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Biology subjects

Hufbauer, R. A.

Publications and source records attributed to Hufbauer, R. A..

14 recordsLinked to original sources

Summer rainfall drives adaptation with gene flow in a widespread butterfly

Understanding how environmental variation interacts with gene flow to shape population genomic patterns is a central goal in evolutionary biology. We investigated how geographic and environmental differences impact genomic variation in the clouded sulfur butterfly (Colias philodice eriphyle) by conducting whole-genome resequencing across replicated transects consisting of paired high- and low-elevation sites on both sides of a major mountain range. Despite sampling across steep environmental gradients, we found no evidence of discrete population structure, indicating high connectivity across the region. Nonetheless, significant isolation by distance - strongest in eastern populations - revealed that geographic distance still imposes limits on gene flow, and genetic diversity was also elevated in the east. Genotype-environment association analyses identified more than 16,000 loci associated with elevation, precipitation, and solar radiation. Our redundancy analysis identified precipitation as the strongest predictor of adaptive genomic differentiation, and candidate genes included those linked to melanization and thermoregulation (e.g., TH and yellow). These results demonstrate that even in a largely panmictic population, environmental variation can maintain regional-scale signals of local adaptation. Because insects are declining globally and remain underrepresented in genomic monitoring, conducting whole-genome analyses in a widespread species provides valuable context for assessing how insects today persist across such diverse landscapes and their potential for withstanding future environmental change.

evolutionary biology↗

Density dependence impedes evolutionary rescue

Evolutionary rescue allows populations to adapt and persist despite severe environmental change. While well studied under density-independent conditions, the role of density dependence, including competition, remains unclear. Theoretical models offer conflicting predictions, with density dependence either increasing extinction risk or enhancing adaptation. We empirically tested how density dependence influences evolutionary rescue by exposing experimental populations to a stressful environment for six generations under density-dependent or independent conditions, with populations where either evolution was possible or was prevented by replacing individuals each generation. Density dependence suppressed population size and increased extinction risk, whereas density independence enabled rapid growth, especially in genetically diverse populations where evolution was possible. Although density dependence raises extinction risk, it does not prevent populations from responding to selection, since surviving density-dependent populations still exhibited increased intrinsic and realized fitness. These findings reconcile theoretical discrepancies, showing density dependence can simultaneously increase extinction risk but may favor adaptation. Our results underscore the importance of considering density dependence in conservation strategies.

evolutionary biology↗

Environmental gradients mediate dispersal evolution during biological invasions

Rapid dispersal evolution at the edge of a range expansion can accelerate invasions. However, expanding populations will often encounter environmental gradients that entail a fitness cost of dispersal. We used an eco-evolutionary model to explore how environmental heterogeneity influences adaptation and dispersal evolution during range expansion and, in turn, modulates the speed and predictability of invasion. Environmental gradients opposed the evolution of increased dispersal during invasion, even leading to the evolution of reduced dispersal along steep gradients. Counterintuitively, reduced dispersal allowed for faster expansion by minimizing maladaptation. While evolution across homogenous landscapes caused invasions to be highly unpredictable, even shallow environmental gradients greatly increased invasion predictability. We illustrate our models potential application to prediction and management of invasions by parameterizing it with data from a recent invertebrate range expansion. Overall, we find that environmental heterogeneity and local adaptation strongly modulate the effect of dispersal evolution on invasion trajectories.

ecology↗

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

In todays 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 three immigration rates (zero, one, or five 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 seven 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.

evolutionary biology↗

Adaptation at the edge: Patterns of local adaptation and genetic variation during a contemporary range expansion

During range expansion, differences can evolve between populations at the core and expanding edge of a range. While theory and experimental work has focused on range expansions across uniform environments, natural range expansions often occur over environmental gradients, which present novel selection pressures. We seek to understand how genetic variation expressed in different environments may constrain adaptation during range expansion across environmental gradients, by testing whether long-established populations are better adapted to their local environments than newly established populations in the expanding edge. We study the timing of winter dormancy in a beetle introduced for biological control (Diorhabda carinulata), expanding from areas with cold winters to areas with milder, shorter winters. In a reciprocal environment experiment, core populations showed a pattern of local adaptation, but only some edge populations showed a similar pattern, indicating these populations vary in their degree of adaptation. Expressed genetic variation of dormancy timing in a core population was high in a local (core) environment but disappeared in a novel (edge) environment. These results show that adaptive evolution has been rapid, likely fueled by high heritability, but long-distance movement may hinder adaptation by reducing the heritable genetic variation on which selection can act.

evolutionary biology↗

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.

evolutionary biology↗

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.

ecology↗

Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive 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, while 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. Impact SummaryNatural populations often exhibit good "fit" to the environment they are in. However, environments change over time and space, and following change, the fit between a population and its environment may be poor. A question of long-standing interest is how do populations track changing environments to maintain fitness? Two main mechanisms are known: (i) genetic shifts in the form of local adaptation, in which traits evolve over time through differences in fitness of individuals harboring different genetic variants, and (ii) plastic shifts, or adaptive phenotypic plasticity, in which traits immediately change in response to environmental change. Adaptation is common when environments change over multiple generations, while plasticity is common when environments change over an individuals lifetime. However, it remains unclear whether plasticity or adaptation is more vital to maintaining fitness when environments change at an intermediate pace. Drosophila suzukii is well-suited to evaluating the relative importance of plasticity and adaptation in response to an intermediate pace of environmental change. This invasive pest species experiences an environment that shifts every 1-4 generations as host fruits change over time and space. Here, we studied natural populations of D. suzukii collected from different hosts. Using reciprocal common environment experiments, we evaluated their fitness on their source and alternative hosts. Drosophila suzukii populations were most fit on their source host, successfully tracking an intermediate pace of environmental change. We developed a statistical method to quantify the contributions of adaptive plasticity and local adaptation in determining fitness. We found that fitness was mainly maintained through local adaptation to each new host in succession. This study highlights that spatially and temporally variable selection does not prevent local adaptation and, on the contrary, illustrates how rapid the adaptive process can be. It also provides a novel statistical tool that can be applied to other systems

evolutionary biology↗

Can intraspecific variation in a herbivorous mite alter responses to drought-stressed host plant? A common garden experiment in the context of climate change

