Marianna Szűcs

Underutilized resources for studying the evolution of invasive species during their introduction, establishment, and lag phases

The early phases of biological invasions are poorly understood. In particular, during the introduction, establishment, and possible lag phases, it is unclear to what extent evolution must take place for an introduced species to transition from established to expanding. In this study, we highlight three disparate data sources that can provide insights into evolutionary processes associated with invasion success: biological control organisms, horticultural introductions, and natural history collections. All three data sources potentially provide introduction dates, information about source populations, and genetic and morphological samples at different time points along the invasion trajectory that can be used to investigate preadaptation and evolution during the invasion process, including immediately after introduction and before invasive expansion. For all three data sources, we explore where the data are held, their quality, and their accessibility. We argue that these sources could find widespread use with a few additional pieces of data, such as voucher specimens collected at certain critical time points during biocontrol agent quarantine, rearing, and release and also for horticultural imports, neither of which are currently done consistently. In addition, public access to collected information must become available on centralized databases to increase its utility in ecological and evolutionary research.

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.

Three types of rescue can avert extinction in a changing environment

Significance Preventing extinction of small populations in rapidly changing environments is crucial to long-term preservation of diversity, because the creation of large reserves is often not feasible. An option immediately available to managers is bringing migrants in to increase size or improve genetic composition of populations at risk. We experimentally manipulate different types and combinations of migrants to evaluate which will be most effective in rescuing populations from extinction. We find that migration of numerous individuals can reduce the probability of extinction. However, migration of just a few genetically distinct individuals both reduces probability of extinction and dramatically increases fitness and population size. We suggest managers with limited conservation resources should prioritize genetic rescue over increasing demographic size for small populations. 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.

Hybrid vigor in the biological control agent, Longitarsus jacobaeae

Hybridization is an important evolutionary mechanism that can increase the fitness and adaptive potential of populations. A growing body of evidence supports its importance as a key factor contributing to rapid evolution in invasive species, but the effects of hybridization have rarely been assessed in intentionally introduced biological control agents. We investigated hybrids between a Swiss and an Italian population of the beetle, Longitarsus jacobaeae, a biological control agent of Jacobaea vulgaris, by reciprocally crossing individuals in the laboratory. Phenological traits of F1 and F2 hybrid lineages showed intermediate values relative to their parental populations, with some maternal influence. Fitness of the F2 generation, measured as lifetime fecundity, was higher than that of the Italian parent in one of the lineages and higher than that of either parent in the other hybrid lineage. The increased fecundity of hybrids may benefit tansy ragwort biological control by increasing the establishment success and facilitating a more rapid population buildup in the early generations. Even though the long‐term consequences of hybridization in this and other systems are hard to predict, intentional hybridization may be a useful tool in biological control strategies as it would promote similar microevolutionary processes operating in numerous targeted invasive species.

Post-introduction evolution in the biological control agent Longitarsus jacobaeae (Coleoptera: Chrysomelidae).

Rapid evolution has rarely been assessed in biological control systems despite the similarity with biological invasions, which are widely used as model systems. We assessed post‐introduction climatic adaptation in a population of Longitarsus jacobaeae, a biological control agent of Jacobaea vulgaris, which originated from a low‐elevation site in Italy and was introduced in the USA to a high‐elevation site (Mt. Hood, Oregon) in the early 1980s. Life‐history characteristics of beetle populations from Mt. Hood, from two low‐elevation sites in Oregon (Italian origin) and from a high‐elevation site from Switzerland were compared in common gardens. The performance of low‐ and high‐elevation populations at a low‐ and a high‐elevation site was evaluated using reciprocal transplants. The results revealed significant changes in aestival diapause and shifts in phenology in the Mt. Hood population, compared with the low‐elevation populations. We found increased performance of the Mt. Hood population in its home environment compared with the low‐elevation populations that it originated from. The results indicate that the beetles at Mt. Hood have adapted to the cooler conditions by life‐history changes that conform to predictions based on theory and the phenology of the cold‐adapted Swiss beetles.

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.

Rapid adaptive evolution in novel environments acts as an architect of population range expansion

