Environmental gradients mediate dispersal evolution during biological invasions.

Rapid evolution of increased dispersal at the edge of a range expansion can accelerate invasions. However, populations expanding across environmental gradients often face challenging environments that reduce fitness of dispersing individuals. We used an eco-evolutionary model to explore how environmental gradients influence dispersal evolution and, in turn, modulate the speed and predictability of invasion. Environmental gradients opposed evolution of increased dispersal during invasion, even leading to evolution of reduced dispersal along steeper gradients. Counterintuitively, reduced dispersal could allow for faster expansion by minimizing maladaptive gene flow and facilitating adaptation. While dispersal evolution across homogenous landscapes increased both the mean and variance of expansion speed, these increases were greatly dampened by environmental gradients. We illustrate our model's potential application to prediction and management of invasions by parameterizing it with data from a recent invertebrate range expansion. Overall, we find that environmental gradients strongly modulate the effect of dispersal evolution on invasion trajectories.

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.

Restoration ecology through the lens of coexistence theory.

Advances in restoration ecology are needed to guide ecological restoration in a variable and changing world. Coexistence theory provides a framework for how variability in environmental conditions and species interactions affects species success. Here, we conceptually link coexistence theory and restoration ecology. First, including low-density growth rates (LDGRs), a classic metric of coexistence, can improve abundance-based restoration goals, because abundances are sensitive to initial treatments and ongoing variability. Second, growth-rate partitioning, developed to identify coexistence mechanisms, can improve restoration practice by informing site selection and indicating necessary interventions (e.g., site amelioration or competitor removal). Finally, coexistence methods can improve restoration assessment, because initial growth rates indicate trajectories, average growth rates measure success, and growth partitioning highlights interventions needed in future.

Experimental evolution of dispersal: Unifying theory, experiments and natural systems.

Dispersal is a central life history trait that affects the ecological and evolutionary dynamics of populations and communities. The recent use of experimental evolution for the study of dispersal is a promising avenue for demonstrating valuable proofs of concept, bringing insight into alternative dispersal strategies and trade-offs, and testing the repeatability of evolutionary outcomes. Practical constraints restrict experimental evolution studies of dispersal to a set of typically small, short-lived organisms reared in artificial laboratory conditions. Here, we argue that despite these restrictions, inferences from these studies can reinforce links between theoretical predictions and empirical observations and advance our understanding of the eco-evolutionary consequences of dispersal. We illustrate how applying an integrative framework of theory, experimental evolution and natural systems can improve our understanding of dispersal evolution under more complex and realistic biological scenarios, such as the role of biotic interactions and complex dispersal syndromes.

Positive effects of exotic species dampened by neighborhood heterogeneity.

It is well known that species interactions between exotic and native species are important for determining the success of biological invasions and how influential exotic species become in invaded communities. The strength and type of interactions between species can substantially vary, however, from negative and detrimental to minimal or even positive. Increasing evidence from the literature shows that exotic species have positive interactions with native species more often than originally thought. Gaps in our theory for how population growth is limited when interactions are positive, however, restrict our understanding of the mechanisms by which exotic "facilitators" contribute to diversity maintenance in invaded systems. Here, we quantified interactions between seven native and four exotic (established nonnative) common annual plant species in the highly diverse, York Gum woodlands of Western Australia. We used a Bayesian demographic modeling approach that allowed for interaction coefficients to be positive or negative, and explored key sources of variation in species responses to native and exotic neighbors at per capita (individual) and neighborhood levels. We observed positive per capita effects from exotic neighbors on exotic focal species as well as on several native focal species. However, all focal species were, on average, inhibited by their interaction neighborhood, when the variance in identity and abundance of observed neighbors was considered. At the neighborhood scale, exotic species were found to suppress all focal species, particularly those with high intrinsic fecundity. Our study demonstrates that within-neighborhood heterogeneity can regulate per capita positive effects of invaders, limiting runaway population growth of both natives and exotic invaders.

Accounting for demographic uncertainty increases predictions for species coexistence: A case study with annual plants.

