Evolutionary game theory as a framework for studying biological invasions

Although biological invasions pose serious threats to biodiversity, they also provide the opportunity to better understand interactions between the ecological and evolutionary processes structuring populations and communities. However, ecoevolutionary frameworks for studying species invasions are lacking. We propose using game theory and the concept of an evolutionarily stable strategy (ESS) as a conceptual framework for integrating the ecological and evolutionary dynamics of invasions. We suggest that the pathways by which a recipient community may have no ESS provide mechanistic hypotheses for how such communities may be vulnerable to invasion and how invaders can exploit these vulnerabilities. We distinguish among these pathways by formalizing the evolutionary contexts of the invader relative to the recipient community. We model both the ecological and the adaptive dynamics of the interacting species. We show how the ESS concept provides new mechanistic hypotheses for when invasions result in long- or short-term increases in biodiversity, species replacement, and subsequent evolutionary changes.     

All stressed out and nowhere to go: does evolvability limit adaptation in invasive species?

Introduced and invasive species are major threats native species and communities and, quite naturally, most scientists and managers think of them in terms of ecological problems. However, species introductions are also experiments in evolution, both for the alien species and for the community that they colonize. We focus here on the introduced species because these offer opportunities to study the properties that allow a species to succeed in a novel habitat and the constraints that limit range expansion. Moreover, an increasing body of evidence from diverse taxa suggests that the introduced species often undergo rapid and observable evolutionary change in their new habitat. Evolution requires genetic variation, which may be decreased or expanded during an invasion, and an evolutionary mechanism such as genetic drift or natural selection. In this volume, we seek to understand how natural selection produces adaptive evolution during invasions. Key questions include what is the role of biotic and abiotic stress in driving adaptation, and what is the source of genetic variation in introduced populations.     

Evolution in invasive plants: implications for biological control

Evidence is increasing that invasive plants can undergo rapid adaptive evolution during the process of range expansion. Here, we argue that evolutionary change during invasions will also affect plant-antagonist interactions and, thus, will have important implications for biological control programmes targeted at invasive plants. We explore how altered selection in the new range might influence the evolution of plant defence (resistance and tolerance) and life history. The degree to which such evolutionary processes might affect biological control efficacy is largely unexplored. We hope that, by testing the hypotheses that we propose here, a closer link can be established between biological control and evolutionary biology, to the benefit of both disciplines.     

Understanding the establishment success of non-indigenous fishes: lessons from population genetics

During the last 10 years, an increasing number of studies have explored evolutionary aspects of biological invasions. It is becoming increasingly clear that evolutionary processes play an important role during the establishment of non-native species. Genetic drift during the colonization process followed by strong selection imposed through a change in biotic conditions and co-evolutionary disequilibrium set the conditions for rapid evolutionary change in introduced populations. Different hypotheses, which have been proposed to explain how evolutionary and genetic processes, can facilitate invasiveness are explored and their relevance for fish invasions is discussed. Empirical evidence increasingly suggests that admixture after multiple introductions, hybridization between native and non-native species and enemy release can all catalyse the evolution of invasiveness. A number of studies also suggest that genetic bottlenecks might represent less of genetic paradox than previously thought. Much of the theoretical developments and empirical evidence concerning the importance of evolution during biological invasions has been provided from studies on invasive plants. Despite their prominence, fish invasions have received little attention from evolutionary biologists. Recent advances in population genetic analysis such as non-equilibrium methods and genomic techniques such as microarray technology provide suitable tools to address such issues.     

Tree invasions: a comparative test of the dominant hypotheses and functional traits

Trees act as ecosystem engineers and invasions by exotic tree species profoundly impact recipient communities. Recently, research on invasive trees has dramatically increased, enabling the assessment of general trends in tree invasion. Analysing 90 studies dealing with 45 invasive tree species, we conducted a quantitative review and a meta-analysis to estimate the relevance of eight leading hypotheses for explaining tree invasions. We also tested whether species functional traits (growth rate, density/cover, germination, biomass and survival) equally promote tree invasiveness. Overall, our results suggest that several hypotheses, linked to invasibility or invasiveness, are pertinent to explain tree invasions. Furthermore, more than one hypothesis has been supported for a given species, which indicates that multiple factors lead to the success of invasive tree species. In addition, growth rate appears to be the most efficient predictor of invasiveness for invasive trees and could thus be used as a means to identify potential alien tree invasions. We conclude that further investigations are needed to test the consistency of some hypotheses across a broader pool of invasive tree species, whilst experimental studies with the same tree species across a larger range of sites would help to reveal the full suite of factors that affect tree invasions.     

