Immigration delays but does not prevent adaptation following environmental change: experimental evidence.

In today's rapidly changing world, it is critical to examine how animal populations will respond to severe environmental change. Following events such as pollution or deforestation that cause populations to decline, extinction will occur unless populations can adapt in response to natural selection, a process called evolutionary rescue. Theory predicts that immigration can delay extinction and provide novel genetic material that can prevent inbreeding depression and facilitate adaptation. However, when potential source populations have not experienced the new environment before (i.e., are naive), immigration can counteract selection and constrain adaptation. This study evaluated the effects of immigration of naive individuals on evolutionary rescue using the red flour beetle, Tribolium castaneum, as a model system. Small populations were exposed to a challenging environment, and 3 immigration rates (0, 1, or 5 migrants per generation) were implemented with migrants from a benign environment. Following an initial decline in population size across all treatments, populations receiving no immigration gained a higher growth rate one generation earlier than those with immigration, illustrating the constraining effects of immigration on adaptation. After 7 generations, a reciprocal transplant experiment found evidence for adaptation regardless of immigration rate. Thus, while the immigration of naive individuals briefly delayed adaptation, it did not increase extinction risk or prevent adaptation following environmental change.

How density dependence, genetic erosion and the extinction vortex impact evolutionary rescue.

Following severe environmental change that reduces mean population fitness below replacement, populations must adapt to avoid eventual extinction, a process called evolutionary rescue. Models of evolutionary rescue demonstrate that initial size, genetic variation and degree of maladaptation influence population fates. However, many models feature populations that grow without negative density dependence or with constant genetic diversity despite precipitous population decline, assumptions likely to be violated in conservation settings. We examined the simultaneous influences of density-dependent growth and erosion of genetic diversity on populations adapting to novel environmental change using stochastic, individual-based simulations. Density dependence decreased the probability of rescue and increased the probability of extinction, especially in large and initially well-adapted populations that previously have been predicted to be at low risk. Increased extinction occurred shortly following environmental change, as populations under density dependence experienced more rapid decline and reached smaller sizes. Populations that experienced evolutionary rescue lost genetic diversity through drift and adaptation, particularly under density dependence. Populations that declined to extinction entered an extinction vortex, where small size increased drift, loss of genetic diversity and the fixation of maladaptive alleles, hindered adaptation and kept populations at small densities where they were vulnerable to extinction via demographic stochasticity.

Phylogenetic risk assessment is robust for forecasting the impact of European insects on North American conifers.

Some introduced species cause severe damage, although the majority have little impact. Robust predictions of which species are most likely to cause substantial impacts could focus efforts to mitigate those impacts or prevent certain invasions entirely. Introduced herbivorous insects can reduce crop yield, fundamentally alter natural and managed forest ecosystems, and are unique among invasive species in that they require certain host plants to succeed. Recent studies have demonstrated that understanding the evolutionary history of introduced herbivores and their host plants can provide robust predictions of impact. Specifically, divergence times between hosts in the native and introduced ranges of a nonnative insect can be used to predict the potential impact of the insect should it establish in a novel ecosystem. However, divergence time estimates vary among published phylogenetic datasets, making it crucial to understand if and how the choice of phylogeny affects prediction of impact. Here, we tested the robustness of impact prediction to variation in host phylogeny by using insects that feed on conifers and predicting the likelihood of high impact using four different published phylogenies. Our analyses ranked 62 insects that are not established in North America and 47 North American conifer species according to overall risk and vulnerability, respectively. We found that results were robust to the choice of phylogeny. Although published vascular plant phylogenies continue to be refined, our analysis indicates that those differences are not substantial enough to alter the predictions of invader impact. Our results can assist in focusing biosecurity programs for conifer pests and can be more generally applied to nonnative insects and their potential hosts by prioritizing surveillance for those insects most likely to be damaging invaders.

Increasing temporal variance leads to stable species range limits.

What prevents populations of a species from adapting to the novel environments outside the species' geographic distribution? Previous models highlighted how gene flow across spatial environmental gradients determines species expansion versus extinction and the location of species range limits. However, space is only one of two axes of environmental variation-environments also vary in time, and we know temporal environmental variation has important consequences for population demography and evolution. We used analytical and individual-based evolutionary models to explore how temporal variation in environmental conditions influences the spread of populations across a spatial environmental gradient. We find that temporal variation greatly alters our predictions for range dynamics compared to temporally static environments. When temporal variance is equal across the landscape, the fate of species (expansion versus extinction) is determined by the interaction between the degree of temporal autocorrelation in environmental fluctuations and the steepness of the spatial environmental gradient. When the magnitude of temporal variance changes across the landscape, stable range limits form where this variance increases maladaptation sufficiently to prevent local persistence. These results illustrate the pivotal influence of temporal variation on the likelihood of populations colonizing novel habitats and the location of species range limits.