Drought associated with climate change can stress plants, altering their interactions with phytophagous arthropods. Drought not only impacts cultivated plants but also their parasites, which in some cases are favored by drought. Herbivorous arthropods feeding on drought-stressed plants typically produce bigger offspring and develop faster. However, it is unclear how much responses to drought stress differ among populations of herbivore species. Here, we evaluate variability among populations of a major agricultural pest, the two spotted spider mite, Tetranychus urticae, in response to drought stress. We compare key life history parameters of twelve populations that originate from climates ranging from wet and cool Atlantic locations to medium to dry hot Mediterranean locations. We evaluated how plant drought stress affects four life history traits: development time, fecundity, sex-ratio and emigration rate in an experiment comparing well-watered and drought-stressed bean plants. Mites feeding on drought-stressed plants developed faster and attempted to leave leaves less often, and young females were more fecund. The mites from wet temperate climates exhibited greater plasticity between the two water regimes than mites originating from dryer and hot climates, suggesting that the climate in the area of origin influences mite response to drought.

zoology↗

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 vs. 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 vs. 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.

evolutionary biology↗

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 from laboratory cultures, the native ranges, and across 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 x 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.

evolutionary biology↗

How do invasion syndromes evolve? An experimental evolution approach using the ladybug Harmonia axyridis

Experiments comparing native to introduced populations or distinct introduced populations to each other show that phenotypic evolution is common and often involves a suit of interacting phenotypic traits. We define such sets of traits that evolve in concert and contribute to the success of invasive populations as an invasion syndrome. The invasive Harlequin ladybird Harmonia axyridis displays such an invasion syndrome with, for instance, females from invasive populations being larger and heavier than individuals from native populations, allocating more resources to reproduction, and spreading reproduction over a longer lifespan. Invasion syndromes could emerge due to selection acting jointly and directly on a multitude of traits, or due to selection on one or a few key traits that drive correlated indirect responses in other traits. Here, we investigated the degree to which the H. axyridis invasion syndrome would emerge in response to artificial selection on either female body mass or on age at first reproduction, two traits involved in their invasion syndrome. To further explore the interaction between environmental context and evolutionary change in molding the phenotypic response, we phenotyped the individuals from the selection experiments in two environments, one with abundant food resources and one with limited resources. The two artificial selection experiments show that the number of traits showing a correlated response depends upon the trait undergoing direct selection. Artificial selection on female body mass resulted in few correlated responses and hence poorly reproduced the invasion syndrome. In contrast, artificial selection on age at first reproduction resulted in more widespread phenotypic changes, which nevertheless corresponded only partly to the invasion syndrome. The artificial selection experiments also revealed a large impact of diet on the traits, with effects dependent on the trait considered and the selection regime. Overall, our results indicate that direct selection on multiple traits was likely necessary in the evolution of the H. axyridis invasion syndrome. Furthermore, they show the strength of using artificial selection to identify the traits that are correlated in different selective contexts, which represents a crucial first step in understanding the evolution of complex phenotypic patterns, including invasion syndromes.

evolutionary biology↗

Evolution of trade-offs across environments following experimental evolution of the generalist Drosophila suzukii to different fruit media

The process of local adaptation involves differential changes in fitness over time across different environments. While 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 analyzed 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.

evolutionary biology↗

Parsing propagule pressure: Simulated and experimental disentanglement of introduction size and number of introductions for colonizing individuals

Predicting whether individuals will colonize a novel habitat is of fundamental ecological interest and is crucial to both conservation efforts and invasive species management. A consistently supported predictor of colonization success is the number of individuals introduced, also called propagule pressure. Propagule pressure increases with the number of introductions and the number of individuals per introduction (the size of the introduction), but it is unresolved which process is a stronger driver of colonization success. Furthermore their relative importance may depend upon the environment, with multiple introductions potentially enhancing colonization of fluctuating environments. To evaluate the relative importance of the number and size of introductions and its dependence upon environmental variability, we paired demographic simulations with a microcosm experiment. Using Tribolium flour beetles as a model system, we introduced a fixed number of individuals into replicated novel habitats of stable or fluctuating quality, varying the number of introductions through time and size of each introduction. We evaluated establishment probability and the size of extant populations after 7 generations. In the simulations and microcosms, we found that establishment probability increased with more, smaller introductions, but was not affected by biologically realistic fluctuations in environmental quality. Population size was not significantly affected by environmental variability in the simulations, but populations in the microcosms grew larger in a stable environment, especially with more introduction events. In general, the microcosm experiment yielded higher establishment probability and larger populations than the demographic simulations. We suggest that genetic mechanisms likely underlie these differences and thus deserve more attention in efforts to parse propagule pressure. Our results highlight the importance of preventing further introductions of undesirable species to invaded sites, and suggest conservation efforts should focus on increasing the number of introductions or re-introductions of desirable species rather than increasing the size of those introduction events.

ecology↗