive optima for traits and their plasticities.     

Incomplete loss of a conserved trait: function,latitudinal cline,and genetic constraints

Retention of nonfunctional traits over evolutionary time is puzzling, because the cost of trait production should drive loss. Indeed, several studies have found nonfunctional traits are rapidly eliminated by selection. However, theory suggests that complex genetic interactions and a lack of genetic variance can constrain evolution, including trait loss. In the mustard family Brassicaceae the conserved floral condition includes four long and two short stamens, but we show that short stamens in the highly self‐pollinating mustard Arabidopsis thaliana do not significantly increase selfed seed set, suggesting that the trait has lost most or all of its function after the transition to selfing. We find that short stamen loss is common in native populations. Loss is incomplete and decreases with increasing latitude, a cline unexplained by correlations with flowering time or ovule count (which also vary with latitude). Using recombinant inbred lines derived from a cross between plants at the latitudinal extremes of the native range, we found three QTLs affecting short stamen number, with epistasis among them constraining stamen loss. Constraints on stamen loss from both epistasis and low genetic variance may be augmented by high selfing rates, suggesting that these kinds of constraints may be common in inbred species.     

Changes in Defense of an Alien Plant Ambrosia artemisiifolia before and after the Invasion of a Native Specialist Enemy Ophraella communa

The evolution of increased competitive ability hypothesis (EICA) predicts that when alien plants are free from their natural enemies they evolve lower allocation to defense in order to achieve a higher growth rate. If this hypothesis is true, the converse implication would be that the defense against herbivory could be restored if a natural enemy also becomes present in the introduced range. We tested this scenario in the case of Ambrosia artemisiifolia (common ragweed) – a species that invaded Japan from North America. We collected seeds from five North American populations, three populations in enemy free areas of Japan and four populations in Japan where the specialist herbivore Ophraella communa naturalized recently. Using plants grown in a common garden in Japan, we compared performance of O. communa with a bioassay experiment. Consistent with the EICA hypothesis, invasive Japanese populations of A. artemisiifolia exhibited a weakened defense against the specialist herbivores and higher growth rate than native populations. Conversely, in locations where the herbivore O. communa appeared during the past decade, populations of A. artemisiifolia exhibited stronger defensive capabilities. These results strengthen the case for EICA and suggest that defense levels of alien populations can be recuperated rapidly after the native specialist becomes present in the introduced range. Our study implies that the plant defense is evolutionary labile depending on plant-herbivore interactions.     

Response to enemies in the invasive plant Lythrum salicaria is genetically determined

Background and Aims

The enemy release hypothesis assumes that invasive plants lose their co-evolved natural enemies during introduction into the new range. This study tested, as proposed by the evolution of increased competitive ability (EICA) hypothesis, whether escape from enemies results in a decrease in defence ability in plants from the invaded range. Two straightforward aspects of the EICA are examined: (1) if invasives have lost their enemies and their defence, they should be more negatively affected by their full natural pre-invasion herbivore spectrum than their native conspecifics; and (2) the genetic basis of evolutionary change in response to enemy release in the invasive range has not been taken sufficiently into account.

Methods

Lythrum salicaria (purple loosestrife) from several populations in its native (Europe) and invasive range (North America) was exposed to all above-ground herbivores in replicated natural populations in the native range. The experiment was performed both with plants raised from field-collected seeds as well as with offspring of these where maternal effects were removed.

Key Results

Absolute and relative leaf damage was higher for introduced than for native plants. Despite having smaller height growth rate, invasive plants attained a much larger final size than natives irrespective of damage, indicating large tolerance rather than effective defence. Origin effects on response to herbivory and growth were stronger in second-generation plants, suggesting that invasive potential through enemy release has a genetic basis.

Conclusions

The findings support two predictions of the EICA hypothesis – a genetically determined difference between native and invasive plants in plant vigour and response to enemies – and point to the importance of experiments that control for maternal effects and include the entire spectrum of native range enemies.     

The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus

Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait‐specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high‐throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy‐mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.     

The genetic variance but not the genetic covariance of life‐history traits changes towards the north in a time‐constrained insect

Seasonal time constraints are usually stronger at higher than lower latitudes and can exert strong selection on life‐history traits and the correlations among these traits. To predict the response of life‐history traits to environmental change along a latitudinal gradient, information must be obtained about genetic variance in traits and also genetic correlation between traits, that is the genetic variance‐covariance matrix, G . Here, we estimated G for key life‐history traits in an obligate univoltine damselfly that faces seasonal time constraints. We exposed populations to simulated native temperatures and photoperiods and common garden environmental conditions in a laboratory set‐up. Despite differences in genetic variance in these traits between populations (lower variance at northern latitudes), there was no evidence for latitude‐specific covariance of the life‐history traits. At simulated native conditions, all populations showed strong genetic and phenotypic correlations between traits that shaped growth and development. The variance–covariance matrix changed considerably when populations were exposed to common garden conditions compared with the simulated natural conditions, showing the importance of environmentally induced changes in multivariate genetic structure. Our results highlight the importance of estimating variance–covariance matrixes in environments that mimic selection pressures and not only trait variances or mean trait values in common garden conditions for understanding the trait evolution across populations and environments.     

