Genetic architecture of dispersal and local adaptation drives accelerating range expansions.

Contemporary evolution has the potential to significantly alter biotic responses to global change, including range expansion dynamics and biological invasions. Models predicting range dynamics often make highly simplifying assumptions about the genetic architecture underlying relevant traits. However, genetic architecture defines evolvability and higher-order evolutionary processes, which determine whether evolution will be able to keep up with environmental change or not. Therefore, we here study the impact of the genetic architecture of dispersal and local adaptation, two central traits of high relevance for range expansions, on the dynamics and predictability of invasion into an environmental gradient, such as temperature. In our theoretical model we assume that dispersal and local adaptation traits result from the products of two noninteracting gene-regulatory networks (GRNs). We compare our model to simpler quantitative genetics models and show that in the GRN model, range expansions are accelerating and less predictable. We further find that accelerating dynamics in the GRN model are primarily driven by an increase in the rate of local adaptation to novel habitats which results from greater sensitivity to mutation (decreased robustness) and increased gene expression. Our results highlight how processes at microscopic scales, here within genomes, can impact the predictions of large-scale, macroscopic phenomena, such as range expansions, by modulating the rate of evolution.

Biodiversity increases and decreases ecosystem stability.

Losses and gains in species diversity affect ecological stability1-7 and the sustainability of ecosystem functions and services8-13. Experiments and models have revealed positive, negative and no effects of diversity on individual components of stability, such as temporal variability, resistance and resilience2,3,6,11,12,14. How these stability components covary remains poorly understood15. Similarly, the effects of diversity on overall ecosystem stability16, which is conceptually akin to ecosystem multifunctionality17,18, remain unknown. Here we studied communities of aquatic ciliates to understand how temporal variability, resistance and overall ecosystem stability responded to diversity (that is, species richness) in a large experiment involving 690 micro-ecosystems sampled 19 times over 40 days, resulting in 12,939 samplings. Species richness increased temporal stability but decreased resistance to warming. Thus, two stability components covaried negatively along the diversity gradient. Previous biodiversity manipulation studies rarely reported such negative covariation despite general predictions of the negative effects of diversity on individual stability components3. Integrating our findings with the ecosystem multifunctionality concept revealed hump- and U-shaped effects of diversity on overall ecosystem stability. That is, biodiversity can increase overall ecosystem stability when biodiversity is low, and decrease it when biodiversity is high, or the opposite with a U-shaped relationship. The effects of diversity on ecosystem multifunctionality would also be hump- or U-shaped if diversity had positive effects on some functions and negative effects on others. Linking the ecosystem multifunctionality concept and ecosystem stability can transform the perceived effects of diversity on ecological stability and may help to translate this science into policy-relevant information.

Eco-evolution from deep time to contemporary dynamics: The role of timescales and rate modulators.

Eco-evolutionary dynamics, or eco-evolution for short, are often thought to involve rapid demography (ecology) and equally rapid heritable phenotypic changes (evolution) leading to novel, emergent system behaviours. We argue that this focus on contemporary dynamics is too narrow: Eco-evolution should be extended, first, beyond pure demography to include all environmental dimensions and, second, to include slow eco-evolution which unfolds over thousands or millions of years. This extension allows us to conceptualise biological systems as occupying a two-dimensional time space along axes that capture the speed of ecology and evolution. Using Hutchinson's analogy: Time is the 'theatre' in which ecology and evolution are two interacting 'players'. Eco-evolutionary systems are therefore dynamic: We identify modulators of ecological and evolutionary rates, like temperature or sensitivity to mutation, which can change the speed of ecology and evolution, and hence impact eco-evolution. Environmental change may synchronise the speed of ecology and evolution via these rate modulators, increasing the occurrence of eco-evolution and emergent system behaviours. This represents substantial challenges for prediction, especially in the context of global change. Our perspective attempts to integrate ecology and evolution across disciplines, from gene-regulatory networks to geomorphology and across timescales, from today to deep time.

Landscape Structure Affects Metapopulation-Scale Tipping Points.

AbstractEven when environments deteriorate gradually, ecosystems may shift abruptly from one state to another. Such catastrophic shifts are difficult to predict and sometimes to reverse (so-called hysteresis). While well studied in simplified contexts, we lack a general understanding of how catastrophic shifts spread in realistically spatially structured landscapes. For different types of landscape structures, including typical terrestrial modular and riverine dendritic networks, we here investigate landscape-scale stability in metapopulations whose patches can locally exhibit catastrophic shifts. We find that such metapopulations usually exhibit large-scale catastrophic shifts and hysteresis and that the properties of these shifts depend strongly on the metapopulation spatial structure and on the population dispersal rate: an intermediate dispersal rate, a low average degree, or a riverine spatial structure can largely reduce hysteresis size. Our study suggests that large-scale restoration is easier with spatially clustered restoration efforts and in populations characterized by an intermediate dispersal rate.