Evolutionary responses to global change: lessons from invasive species

Biologists have recently devoted increasing attention to the role of rapid evolution in species' responses to environmental change. However, it is still unclear what evolutionary responses should be expected, at what rates, and whether evolution will save populations at risk of extinction. The potential of biological invasions to provide useful insights has barely been realised, despite the close analogies to species responding to global change, particularly climate change; in both cases, populations encounter novel climatic and biotic selection pressures, with expected evolutionary responses occurring over similar timescales. However, the analogy is not perfect, and invasive species are perhaps best used as an upper bound on expected change. In this article, we review what invasive species can and cannot teach us about likely evolutionary responses to global change and the constraints on those responses. We also discuss the limitations of invasive species as a model and outline directions for future research.     

Linking climate change and species invasion: an illustration using insect herbivores

Climate change and invasive species are two of the most important ecological issues facing the world today. Yet, to date these two factors have largely been viewed independently. In order to prevent large-scale economic and environmental damage and as a first step towards predicting and preventing invasions, it is important to understand the factors affecting invasions. Here, we focus on insect herbivores and link the climate change and invasive research fields. We illustrate using existing published research that life history traits can be useful indicators of future invasive potential. However, climate change will also affect propagule pressure and the communities into which invaders will arrive. With the aid of a meta-analysis we show that climate-induced community changes are likely to increase niche-availability in the future, further exacerbating the problem of invasive species. It is timely and important that further research linking these two important ecological threats is undertaken.     

Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems

Although the number of studies on invasive plants and animals has risen exponentially, little is known about invasive microbes, especially non-pathogenic ones. Microbial invasions by viruses, bacteria, fungi and protists occur worldwide but are much harder to detect than invasions by macroorganisms. Invasive microbes have the potential to significantly alter community structure and ecosystem functioning in diverse terrestrial and aquatic ecosystems. Consequently, increased attention is needed on non-pathogenic invasive microbes, both free-living and symbiotic, and their impacts on communities and ecosystems. Major unknowns include the characteristics that make microbes invasive and properties of the resident communities and the environment that facilitate invasions. A comparison of microbial invasions with invasions of macroorganisms should provide valuable insights into general principles that apply to invasions across all domains of life and to taxon-specific invasion patterns. Invasive microbes appear to possess traits thought to be common in many invasive macroorganisms: high growth rate and resource utilization efficiency, and superior competitive abilities. Invading microorganisms are often similar to native species, but with enhanced performance traits, and tend to spread in lower diversity communities. Global change can exacerbate microbial invasions; therefore, they will likely increase in the future.     

The changing nature of plant–microbe interactions during a biological invasion

Invasive plant species can alter belowground microbial communities. Simultaneously, the composition of soil microbial communities and the abundance of key microbes can influence invasive plant success. Such reciprocal effects may cause plant–microbe interactions to change rapidly during the course of biological invasions in ways that either inhibit or promote invasive species growth. Here we use a space-for-time substitution to illustrate how effects of soil microbial communities on the exotic legume Vicia villosa vary across uninvaded sites, recently invaded sites, and sites invaded by V. villosa for over a decade. We find that soil microorganisms from invaded areas increase V. villosa growth compared to sterilized soil or live soils collected from uninvaded sites, likely because mutualistic nitrogen-fixing rhizobia are not abundant in uninvaded areas. Notably, the benefits resulting from inoculation with live soils were higher for soils from recently invaded sites compared to older invasions, potentially indicating that over longer time scales, soil microbial communities change in ways that may reduce the success of exotic species. These findings suggest that short-term changes to soil microbial communities following invasion may facilitate exotic legume growth likely because of increases in the abundance of mutualistic rhizobia, but also indicate that longer term changes to soil microbial communities may reduce the growth benefits belowground microbial communities provide to exotic species. Our results highlight the changing nature of plant–microbe interactions during biological invasions and illustrate how altered biotic interactions could contribute to both the initial success and subsequent naturalization of invasive legume species.     