Adaptation and correlated fitness responses over two time scales in Drosophila suzukii populations evolving in different environments.

The process of local adaptation involves differential changes in fitness over time across different environments. Although experimental evolution studies have extensively tested for patterns of local adaptation at a single time point, there is relatively little research that examines fitness more than once during the time course of adaptation. We allowed replicate populations of the fruit pest Drosophila suzukii to evolve in one of eight different fruit media. After five generations, populations with the highest initial levels of maladaptation had mostly gone extinct, whereas experimental populations evolving on cherry, strawberry and cranberry media had survived. We measured the fitness of each surviving population in each of the three fruit media after five and after 26 generations of evolution. After five generations, adaptation to each medium was associated with increased fitness in the two other media. This was also true after 26 generations, except when populations that evolved on cranberry medium developed on cherry medium. These results suggest that, in the theoretical framework of a fitness landscape, the fitness optima of cherry and cranberry media are the furthest apart. Our results show that studying how fitness changes across several environments and across multiple generations provides insights into the dynamics of local adaptation that would not be evident if fitness were analysed at a single point in time. By allowing a qualitative mapping of an experimental fitness landscape, our approach will improve our understanding of the ecological factors that drive the evolution of local adaptation in D. suzukii.

The importance of growing up: juvenile environment influences dispersal of individuals and their neighbours.

Dispersal is a key ecological process that is strongly influenced by both phenotype and environment. Here, we show that juvenile environment influences dispersal not only by shaping individual phenotypes, but also by changing the phenotypes of neighbouring conspecifics, which influence how individuals disperse. We used a model system (Tribolium castaneum, red flour beetles) to test how the past environment of dispersing individuals and their neighbours influences how they disperse in their current environment. We found that individuals dispersed especially far when exposed to a poor environment as adults if their phenotype, or even one-third of their neighbours' phenotypes, were shaped by a poor environment as juveniles. Juvenile environment therefore shapes dispersal both directly, by influencing phenotype, as well as indirectly, by influencing the external social environment. Thus, the juvenile environment of even a minority of individuals in a group can influence the dispersal of the entire group.

Stochastic processes drive rapid genomic divergence during experimental range expansions.

Range expansions are crucibles for rapid evolution, acting via both selective and neutral mechanisms. While selection on traits such as dispersal and fecundity may increase expansion speed, neutral mechanisms arising from repeated bottlenecks and genetic drift in edge populations (i.e. gene surfing) could slow spread or make it less predictable. Thus, it is necessary to disentangle the effects of selection from neutral mechanisms to robustly predict expansion dynamics. This is difficult to do with expansions in nature, as replicated expansions are required to distinguish selective and neutral processes in the genome. Using replicated microcosms of the red flour beetle ( Tribolium castaneum), we identify a robust signature of stochastic, neutral mechanisms in genomic changes arising over only eight generations of expansion and assess the role of standing variation and de novo mutations in driving these changes. Average genetic diversity was reduced within edge populations, but with substantial among-replicate variability in the changes at specific genomic windows. Such variability in genomic changes is consistent with a large role for stochastic, neutral processes. This increased genomic divergence among populations was mirrored by heightened variation in population size and expansion speed, suggesting that stochastic variation in the genome could increase unpredictability of range expansions.

Deciphering the Routes of invasion of Drosophila suzukii by Means of ABC Random Forest.