Meta‐analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA)

Ecological explanations for the success and persistence of invasive species vastly outnumber evolutionary hypotheses, yet evolution is a fundamental process in the success of any species. The Evolution of Increased Competitive Ability (EICA) hypothesis (Blossey and Nötzold 1995) proposes that evolutionary change in response to release from coevolved herbivores is responsible for the success of many invasive plant species. Studies that evaluate this hypothesis have used different approaches to test whether invasive populations allocate fewer resources to defense and more to growth and competitive ability than do source populations, with mixed results. We conducted a meta‐analysis of experimental tests of evolutionary change in the context of EICA. In contrast to previous reviews, there was no support across invasive species for EICA's predictions regarding defense or competitive ability, although invasive populations were more productive than conspecific native populations under noncompetitive conditions. We found broad support for genetically based changes in defense and competitive plant traits after introduction into new ranges, but not in the manner suggested by EICA. This review suggests that evolution occurs as a result of plant introduction and population expansion in invasive plant species, and may contribute to the invasiveness and persistence of some introduced species.     

Selection on herbivory resistance and growth rate in an invasive plant

The evolution of increased competitive ability (EICA) hypothesis proposes that invasive species evolve decreased defense and increased competitive ability following natural enemy release. Previous tests of EICA examined the result of evolution by comparing individuals from home and introduced ranges, but no previous study of this hypothesis has examined the process of evolution by analyzing patterns of selection. On the basis of EICA, there should be selection for competitive ability without herbivores and selection for defense with herbivores. Selection on competitive ability should be stronger for genotypes accustomed to herbivores (home range genotypes), and selection on defense should be stronger for genotypes unaccustomed to herbivores (introduced range genotypes). Using a field experiment, we tested these hypotheses for the invasive plant Melaleuca quinquenervia. There was a negative genetic correlation between resistance and growth, indicating a trade-off. However, selection for stem elongation (an indicator of competitive ability) was always positive, and selection on resistance was always negative and did not depend on genotype source or the presence of herbivores. The patterns of selection found in this study contrast with predictions from EICA and accurately predict the lack of evolutionary change in growth and resistance following the introduction of this species from Australia to Florida.     

飞机草入侵种群与原产地种群生长性状的差异

飞机草(Chromolaena odorata)是我国热带地区危害严重的外来入侵植物,为揭示适应进化对其成功入侵的贡献,在同质种植园中,比较研究了飞机草10个入侵地种群与12个原产地种群生长性状的差异,为排除奠基者效应的可能影响,进一步比较了飞机草10个入侵地种群与其原产地可能的祖先种群间的差异。结果表明,飞机草10个入侵地种群的基茎、株高、分枝数、生物量和比叶面积均显著高于12个原产地种群;与可能的祖先种群相比,飞机草10个入侵种群的生物量、分枝数和比叶面积仍更高。这些结果表明,在长期的入侵过程中飞机草通过进化提高了资源向生长的分配,支持增强竞争能力的进化假说。     

Reduced inflammation in expanding populations of a neotropical bird species

The loss of regulating agents such as parasites is among the most important changes in biotic interactions experienced by populations established in newly colonized areas. Under a relaxed parasite pressure, individuals investing less in costly immune mechanisms might experience a selective advantage and become successful colonizers as they re‐allocate resources to other fitness‐related traits. Accordingly, a refinement of the evolution of increased competitive ability (EICA) hypothesis proposed that immunity of invasive populations has evolved toward a reduced investment in innate immunity, the most costly component of immunity, and an increased humoral immunity that is less costly. Biogeographical approaches comparing populations between native and expansion ranges are particularly relevant in exploring this issue, but remain very scarce. We conducted a biogeographical comparison between populations of Spectacled Thrush (Turdus nudigenis) from the native area (South America) and from the expansion range (Caribbean islands). First, we compared haemosporidian prevalence and circulating haptoglobin (an acute‐phase protein produced during inflammation). Second, we challenged captive birds from both ranges with Escherichia coli lipopolysaccharides (LPS) and measured postchallenge haptoglobin production and body mass change. Birds from the expansion range showed lower haemosporidian prevalence and lower levels of haptoglobin than birds from the native range. In addition, the inflammation elicited by LPS injection and its associated cost in terms of body mass loss were lower in birds from the expansion range than in birds from the native range. In accordance with the enemy release hypothesis, our results suggest that range expansion is associated with a reduced infection risk. Our study also supports the hypothesis that individuals from newly established populations have evolved mechanisms to dampen the inflammatory response and are in accordance with one prediction of the refined EICA hypothesis, proposed to understand biological invasions.     

Footprints in time: comparative quantitative trait loci mapping of the pitcher-plant mosquito,Wyeomyia smithii

Identifying regions of the genome contributing to phenotypic evolution often involves genetic mapping of quantitative traits. The focus then turns to identifying regions of ‘major’ effect, overlooking the observation that traits of ecological or evolutionary relevance usually involve many genes whose individual effects are small but whose cumulative effect is large. Herein, we use the power of fully interfertile natural populations of a single species of mosquito to develop three quantitative trait loci (QTL) maps: one between two post-glacially diverged populations and two between a more ancient and a post-glacial population. All demonstrate that photoperiodic response is genetically a highly complex trait. Furthermore, we show that marker regressions identify apparently ‘non-significant’ regions of the genome not identified by composite interval mapping, that the perception of the genetic basis of adaptive evolution is crucially dependent upon genetic background and that the genetic basis for adaptive evolution of photoperiodic response is highly variable within contemporary populations as well as between anciently diverged populations.