Molecular genetic approaches to elucidate the ecological and evolutionary issues associated with biological invasions

Biological invasions may cause serious damage to the native environments and threaten the native biodiversity. Molecular genetic approaches have been found to be powerful tools for investigating the ecological and evolutionary aspects of biological invasions because the genetic structure and level of genetic variation of an invasive species are changed following its invasion. The present article reviews the use of molecular markers in addressing various aspects of invasive species. The application of these techniques has shown that many invasive species are actually "cryptic" species – species whose uniqueness is only recognizable at the genetic level. An estimation of the actual number of invasive species is essential when evaluating its ecological and economic impacts. Molecular genetic approaches have also enabled the source populations of invasive species to be identified. Reconstructions of invasion histories are crucial to preventing future invasions and conserving the native biodiversity, while comparisons of genetic variations between the native and introduced populations provide valuable opportunities to elucidate the mechanisms of rapid adaptation demonstrated by many invasive species.     

Understanding the long-term effects of species invasions

We describe here the ecological and evolutionary processes that modulate the effects of invasive species over time, and argue that such processes are so widespread and important that ecologists should adopt a long-term perspective on the effects of invasive species. These processes (including evolution, shifts in species composition, accumulation of materials and interactions with abiotic variables) can increase, decrease, or qualitatively change the impacts of an invader through time. However, most studies of the effects of invasive species have been brief and lack a temporal context; 40% of recent studies did not even state the amount of time that had passed since the invasion. Ecologists need theory and empirical data to enable prediction, understanding and management of the acute and chronic effects of species invasions.     

Post-invasion evolution of native plant populations: a test of biological resilience

Contemporary evolution may explain the success of some exotic plant invasions. However, the evolutionary response of recipient native plant populations to exotic invasion has received relatively little attention. Because plant populations are genetically variable, contemporary evolution may also occur in native populations following entry of invasive species. Previously, we documented molecular differences in native populations; here we extend these studies to evaluate growth of native species in a common garden experiment. We seek to determine if three populations of two native grass species ( Hesperostipa comata and Sporobolus airoides ) demonstrate evidence of contemporary evolution in response to invasion by Acroptilon repens . We obtained 50 genets of the two native grass species from communities long-invaded (25–80 years) by A. repens and from adjacent, noninvaded areas, and planted five transplants of each genet into two A. repens infestations (Laramie and Fort Steele, Wyoming, USA) to document their growth and survival. Cumulative differences between collections from invaded and noninvaded communities were species-specific. S. airoides displayed a consistent positive response to long-term coexistence with A. repens , whereas the performance of H. comata originating from invaded communities was not different from H. comata collected from noninvaded communities. In general, genets from invaded communities had fewer tillers than genets from noninvaded communities, but their relative tiller production (percent increase) was greater for genets from invaded communities at both field transplant sites for both grass species. Basal area increase and overall performance of collections from invaded and noninvaded communities of origin depended on transplant site and grass species. The results suggest that native species have the potential for adaptation to coexist with exotic invasives, although that potential may differ among species.     

A functional trait perspective on plant invasion

Background and Aims

Global environmental change will affect non-native plant invasions, with profound potential impacts on native plant populations, communities and ecosystems. In this context, we review plant functional traits, particularly those that drive invader abundance (invasiveness) and impacts, as well as the integration of these traits across multiple ecological scales, and as a basis for restoration and management.

Scope

We review the concepts and terminology surrounding functional traits and how functional traits influence processes at the individual level. We explore how phenotypic plasticity may lead to rapid evolution of novel traits facilitating invasiveness in changing environments and then ‘scale up’ to evaluate the relative importance of demographic traits and their links to invasion rates. We then suggest a functional trait framework for assessing per capita effects and, ultimately, impacts of invasive plants on plant communities and ecosystems. Lastly, we focus on the role of functional trait-based approaches in invasive species management and restoration in the context of rapid, global environmental change.