Travelling with a parasite: the evolution of resistance and dispersal syndromes during experimental range expansion.

Rapid evolutionary change during range expansions can lead to diverging range core and front populations, with the emergence of dispersal syndromes (coupled responses in dispersal and life-history traits). Besides intraspecific effects, range expansions may be impacted by interspecific interactions such as parasitism. Yet, despite the potentially large impact of parasites imposing additional selective pressures on the host, their role on range expansions remains largely unexplored. Using microcosm populations of the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata, we studied experimental range expansions under parasite presence or absence. We found that the interaction of range expansion and parasite treatments affected the evolution of host dispersal syndromes. Namely, front populations showed different associations of population growth parameters and swimming behaviours than core populations, indicating divergent evolution. Parasitism reshaped trait associations, with hosts evolved in the presence of the parasite exhibiting overall increased resistance and reduced dispersal. Nonetheless, when comparing infected range core and front populations, we found a positive association, suggesting joint evolution of resistance and dispersal at the front. We conclude that host-parasite interactions during range expansions can change evolutionary trajectories; this in turn may feedback on the ecological dynamics of the range expansion and parasite epidemics.

Evolution of thermal performance curves: A meta-analysis of selection experiments.

Temperatures are increasing due to global changes, putting biodiversity at risk. Organisms are faced with a limited set of options to cope with this situation: adapt, disperse or die. We here focus on the first possibility, more specifically, on evolutionary adaptations to temperature. Ectotherms are usually characterized by a hump-shaped relationship between fitness and temperature, a non-linear reaction norm that is referred to as thermal performance curve (TPC). To understand and predict impacts of global change, we need to know whether and how such TPCs evolve. Therefore, we performed a systematic literature search and a statistical meta-analysis focusing on experimental evolution and artificial selection studies. This focus allows us to directly quantify relative fitness responses to temperature selection by calculating fitness differences between TPCs from ancestral and derived populations after thermal selection. Out of 7561 publications screened, we found 47 studies corresponding to our search criteria representing taxa across the tree of life, from bacteria, to plants and vertebrates. We show that, independently of species identity, the studies we found report a positive response to temperature selection. Considering entire TPC shapes, adaptation to higher temperatures traded off with fitness at lower temperatures, leading to niche shifts. Effects were generally stronger in unicellular organisms. By contrast, we do not find statistical support for the often discussed "Hotter is better" hypothesis. While our meta-analysis provides evidence for adaptive potential of TPCs across organisms, it also highlights that more experimental work is needed, especially for under-represented taxa, such as plants and non-model systems.

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.

Dispersal syndromes in challenging environments: A cross-species experiment.

Dispersal is a central biological process tightly integrated into life-histories, morphology, physiology and behaviour. Such associations, or syndromes, are anticipated to impact the eco-evolutionary dynamics of spatially structured populations, and cascade into ecosystem processes. As for dispersal on its own, these syndromes are likely neither fixed nor random, but conditional on the experienced environment. We experimentally studied how dispersal propensity varies with individuals' phenotype and local environmental harshness using 15 species ranging from protists to vertebrates. We reveal a general phenotypic dispersal syndrome across studied species, with dispersers being larger, more active and having a marked locomotion-oriented morphology and a strengthening of the link between dispersal and some phenotypic traits with environmental harshness. Our proof-of-concept metacommunity model further reveals cascading effects of context-dependent syndromes on the local and regional organisation of functional diversity. Our study opens new avenues to advance our understanding of the functioning of spatially structured populations, communities and ecosystems.

Spatial autocorrelation of local patch extinctions drives recovery dynamics in metacommunities.

Human activities put ecosystems under increasing pressure, often resulting in local extinctions. However, it is unclear how local extinctions affect regional processes, such as the distribution of diversity in space, especially if extinctions show spatial patterns, such as being clustered. Therefore, it is crucial to investigate extinctions and their consequences in a spatially explicit framework. Using highly controlled microcosm experiments and theoretical models, we ask here how the number and spatial autocorrelation of extinctions interactively affect metacommunity dynamics. We found that local patch extinctions increased local diversity (α-diversity) and inter-patch diversity (ß-diversity) by delaying the exclusion of inferior competitors. Importantly, recolonization dynamics depended more strongly on the spatial distribution than on the number of patch extinctions: clustered local patch extinctions resulted in slower recovery, lower α-diversity and higher ß-diversity. Our results highlight that the spatial distribution of perturbations should be taken into account when studying and managing spatially structured communities.