Deciphering invasion routes from molecular data is crucial to understanding biological invasions, including identifying bottlenecks in population size and admixture among distinct populations. Here, we unravel the invasion routes of the invasive pest Drosophila suzukii using a multi-locus microsatellite dataset (25 loci on 23 worldwide sampling locations). To do this, we use approximate Bayesian computation (ABC), which has improved the reconstruction of invasion routes, but can be computationally expensive. We use our study to illustrate the use of a new, more efficient, ABC method, ABC random forest (ABC-RF) and compare it to a standard ABC method (ABC-LDA). We find that Japan emerges as the most probable source of the earliest recorded invasion into Hawaii. Southeast China and Hawaii together are the most probable sources of populations in western North America, which then in turn served as sources for those in eastern North America. European populations are genetically more homogeneous than North American populations, and their most probable source is northeast China, with evidence of limited gene flow from the eastern US as well. All introduced populations passed through bottlenecks, and analyses reveal five distinct admixture events. These findings can inform hypotheses concerning how this species evolved between different and independent source and invasive populations. Methodological comparisons indicate that ABC-RF and ABC-LDA show concordant results if ABC-LDA is based on a large number of simulated datasets but that ABC-RF out-performs ABC-LDA when using a comparable and more manageable number of simulated datasets, especially when analyzing complex introduction scenarios.

Three types of rescue can avert extinction in a changing environment.

Setting aside high-quality large areas of habitat to protect threatened populations is becoming increasingly difficult as humans fragment and degrade the environment. Biologists and managers therefore must determine the best way to shepherd small populations through the dual challenges of reductions in both the number of individuals and genetic variability. By bringing in additional individuals, threatened populations can be increased in size (demographic rescue) or provided with variation to facilitate adaptation and reduce inbreeding (genetic rescue). The relative strengths of demographic and genetic rescue for reducing extinction and increasing growth of threatened populations are untested, and which type of rescue is effective may vary with population size. Using the flour beetle (Tribolium castaneum) in a microcosm experiment, we disentangled the genetic and demographic components of rescue, and compared them with adaptation from standing genetic variation (evolutionary rescue in the strictest sense) using 244 experimental populations founded at either a smaller (50 individuals) or larger (150 individuals) size. Both types of rescue reduced extinction, and those effects were additive. Over the course of six generations, genetic rescue increased population sizes and intrinsic fitness substantially. Both large and small populations showed evidence of being able to adapt from standing genetic variation. Our results support the practice of genetic rescue in facilitating adaptation and reducing inbreeding depression, and suggest that demographic rescue alone may suffice in larger populations even if only moderately inbred individuals are available for addition.

Genetic and demographic founder effects have long-term fitness consequences for colonising populations.

Colonisation is a fundamental ecological and evolutionary process that drives the distribution and abundance of organisms. The initial ability of colonists to establish is determined largely by the number of founders and their genetic background. We explore the importance of these demographic and genetic properties for longer term persistence and adaptation of populations colonising a novel habitat using experimental populations of Tribolium castaneum. We introduced individuals from three genetic backgrounds (inbred - outbred) into a novel environment at three founding sizes (2-32), and tracked populations for seven generations. Inbreeding had negative effects, whereas outbreeding generally had positive effects on establishment, population growth and long-term persistence. Severe bottlenecks due to small founding sizes reduced genetic variation and fitness but did not prevent adaptation if the founders originated from genetically diverse populations. Thus, we find important and largely independent roles for both demographic and genetic processes in driving colonisation success.

Admixture is a driver rather than a passenger in experimental invasions.

Genetic admixture propels invasions of Callosobruchus maculatus across experimental landscapes. In Focus: Wagner, N.K., Ochocki, B.M., Crawford, K.M., Compagnoni, A. & Miller, T.E.X. (2017) Genetic mixture of multiple source populations accelerates invasive range expansion. Journal of Animal Ecology, 86, 21-34. In this issue of Journal of Animal Ecology, Wagner et al. (2017) demonstrate that genetic diversity can alter the course of spread of biological invasions. They employ Callosobruchus seed beetles in a clever array of linked habitat patches to compare experimental invasions using individuals from single population sources or from mixes of two, four or six population sources. By taking a model-selection approach, they find that any amount of mixture propels growth rates and spread of introduced populations. This suggests that heterosis alone can alter the course of an invasive range expansion.

The roles of demography and genetics in the early stages of colonization.