Conclusions

To understand how the abundance and impacts of invasive plants will respond to rapid environmental changes it is essential to link trait-based responses of invaders to changes in community and ecosystem properties. To do so requires a comprehensive effort that considers dynamic environmental controls and a targeted approach to understand key functional traits driving both invader abundance and impacts. If we are to predict future invasions, manage those at hand and use restoration technology to mitigate invasive species impacts, future research must focus on functional traits that promote invasiveness and invader impacts under changing conditions, and integrate major factors driving invasions from individual to ecosystem levels.     

Ramesh Gulati: a personal approach,based on his retirement lecture

Historical and modern migrations and dispersal of most marine organisms (intertidal, benthic, meiofaunal, planktonic, nektonic, or neustonic) are classically interpreted in terms of their natural dispersal potential. Exceptions are introduced species, largely recognized since the 19th century, known to have been transported by human activities. However, humans were transporting species along coastlines and across oceans for millennia and centuries prior to the advent of the first biological surveys. Thus, the presumptive natural distributions of many species may be questioned. Reviewed here are some basic concepts about invasions of non-native species. Human activities move species isolated in time and space from other oceans or continents, and thus human-mediated transport does not simply speed up natural dispersal processes. Both past and modern-day invasions are often overlooked, leading to an underestimation of the scale of invasion diversity and impact. Because vectors, donor regions, and recipient regions change over time, invasions will continue along long-standing but un-managed corridors. The impact of most invasions has never been studied and, therefore, it is not possible to conclude that most invasions have no impact, nor is it generally possible to say that invasions have become `integrated' into a community or ecosystem in ecological time. Finally, invasions in the ocean are not limited to harbours and ports, but are found in a wide variety of marine habitats, ranging from the open ocean continental shelf to exposed rocky shores. The existence of human-mediated vectors has created extraordinary challenges to our understanding and interpretation of the ecology, biogeography, evolutionary biology, and conservation biology of marine communities.     

What invasive species reveal about the rate and form of contemporary phenotypic change in nature

Biological invasions are opportunities to gain insight into fundamental evolutionary questions, because reproductive isolation and sudden alterations in selection pressures are likely to lead to rapid evolutionary change. Here I investigate the role played by invasive species in revealing the rate and form of contemporary phenotypic change in wild populations by expanding a database of more than 5,500 rates of phenotypic change from 90 species of plants and animals. Invasive species are frequently used as model organisms and thus contribute disproportionately to available rates of phenotypic change. However, the preponderance of these rates is the consequence of extensive study in a small number of species. I found mixed evidence to support the hypothesis that phenotypic change is associated with time depending on the metric of choice (i.e., darwins or haldanes). Insights from both invasive and native species provide evidence for abrupt phenotypic change and suggest that the environment plays a potentially important role in driving trait change in wild populations, although the environmental influence on the observed trajectories remains unclear. Thus, future work should continue to seek an understanding of the mechanistic underpinnings--both genetic and environmental--of how phenotypic variation allows populations to adapt to rapidly changing global environments.     

<Emphasis Type="Italic">Phragmites</Emphasis><Emphasis Type="Italic">australis</Emphasis> as a model organism for studying plant invasions

The cosmopolitan reed grass Phragmites australis (Poaceae) is an intensively studied species globally with a substantial focus in the last two decades on its invasive populations. Here we argue that P. australis meets the criteria to serve as a model organism for studying plant invasions. First, as a dominant species in globally important wetland habitats, it has generated significant pre-existing research, demonstrating a high potential for funding. Second, this plant is easy to grow and use in experiments. Third, it grows abundantly in a wide range of ecological systems and plant communities, allowing a broad range of research questions to be addressed. We formalize the designation of P. australis as a model organism for plant invasions in order to encourage and standardize collaborative research on multiple spatial scales that will help to integrate studies on the ecology and evolution of P. australis invasive populations, their response to global environmental change, and implications for biological security. Such an integrative framework can serve as guidance for studying invasive plant species at the population level and global spatial scale.     