Selection on growth rate and local adaptation drive genomic adaptation during experimental range expansions in the protist Tetrahymena thermophila.

Populations that expand their range can undergo rapid evolutionary adaptation of life-history traits, dispersal behaviour and adaptation to the local environment. Such adaptation may be aided or hindered by sexual reproduction, depending on the context. However, few empirical and experimental studies have investigated the genetic basis of adaptive evolution during range expansions. Even less attention has been given to the question how sexual reproduction may modulate such adaptive evolution during range expansions. We here studied genomic adaptation during experimental range expansions of the protist Tetrahymena thermophila in landscapes with a uniform environment or a pH gradient. Specifically, we investigated two aspects of genomic adaptation during range expansion. First, we investigated adaptive genetic change in terms of the underlying numbers of allele frequency changes from standing genetic variation and de novo variants. We focused on how sexual reproduction may alter this adaptive genetic change. Second, we identified genes subject to selection caused by the expanding range itself, and directional selection due to the presence or absence of the pH gradient. We focused this analysis on alleles with large frequency changes that occurred in parallel in more than one population to identify the most likely candidate targets of selection. We found that sexual reproduction altered adaptive genetic change both in terms of de novo variants and standing genetic variation. However, sexual reproduction affected allele frequency changes in standing genetic variation only in the absence of long-distance gene flow. Adaptation to the range expansion affected genes involved in cell divisions and DNA repair, whereas adaptation to the pH gradient additionally affected genes involved in ion balance and oxidoreductase reactions. These genetic changes may result from selection on growth and adaptation to low pH. In the absence of gene flow, sexual reproduction may have aided genetic adaptation. Gene flow may have swamped expanding populations with maladapted alleles, thus reducing the extent of evolutionary adaptation during range expansion. Sexual reproduction also altered the genetic basis of adaptation in our evolving populations via de novo variants, possibly by purging deleterious mutations or by revealing fitness benefits of rare genetic variants.

The conflict between adaptation and dispersal for maintaining biodiversity in changing environments.

Dispersal and adaptation both allow species to persist in changing environments. Yet, we have limited understanding of how these processes interact to affect species persistence, especially in diverse communities where biotic interactions greatly complicate responses to environmental change. Here we use a stochastic metacommunity model to demonstrate how dispersal and adaptation to environmental change independently and interactively contribute to biodiversity maintenance. Dispersal provides spatial insurance, whereby species persist on the landscape by shifting their distributions to track favorable conditions. In contrast, adaptation allows species to persist by allowing for evolutionary rescue. But, when species both adapt and disperse, dispersal and adaptation do not combine positively to affect biodiversity maintenance, even if they do increase the persistence of individual species. This occurs because faster adapting species evolve to hold onto their initial ranges (i.e., monopolization effects), thus impeding slower adapting species from shifting their ranges and thereby causing extinctions. Importantly, these differences in adaptation speed emerge as the result of competition, which alters population sizes and colonization success. By demonstrating how dispersal and adaptation each independently and interactively contribute to the maintenance of biodiversity, we provide a framework that links the theories of spatial insurance, evolutionary rescue, and monopolization. This highlights the expectation that the maintenance of biodiversity in changing environments depends jointly on rates of dispersal and adaptation, and, critically, the interaction between these processes.

An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts.

Exploitative parasites are predicted to evolve in highly connected populations or in expanding epidemics. However, many parasites rely on host dispersal to reach new populations, potentially causing conflict between local transmission and global spread. We performed experimental range expansions in interconnected microcosms of the protozoan Paramecium caudatum, allowing natural dispersal of hosts infected with the bacterial parasite Holospora undulata. Parasites from range front treatments facilitated host dispersal and were less virulent, but also invested less in horizontal transmission than parasites from range cores. These differences were consistent with parameter estimates derived from an epidemiological model fitted on population-level time-series data. Our results illustrate how dispersal selection can have profound consequences for the evolution of parasite life history and virulence. Decrypting the eco-evolutionary processes that shape parasite 'dispersal syndromes' may be important for the management of spreading epidemics in changing environments, biological invasions or in other spatial non-equilibrium settings.

Dispersal behaviour and riverine network connectivity shape the genetic diversity of freshwater amphipod metapopulations.