Natural systems contain more complexity than is accounted for in models of modern coexistence theory. Coexistence modelling often disregards variation arising from stochasticity in biological processes, heterogeneity among individuals and plasticity in trait values. However, these unaccounted-for sources of uncertainty are likely to be ecologically important and have the potential to impact estimates of coexistence. We applied a Bayesian modelling framework to data from an annual plant community in Western Australia to propagate uncertainty in coexistence outcomes using the invasion criterion and ratio of niche to fitness differences. We found accounting for this uncertainty altered predictions of coexistence versus competitive exclusion for 3 out of 14 species pairs and yielded a probability of priority effects for an additional species pair. The propagation of uncertainty arising from sources of biological complexity improves our ability to predict coexistence more accurately in natural systems.

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.

Disentangling key species interactions in diverse and heterogeneous communities: A Bayesian sparse modelling approach.

Modelling species interactions in diverse communities traditionally requires a prohibitively large number of species-interaction coefficients, especially when considering environmental dependence of parameters. We implemented Bayesian variable selection via sparsity-inducing priors on non-linear species abundance models to determine which species interactions should be retained and which can be represented as an average heterospecific interaction term, reducing the number of model parameters. We evaluated model performance using simulated communities, computing out-of-sample predictive accuracy and parameter recovery across different input sample sizes. We applied our method to a diverse empirical community, allowing us to disentangle the direct role of environmental gradients on species' intrinsic growth rates from indirect effects via competitive interactions. We also identified a few neighbouring species from the diverse community that had non-generic interactions with our focal species. This sparse modelling approach facilitates exploration of species interactions in diverse communities while maintaining a manageable number of parameters.

Eco-evolutionary dynamics of range expansion.

Understanding the movement of species' ranges is a classic ecological problem that takes on urgency in this era of global change. Historically treated as a purely ecological process, range expansion is now understood to involve eco-evolutionary feedbacks due to spatial genetic structure that emerges as populations spread. We synthesize empirical and theoretical work on the eco-evolutionary dynamics of range expansion, with emphasis on bridging directional, deterministic processes that favor evolved increases in dispersal and demographic traits with stochastic processes that lead to the random fixation of alleles and traits. We develop a framework for understanding the joint influence of these processes in changing the mean and variance of expansion speed and its underlying traits. Our synthesis of recent laboratory experiments supports the consistent role of evolution in accelerating expansion speed on average, and highlights unexpected diversity in how evolution can influence variability in speed: results not well predicted by current theory. We discuss and evaluate support for three classes of modifiers of eco-evolutionary range dynamics (landscape context, trait genetics, and biotic interactions), identify emerging themes, and suggest new directions for future work in a field that stands to increase in relevance as populations move in response to global change.

Spatial Population Structure Determines Extinction Risk in Climate-Induced Range Shifts.

Climate change is an escalating threat facing populations around the globe, necessitating a robust understanding of the ecological and evolutionary mechanisms dictating population responses. However, populations respond to climate change not in isolation but rather in the context of their existing ranges. In particular, spatial population structure within a range (e.g., trait clines, starkness of range edges, etc.) likely interacts with other ecological and evolutionary processes during climate-induced range shifts. Here, we use an individual-based model to explore the interacting roles of several such factors in range shift dynamics. We show that increased spatial population structure (driven primarily by a steeper environmental gradient) severely increases a population's extinction risk. Further, we show that while evolution of heightened dispersal during range shifts can aid populations in tracking changing conditions, it can also interact negatively with adaptation to the environmental gradient, leading to reduced fitness and contributing to the increased extinction risk observed in populations structured along steep environmental gradients. Our results demonstrate that the effect of dispersal evolution on range-shifting populations is dependent on environmental context and that spatial population structure can substantially increase extinction risk in range shifts.

Pathogens manipulate the preference of vectors, slowing disease spread in a multi-host system.