Colonization success increases with the size of the founding group. Both demographic and genetic factors underlie this relationship, yet because genetic diversity normally increases with numbers of individuals, their relative importance remains unclear. Furthermore, their influence may depend on the environment and may change as colonization progresses from establishment through population growth and then dispersal. We tested the roles of genetics, demography and environment in the founding of Tribolium castaneum populations. Using three genetic backgrounds (inbred to outbred), we released individuals of four founding sizes (2-32) into two environments (natal and novel), and measured establishment success, initial population growth and dispersal. Establishment increased with founding size, whereas population growth was shaped by founding size, genetic background and environment. Population growth was depressed by inbreeding at small founding sizes, but growth rates were similar across genetic backgrounds at large founding size, an interaction indicating that the magnitude of the genetic effects depends upon founding population size. Dispersal rates increased with genetic diversity. These results suggest that numbers of individuals may drive initial establishment, but that subsequent population growth and spread, even in the first generation of colonization, can be driven by genetic processes, including both reduced growth owing to inbreeding depression, and increased dispersal with increased genetic diversity.

Rapid evolution of an invasive weed.

Trade-offs between performance and the ability to tolerate abiotic and biotic stress have been suggested to explain both the success of invasive species and phenotypic differentiation between native and invasive populations. It is critical to sample broadly across both ranges and to account for latitudinal clines and maternal effects when testing this premise. Wild-collected Centaurea diffusa seeds were grown in benign and stressful conditions (drought, flooding, nutrient stress and simulated herbivory), to evaluate whether native and introduced individuals differ in performance or life history phenotypes. A second experiment used glasshouse-grown seeds to evaluate whether patterns remain comparable when maternal environment is consistent. Many traits differed between ranges, and in all cases but one, invasive individuals grew larger, performed better, or matured later. No trade-off in performance with herbivore defense was evident. Invasive populations may have been released from a trade-off between growth and drought tolerance apparent in the native range. Larger individuals with delayed maturity and greater reproductive potential have evolved in invasive populations, a pattern evident across broad population sampling, and after latitude and maternal environment were considered. Release from abiotic stress tolerance trade-offs may be important for the invasion success of Centaurea diffusa.

Evolution is more repeatable in the introduction than range expansion phase of colonization.

How repeatable is evolution at genomic and phenotypic scales? We studied the repeatability of evolution during 8 generations of colonization using replicated microcosm experiments with the red flour beetle, Tribolium castaneum. Based on the patterns of shared allele frequency changes that occurred in populations from the same generation or experimental location, we found adaptive evolution to be more repeatable in the introduction and establishment phases of colonization than in the spread phase, when populations expand their range. Lastly, by studying changes in allele frequencies at conserved loci, we found evidence for the theoretical prediction that range expansion reduces the efficiency of selection to purge deleterious alleles. Overall, our results increase our understanding of adaptive evolution during colonization, demonstrating that evolution can be highly repeatable while also showing that stochasticity still plays an important role.

Do invasive species perform better in their new ranges?

A fundamental assumption in invasion biology is that most invasive species exhibit enhanced performance in their introduced range relative to their home ranges. This idea has given rise to numerous hypotheses explaining "invasion success" by virtue of altered ecological and evolutionary pressures. There are surprisingly few data, however, testing the underlying assumption that the performance of introduced populations, including organism size, reproductive output, and abundance, is enhanced in their introduced compared to their native range. Here, we combined data from published studies to test this hypothesis for 26 plant and 27 animal species that are considered to be invasive. On average, individuals of these 53 species were indeed larger, more fecund, and more abundant in their introduced ranges. The overall mean, however, belied significant variability among species, as roughly half of the investigated species (N=27) performed similarly when compared to conspecific populations in their native range. Thus, although some invasive species are performing better in their new ranges, the pattern is not universal, and just as many are performing largely the same across ranges.

Population demographic history and evolutionary rescue: Influence of a bottleneck event.

Rapid environmental change presents a significant challenge to the persistence of natural populations. Rapid adaptation that increases population growth, enabling populations that declined following severe environmental change to grow and avoid extinction, is called evolutionary rescue. Numerous studies have shown that evolutionary rescue can indeed prevent extinction. Here, we extend those results by considering the demographic history of populations. To evaluate how demographic history influences evolutionary rescue, we created 80 populations of red flour beetle, Tribolium castaneum, with three classes of demographic history: diverse populations that did not experience a bottleneck, and populations that experienced either an intermediate or a strong bottleneck. We subjected these populations to a new and challenging environment for six discrete generations and tracked extinction and population size. Populations that did not experience a bottleneck in their demographic history avoided extinction entirely, while more than 20% of populations that experienced an intermediate or strong bottleneck went extinct. Similarly, among the extant populations at the end of the experiment, adaptation increased the growth rate in the novel environment the most for populations that had not experienced a bottleneck in their history. Taken together, these results highlight the importance of considering the demographic history of populations to make useful and effective conservation decisions and management strategies for populations experiencing environmental change that pushes them toward extinction.