Theory predicts that the distribution of genetic diversity in a landscape is strongly dependent on the connectivity of the metapopulation and the dispersal of individuals between patches. However, the influence of explicit spatial configurations such as dendritic landscapes on the genetic diversity of metapopulations is still understudied, and theoretical corroborations of empirical patterns are largely lacking. Here, we used microsatellite data and stochastic simulations of two metapopulations of freshwater amphipods in a 28,000 km2 riverine network to study the influence of spatial connectivity and dispersal strategies on the spatial distribution of their genetic diversity. We found a significant imprint of the effects of riverine network connectivity on the local and global genetic diversity of both amphipod species. Data from 95 sites showed that allelic richness significantly increased towards more central nodes of the network. This was also seen for observed heterozygosity, yet not for expected heterozygosity. Genetic differentiation increased with instream distance. In simulation models, depending on the mutational model assumed, upstream movement probability and dispersal rate, respectively, emerged as key factors explaining the empirically observed distribution of local genetic diversity and genetic differentiation. Surprisingly, the role of site-specific carrying capacities, for example by assuming a direct dependency of population size on local river size, was less clear cut: while our best fitting model scenario included this feature, over all simulations, scaling of carrying capacities did not increase data-model fit. This highlights the importance of dispersal behaviour along spatial networks in shaping population genetic diversity.

Parasitism and host dispersal plasticity in an aquatic model system.

Dispersal is a central determinant of spatial dynamics in communities and ecosystems, and various ecological factors can shape the evolution of constitutive and plastic dispersal behaviours. One important driver of dispersal plasticity is the biotic environment. Parasites, for example, influence the internal condition of infected hosts and define external patch quality. Thus, state-dependent dispersal may be determined by infection status and context-dependent dispersal by the abundance of infected hosts in the population. A prerequisite for such dispersal plasticity to evolve is a genetic basis on which natural selection can act. Using interconnected microcosms, we investigated dispersal in experimental populations of the freshwater protist Paramecium caudatum in response to the bacterial parasite Holospora undulata. For a collection of 20 natural host strains, we found substantial variation in constitutive dispersal and to a lesser degree in dispersal plasticity. First, infection tended to increase or decrease dispersal relative to uninfected controls, depending on strain identity, indicative of state-dependent dispersal plasticity. Infection additionally decreased host swimming speed compared to the uninfected counterparts. Second, for certain strains, there was a weak negative association between dispersal and infection prevalence, such that uninfected hosts dispersed less when infection was more frequent in the population, indicating context-dependent dispersal plasticity. Future experiments may test whether the observed differences in dispersal plasticity are sufficiently strong to be picked up by natural selection. The evolution of dispersal plasticity as a strategy to mitigate parasite effects spatially may have important implications for epidemiological dynamics.

Nonlinear Effects of Intraspecific Competition Alter Landscape-Wide Scaling Up of Ecosystem Function.

A major focus of ecology is to understand and predict ecosystem function across scales. Many ecosystem functions are measured only at local scales, while their effects occur at a landscape level. Here we investigate how landscape-scale predictions of ecosystem function depend on intraspecific competition, a fine-scale process, by manipulating intraspecific density of shredding macroinvertebrates and examining effects on leaf litter decomposition, a key function in freshwater ecosystems. For two species, we found that per capita leaf processing rates declined with increasing density following power functions with negative exponents, likely due to interference competition. To demonstrate consequences of this nonlinearity, we scaled up estimates of leaf litter processing from shredder abundance surveys in 10 replicated headwater streams. In accordance with Jensen's inequality, applying density-dependent consumption rates reduced estimates of catchment-scale leaf consumption by an order of magnitude relative to density-independent rates. Density-dependent consumption estimates aligned closely with metabolic requirements in catchments with large-but not small-shredder populations. Importantly, shredder abundance was not limited by leaf litter availability, and catchment-level leaf litter supply was much higher than estimated consumption. Thus leaf litter processing was not limited by resource supply. Our work highlights the need for scaling up, which accounts for intraspecific interactions.

Evolution in interacting species alters predator life-history traits, behaviour and morphology in experimental microbial communities.

Predator-prey interactions heavily influence the dynamics of many ecosystems. An increasing body of evidence suggests that rapid evolution and coevolution can alter these interactions, with important ecological implications, by acting on traits determining fitness, including reproduction, anti-predatory defence and foraging efficiency. However, most studies to date have focused only on evolution in the prey species, and the predator traits in (co)evolving systems remain poorly understood. Here, we investigated changes in predator traits after approximately 600 generations in a predator-prey (ciliate-bacteria) evolutionary experiment. Predators independently evolved on seven different prey species, allowing generalization of the predator's evolutionary response. We used highly resolved automated image analysis to quantify changes in predator life history, morphology and behaviour. Consistent with previous studies, we found that prey evolution impaired growth of the predator, although the effect depended on the prey species. By contrast, predator evolution did not cause a clear increase in predator growth when feeding on ancestral prey. However, predator evolution affected morphology and behaviour, increasing size, speed and directionality of movement, which have all been linked to higher prey search efficiency. These results show that in (co)evolving systems, predator adaptation can occur in traits relevant to foraging efficiency without translating into an increased ability of the predator to grow on the ancestral prey type.