Significance It is crucial to understand what governs the growth and spread of populations colonizing novel environments to better predict species responses to global change, including range shifts in response to warming and biological invasions. Evolutionary processes can be rapid enough to influence colonizing populations; however, it is unclear whether evolution governs the course of colonization events or if it is an outcome that arises gradually after successful establishment. We either allowed or restricted evolution in replicate populations released in a novel environment, and found that populations that were allowed to evolve grew three times larger and expanded their ranges 46% faster compared with nonevolving populations. Thus, evolution facilitates colonization from the outset and should be considered in management decisions. Colonization and expansion into novel landscapes determine the distribution and abundance of species in our rapidly changing ecosystems worldwide. Colonization events are crucibles for rapid evolution, but it is not known whether evolutionary changes arise mainly after successful colonization has occurred, or if evolution plays an immediate role, governing the growth and expansion speed of colonizing populations. There is evidence that spatial evolutionary processes can speed range expansion within a few generations because dispersal tendencies may evolve upwards at range edges. Additionally, rapid adaptation to a novel environment can increase population growth rates, which also promotes spread. However, the role of adaptive evolution and the relative contributions of spatial evolution and adaptation to expansion are unclear. Using a model system, red flour beetles (Tribolium castaneum), we either allowed or constrained evolution of populations colonizing a novel environment and measured population growth and spread. At the end of the experiment we assessed the fitness and dispersal tendency of individuals originating either from the core or edge of evolving populations or from nonevolving populations in a common garden. Within six generations, evolving populations grew three times larger and spread 46% faster than populations in which evolution was constrained. Increased size and expansion speed were strongly driven by adaptation, whereas spatial evolutionary processes acting on edge subpopulations contributed less. This experimental evidence demonstrates that rapid evolution drives both population growth and expansion speed and is thus crucial to consider for managing biological invasions and successfully introducing or reintroducing species for management and conservation.

The power of evolutionary rescue is constrained by genetic load

The risk of extinction faced by small isolated populations in changing environments can be reduced by rapid adaptation and subsequent growth to larger, less vulnerable sizes. Whether this process, called evolutionary rescue, is able to reduce extinction risk and sustain population growth over multiple generations is largely unknown. To understand the consequences of adaptive evolution as well as maladaptive processes in small isolated populations, we subjected experimental Tribolium castaneum populations founded with 10 or 40 individuals to novel environments, one more favorable, and one resource poor, and either allowed evolution, or constrained it by replacing individuals one‐for‐one each generation with those from a large population maintained in the natal environment. Replacement individuals spent one generation in the target novel environment before use to standardize effects due to the parental environment. After eight generations we mixed a subset of surviving populations to facilitate admixture, allowing us to estimate drift load by comparing performance of mixed to unmixed groups. Evolving populations had reduced extinction rates, and increased population sizes in the first four to five generations compared to populations where evolution was constrained. Performance of evolving populations subsequently declined. Admixture restored their performance, indicating high drift load that may have overwhelmed the beneficial effects of adaptation in evolving populations. Our results indicate that evolution may quickly reduce extinction risk and increase population sizes, but suggest that relying solely on adaptation from standing genetic variation may not provide long‐term benefits to small isolated populations of diploid sexual species, and that active management facilitating gene flow may be necessary for longer term persistence.

Reply to Wootton and Pfister: The search for general context should include synthesis with laboratory model systems

Wootton and Pfister (1) note the striking contrast between the results of their elegant field study (2) and our laboratory study (3), both of which manipulated genetic diversity and population size independently. Wootton and Pfister (1) found that population size most strongly influences extinction risk, whereas we (3) found that genetic diversity matters as much as population size in reducing extinction, and that genetic diversity also increases long-term growth rates of extant populations. Given the implications for management of small populations, it is crucial to understand why our results differ.

The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations

The success rate of weed biological control programs is difficult to evaluate and the factors affecting it remain poorly understood. One aspect which is still unclear is whether releases of multiple, genetically distinct populations of a biological control agent increase the likelihood of success, either by independent colonization of different environmental niches or by hybridization that may increase the agents fitness and adaptive ability. Since hybridization is often invoked to explain the success of unintentionally introduced exotic species, hybridization among biocontrol agents may be similarly important in shaping the effectiveness of biological control programs. In this study, we first evaluated intraspecific hybridization among populations of a weed biological control agent, the ragwort flea beetle, Longitarsus jacobaeae. These insects were introduced as part of a classical biological control program from Italy and Switzerland. We genotyped 204 individuals from 15 field sites collected in northwest Montana, and an additional 52 individuals that served as references for Italian and Swiss populations. Bayesian analysis of population structure assigned seven populations as pure Swiss and one population as pure Italian, while intraspecific hybrid individuals were detected in seven populations at frequencies of 5%–69%. Subsequently, we conducted a 2‐year exclusion experiment using six sites with Swiss beetles and three with hybrid beetles to evaluate the impact of biological control. We found that biological control by Swiss beetles and by hybrid beetles is effective, increasing mortality of the target plant, Jacobaea vulgaris, by 42% and 45%, and reducing fecundity of surviving plants by 44% and 72%, respectively. Beetle densities were higher and mortality of larger plants was higher at sites with hybrids present. These results suggest that hybridization of ragwort flea beetles at high‐elevation sites may improve biological control of tansy ragwort and that intraspecific hybridization of agents could benefit biological control programs.