Evolution of reproductive life-history and dispersal traits during the range expansion of a biological control agent.

Evolutionary theory predicts that the process of range expansion will lead to differences in life-history and dispersal traits between the core and edge of a population. At the edge, selection and genetic drift can have opposing effects on reproductive ability, while spatial sorting by dispersal ability can increase dispersal. However, the context that individuals experience, including population density and mating status, also impacts dispersal behavior. We seek to understand the shifts in traits of populations expanding across natural, heterogenous environments, and the evolutionary and behavioral factors that may drive those shifts. We evaluated theoretical predictions for evolution of reproductive life-history and dispersal traits using the range expansion of a biological control agent, Diorhabda carinulata, or northern tamarisk beetle. We find that individuals from the edge had increased fecundity and female body mass, and reduced age at first reproduction, indicating that genetic load is low and suggesting that selection has acted at the edge. We also find that density of conspecifics during rearing and mating status influence dispersal of males and that dispersal increases at the edge of the range under certain conditions, particularly when males were unmated and reared at low density. The restricted conditions in which dispersal has increased suggest that spatial sorting has exerted weak effects relative to other potential processes. Our results support most theoretical predictions about evolution during range expansion, even across a heterogeneous environment, especially when the ecological context is considered.

Hybridization and range expansion in tamarisk beetles (Diorhabda spp.) introduced to North America for classical biological control.

With the global rise of human-mediated translocations and invasions, it is critical to understand the genomic consequences of hybridization and mechanisms of range expansion. Conventional wisdom is that high genetic drift and loss of genetic diversity due to repeated founder effects will constrain introduced species. However, reduced genetic variation can be countered by behavioral aspects and admixture with other distinct populations. As planned invasions, classical biological control (biocontrol) agents present important opportunities to understand the mechanisms of establishment and spread in a novel environment. The ability of biocontrol agents to spread and adapt, and their effects on local ecosystems, depends on genomic variation and the consequences of admixture in novel environments. Here, we use a biocontrol system to examine the genome-wide outcomes of introduction, spread, and hybridization in four cryptic species of a biocontrol agent, the tamarisk beetle (Diorhabda carinata, D. carinulata, D. elongata, and D. sublineata), introduced from six localities across Eurasia to control the invasive shrub tamarisk (Tamarix spp.) in western North America. We assembled a de novo draft reference genome and applied RADseq to over 500 individuals across laboratory cultures, the native ranges, and the introduced range. Despite evidence of a substantial genetic bottleneck among D. carinulata in N. America, populations continue to establish and spread, possibly due to aggregation behavior. We found that D. carinata, D. elongata, and D. sublineata hybridize in the field to varying extents, with D. carinata × D. sublineata hybrids being the most abundant. Genetic diversity was greater at sites with hybrids, highlighting potential for increased ability to adapt and expand. Our results demonstrate the complex patterns of genomic variation that can result from introduction of multiple ecotypes or species for biocontrol, and the importance of understanding them to predict and manage the effects of biocontrol agents in novel ecosystems.

Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly.

Both local adaptation and adaptive phenotypic plasticity can influence the match between phenotypic traits and local environmental conditions. Theory predicts that environments stable for multiple generations promote local adaptation, whereas highly heterogeneous environments favor adaptive phenotypic plasticity. However, when environments have periods of stability mixed with heterogeneity, the relative importance of local adaptation and adaptive phenotypic plasticity is unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on the match of populations to environments with periods of stability from three to four generations. This invasive pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of distinct host fruits, each one being available for only a few generations. Using reciprocal common environment experiments of natural D. suzukii populations collected from cherry, strawberry, and blackberry, we found that both oviposition preference and offspring performance were higher on medium made with the fruit from which the population originated than on media made with alternative fruits. This pattern, which remained after two generations in the laboratory, was analyzed using a statistical method we developed to quantify the contributions of local adaptation and adaptive plasticity in determining fitness. Altogether, we found that genetic effects (local adaptation) dominate over plastic effects (adaptive phenotypic plasticity). Our study demonstrates that spatially and temporally variable selection does not prevent the rapid evolution of local adaptation in natural populations. The speed and strength of adaptation may be facilitated by several mechanisms including a large effective population size and strong selective pressures imposed by host plants.