Gene swamping alters evolution during range expansions in the protist Tetrahymena thermophila.

At species' range edges, individuals often face novel environmental conditions that may limit range expansion until populations adapt. The potential to adapt depends on genetic variation upon which selection can act. However, populations at species' range edges are often genetically depauperate. One mechanism increasing genetic variation is reshuffling existing variation through sex. Sex, however, can potentially limit adaptation by breaking up existing beneficial allele combinations (recombination load). The gene swamping hypothesis predicts this is specifically the case when populations expand along an abiotic gradient and asymmetric dispersal leads to numerous maladapted dispersers from the range core swamping the range edge. We used the ciliate Tetrahymena thermophila as a model for testing the gene swamping hypothesis. We performed replicated range expansions in landscapes with or without a pH-gradient, while simultaneously manipulating the occurrence of gene flow and sexual versus asexual reproduction. We show that sex accelerated evolution of local adaptation in the absence of gene flow, but hindered it in the presence of gene flow. However, sex affected adaptation independently of the pH-gradient, indicating that both abiotic gradients and the biotic gradient in population density lead to gene swamping. Overall, our results show that gene swamping alters adaptation in life-history strategies.

Dispersal syndromes can impact ecosystem functioning in spatially structured freshwater populations.

Dispersal can strongly influence ecological and evolutionary dynamics. Besides the direct contribution of dispersal to population dynamics, dispersers often differ in their phenotypic attributes from non-dispersers, which leads to dispersal syndromes. The consequences of such dispersal syndromes have been widely explored at the population and community level; however, to date, ecosystem-level effects remain unclear. Here, we examine whether dispersing and resident individuals of two different aquatic keystone invertebrate species have different contributions to detrital processing, a key function in freshwater ecosystems. Using experimental two-patch systems, we found no difference in leaf consumption rates with dispersal status of the common native species Gammarus fossarum. In Dikerogammarus villosus, however, a Ponto-Caspian species now expanding throughout Europe, dispersers consumed leaf litter at roughly three times the rate of non-dispersers. Furthermore, this put the contribution of dispersing D. villosus to leaf litter processing on par with native G. fossarum, after adjusting for differences in organismal size. Given that leaf litter decomposition is a key function in aquatic ecosystems, and the rapid species turnover in freshwater habitats with range expansions of non-native species, this finding suggests that dispersal syndromes may have important consequences for ecosystem functioning.

Kin competition accelerates experimental range expansion in an arthropod herbivore.

With ongoing global change, life is continuously forced to move to novel areas, which leads to dynamically changing species ranges. As dispersal is central to range dynamics, factors promoting fast and distant dispersal are key to understanding and predicting species ranges. During range expansions, genetic variation is depleted at the expanding front. Such conditions should reduce evolutionary potential, while increasing kin competition. Organisms able to recognise relatives may be able to assess increased levels of relatedness at expanding range margins and to increase their dispersal in a plastic manner. Using individual-based simulations and experimental range expansions of a spider mite, we demonstrate that plastic responses to kin structure can be at least as important as evolution in driving range expansion speed. Because recognition of kin or kind is increasingly documented across the tree of life, we anticipate it to be a highly important but neglected driver of range expansions.

Disturbance reverses classic biodiversity predictions in river-like landscapes.

Global analyses of biodiversity consistently reveal recurrent patterns of species distributions worldwide. However, unveiling the specific mechanisms behind those patterns remains logistically challenging, yet necessary for reliable biodiversity forecasts. Here, we combine theory and experiments to investigate the processes underlying spatial biodiversity patterns in dendritic, river-like landscapes, iconic examples of highly threatened ecosystems. We used geometric scaling properties, common to all rivers, to show that the distribution of biodiversity in these landscapes fundamentally depends on how ecological selection is modulated across space: while uniform ecological selection across the network leads to higher diversity in downstream confluences, this pattern can be inverted by disturbances when population turnover (i.e. local mortality) is higher upstream than downstream. Higher turnover in small headwater patches can slow down ecological selection, increasing local diversity in comparison to large downstream confluences. Our results show that disturbance-mediated slowing down of competitive exclusion can generate a specific transient signature in terms of biodiversity distribution when applied over a spatial gradient of disturbance, which is a common feature of many river landscapes.