Eco‐evolutionary partitioning metrics: assessing the importance of ecological and evolutionary contributions to population and community change

Interest in eco‐evolutionary dynamics is rapidly increasing thanks to ground‐breaking research indicating that evolution can occur rapidly and can alter the outcome of ecological processes. A key challenge in this sub‐discipline is establishing how important the contribution of evolutionary and ecological processes and their interactions are to observed shifts in population and community characteristics. Although a variety of metrics to separate and quantify the effects of evolutionary and ecological contributions to observed trait changes have been used, they often allocate fractions of observed changes to ecology and evolution in different ways. We used a mathematical and numerical comparison of two commonly used frameworks – the Price equation and reaction norms – to reveal that the Price equation cannot partition genetic from non‐genetic trait change within lineages, whereas the reaction norm approach cannot partition among‐ from within‐lineage trait change. We developed a new metric that combines the strengths of both Price‐based and reaction norm metrics, extended all metrics to analyse community change and also incorporated extinction and colonisation of species in these metrics. Depending on whether our new metric is applied to populations or communities, it can correctly separate intraspecific, interspecific, evolutionary, non‐evolutionary and interacting eco‐evolutionary contributions to trait change.     

Global ecological impacts of invasive species in aquatic ecosystems

The introduction of invasive species, which often differ functionally from the components of the recipient community, generates ecological impacts that propagate along the food web. This review aims to determine how consistent the impacts of aquatic invasions are across taxa and habitats. To that end, we present a global meta‐analysis from 151 publications (733 cases), covering a wide range of invaders (primary producers, filter collectors, omnivores and predators), resident aquatic community components (macrophytes, phytoplankton, zooplankton, benthic invertebrates and fish) and habitats (rivers, lakes and estuaries). Our synthesis suggests a strong negative influence of invasive species on the abundance of aquatic communities, particularly macrophytes, zooplankton and fish. In contrast, there was no general evidence for a decrease in species diversity in invaded habitats, suggesting a time lag between rapid abundance changes and local extinctions. Invaded habitats showed increased water turbidity, nitrogen and organic matter concentration, which are related to the capacity of invaders to transform habitats and increase eutrophication. The expansion of invasive macrophytes caused the largest decrease in fish abundance, the filtering activity of filter collectors depleted planktonic communities, omnivores (including both facultative and obligate herbivores) were responsible for the greatest decline in macrophyte abundance, and benthic invertebrates were most negatively affected by the introduction of new predators. These impacts were relatively consistent across habitats and experimental approaches. Based on our results, we propose a framework of positive and negative links between invasive species at four trophic positions and the five different components of recipient communities. This framework incorporates both direct biotic interactions (predation, competition, grazing) and indirect changes to the water physicochemical conditions mediated by invaders (habitat alteration). Considering the strong trophic links that characterize aquatic ecosystems, this framework is relevant to anticipate the far‐reaching consequences of biological invasions on the structure and functionality of aquatic ecosystems.     

The evolutionary impacts of conservation actions

Conservation management for environmental sustainability is now ubiquitous. The ecological effects of these actions are well-intentioned and well-known. Although conservation biologists and managers increasingly incorporate evolutionary considerations into management plans, the evolutionary consequences of management strategies have remained relatively unexplored and unconsidered. But what are the evolutionary consequences? Here, we advocate a new research agenda focused on identifying, predicting, and countering the evolutionary consequences of conservation management. We showcase the examples of park creation and invasive species management, and speculate further on five other major methods of management. Park creation may cause selection for altered dispersal and behavior that utilizes human foods and structures. Management of invasive species may favor the evolution of resistance to or tolerance of control methods. In these and other cases, evolution may cause deviations from the predicted consequences of management strategies optimized without considering evolution, particularly when management results in or coincides with major environmental change, if population size change strongly, or if life histories are short enough to allow more rapid evolution. We call for research focused on: (1) experimental predictions and tests of evolution under particular management strategies, (2) widespread monitoring of managed populations and communities, and (3) meta-analysis and theoretical study aimed at simplifying the process of evolutionary prediction, particularly at systematizing a means of identifying traits likely to evolve due to likely existing genetic variance or high mutation rates. Ultimately, conservation biologists should incorporate evolutionary prediction into management planning to prevent the evolutionary domestication of the species that they are trying to protect.