The spread of vector-borne pathogens depends on a complex set of interactions among pathogen, vector, and host. In single-host systems, pathogens can induce changes in vector preferences for infected vs. healthy hosts. Yet it is unclear if pathogens also induce changes in vector preference among host species, and how changes in vector behaviour alter the ecological dynamics of disease spread. Here, we couple multi-host preference experiments with a novel model of vector preference general to both single and multi-host communities. We show that viruliferous aphids exhibit strong preferences for healthy and long-lived hosts. Coupling experimental results with modelling to account for preference leads to a strong decrease in overall pathogen spread through multi-host communities due to non-random sorting of viruliferous vectors between preferred and non-preferred host species. Our results demonstrate the importance of the interplay between vector behaviour and host diversity as a key mechanism in the spread of vectored-diseases.

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.

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 trait evolution drives increased speed and variance in experimental range expansions.

Range expansions are central to two ecological issues reshaping patterns of global biodiversity: biological invasions and climate change. Traditional theory considers range expansion as the outcome of the demographic processes of birth, death and dispersal, while ignoring the evolutionary implications of such processes. Recent research suggests evolution could also play a critical role in determining expansion speed but controlled experiments are lacking. Here we use flour beetles (Tribolium castaneum) to show experimentally that mean expansion speed and stochastic variation in speed are both increased by rapid evolution of traits at the expansion edge. We find that higher dispersal ability and lower intrinsic growth rates evolve at the expansion edge compared with spatially nonevolving controls. Furthermore, evolution of these traits is variable, leading to enhanced variance in speed among replicate population expansions. Our results demonstrate that evolutionary processes must be considered alongside demographic ones to better understand and predict range expansions.

Natural variation, differentiation, and genetic trade-offs of ecophysiological traits in response to water limitation in Brachypodium distachyon and its descendent allotetraploid B. hybridum (Poaceae).

Differences in tolerance to water stress may underlie ecological divergence of closely related ploidy lineages. However, the mechanistic basis of physiological variation governing ecogeographical cytotype segregation is not well understood. Here, using Brachypodium distachyon and its derived allotetraploid B. hybridum as model, we test the hypothesis that, for heteroploid annuals, ecological divergence of polyploids in drier environments is based on trait differentiation enabling drought escape. We demonstrate that under water limitation allotetraploids maintain higher photosynthesis and stomatal conductance and show earlier flowering than diploids, concordant with a drought-escape strategy to cope with water stress. Increased heterozygosity and greater genetic variability and plasticity of polyploids could confer a superior adaptive capability. Consistent with these predictions, we document (1) greater standing within-population genetic variation in water-use efficiency (WUE) and flowering time in allotetraploids, and (2) the existence of (nonlinear) environmental clines in physiology across allotetraploid populations. Increased gas exchange and diminished WUE occurred at the driest end of the gradient, consistent with a drought-escape strategy. Finally, we found that allotetraploids showed weaker genetic correlations than diploids congruous with the expectation of relaxed pleiotropic constraints in polyploids. Our results suggest evolutionary divergence of ecophysiological traits in each ploidy lineage.

Environmental aridity is associated with cytotype segregation and polyploidy occurrence in Brachypodium distachyon (Poaceae).

• The ecological and adaptive significance of plant polyploidization is not well understood and no clear pattern of association between polyploid frequency and environment has emerged. Climatic factors are expected to predict cytotype distribution. However, the relationship among climate, cytotype distribution and variation of abiotic stress tolerance traits has rarely been examined. • Here, we use flow cytometry and root-tip squashes to examine the cytotype distribution in the temperate annual grass Brachypodium distachyon in 57 natural populations distributed across an aridity gradient in the Iberian Peninsula. We further investigate the link between environmental aridity, ploidy, and variation of drought tolerance and drought avoidance (flowering time) traits. • Distribution of diploids (2n = 10) and allotetraploids (2n = 30) in this species is geographically structured throughout its range in the Iberian Peninsula, and is associated with aridity gradients. Importantly, after controlling for geographic and altitudinal effects, the link between aridity and polyploidization occurrence persisted. Water-use efficiency varied between ploidy levels, with tetraploids being more efficient in the use of water than diploids under water-restricted growing conditions. • Our results indicate that aridity is an important predictor of polyploid occurrence in B. distachyon, suggesting a possible adaptive origin of the cytotype segregation.