Pollution offsets the rapid evolution of increased heat tolerance in a natural population.

Despite the increasing evidence for rapid thermal evolution in natural populations, evolutionary rescue under global warming may be constrained by the presence of other stressors. Highly relevant in our polluted planet, is the largely ignored evolutionary trade-off between heat tolerance and tolerance to pollutants. By using two subpopulations (separated 40 years in time) from a resurrected natural population of the water flea Daphnia magna that experienced a threefold increase in heat wave frequency during this period, we tested whether rapid evolution of heat tolerance resulted in reduced tolerance to the widespread metal zinc and whether this would affect heat tolerance upon exposure to the pollutant. Our results revealed rapid evolution of increased heat tolerance in the recent subpopulation. Notably, the sensitivity to the metal tended to be stronger (reduction in net energy budget) or was only present (reductions in heat tolerance and in sugar content) in the recent subpopulation. As a result, the rapidly evolved higher heat tolerance of the recent subpopulation was fully offset when exposed to zinc. Our results highlight that the many reports of evolutionary rescue to global change stressors may give a too optimistic view as our warming planet is polluted by metals and other pollutants.

Weak effect of urbanization on bdelloid rotifers living in lichens.

Human activities have an overwhelming impact on the natural environment, leading to a deep biodiversity crisis whose effects range from genes to ecosystems. Here, we analysed the effect of such anthropogenic impacts on bdelloid rotifers (Rotifera Bdelloidea), for whom these effects are poorly understood. We targeted bdelloid rotifers living in lichen patches across urbanization gradients in Flanders and Brussels (Belgium). Urbanization was measured as the percentage of built-up area (BU) across different spatial scales, at circles from 50 to 3200 m of radius around the lichen. Urbanization effects on biodiversity were assessed on abundance, species richness and community-weighted mean body size of bdelloid rotifers, as well as on genetic diversity of a mitochondrial marker (cytochrome c oxidase subunit I) of one of the most common and widespread bdelloid species, Adineta vaga. Overall, no negative effect of urbanization was found at any diversity level and any spatial scale. Counterintuitively, the BU area quantified at the largest spatial scale had a positive effect on abundance. These results leave open the question of whether negative effects of urbanization are present for bdelloid rotifers, if they are mediated by other unexplored drivers, or if such effects are only visible at even larger spatial scales.

Regional and fine-scale local adaptation in salinity tolerance in Daphnia inhabiting contrasting clusters of inland saline waters.

Understanding the spatial scales at which organisms can adapt to strong natural and human-induced environmental gradients is important. Salinization is a key threat to biodiversity, ecosystem functioning and the provision of ecosystem services of freshwater systems. Clusters of naturally saline habitats represent ideal test cases to study the extent and scale of local adaptation to salinization. We studied local adaptation of the water flea Daphnia magna, a key component of pond food webs, to salinity in two contrasting landscapes-a dense cluster of sodic bomb crater ponds and a larger-scale cluster of soda pans. We show regional differentiation in salinity tolerance reflecting the higher salinity levels of soda pans versus bomb crater ponds. We found local adaptation to differences in salinity levels at the scale of tens of metres among bomb crater pond populations but not among geographically more distant soda pan populations. More saline bomb crater ponds showed an upward shift of the minimum salt tolerance observed across clones and a consequent gradual loss of less tolerant clones in a nested pattern. Our results show evolutionary adaptation to salinity gradients at different spatial scales, including fine-tuned local adaptation in neighbouring habitat patches in a natural landscape.

Hierarchical eco-evo dynamics mediated by the gut microbiome.

The concept of eco-evolutionary (eco-evo) dynamics, stating that ecological and evolutionary processes occur at similar time scales and influence each other, has contributed to our understanding of responses of populations, communities, and ecosystems to environmental change. Phenotypes, central to these eco-evo processes, can be strongly impacted by the gut microbiome. The gut microbiome shapes eco-evo dynamics in the host community through its effects on the host phenotype. Complex eco-evo feedback loops between the gut microbiome and the host communities might thus be common. Bottom-up dynamics occur when eco-evo interactions shaping the gut microbiome affect host phenotypes with consequences at population, community, and ecosystem levels. Top-down dynamics occur when eco-evo dynamics shaping the host community structure the gut microbiome.

Pesticide exposure enhances dominance patterns in a zooplankton community.

Exposure to pesticides can profoundly alter community dynamics. It is expected that dominance patterns will be enhanced or reduced depending on whether the dominant species is less or more sensitive to the pesticide than the subdominant species. Community dynamics are, however, also determined by processes linked to population growth as well as competition at carrying capacity. Here, we used a mesocosm experiment to quantify the effect of chlorpyrifos exposure on the population dynamics of four cladoceran species (Daphnia magna, Daphnia pulicaria, Daphnia galeata and Scapholeberis mucronata) in mixed cultures, testing for direct effects of chlorpyrifos and indirect effects mediated by interactions with other species on the timing of population growth and dominance at carrying capacity. We also quantified whether the pesticide-induced changes in community dynamics affected top-down control of phytoplankton. By adding a treatment in which we used different genotype combinations of each species, we also tested to what extent genetic composition affects community responses to pesticide exposure. Immobilization tests showed that D. magna is the least sensitive to chlorpyrifos of the tested species. Chlorpyrifos exposure first leads to a reduction in the abundance of D. galeata to the benefit of D. pulicaria, and subsequently to a reduction in densities of D. pulicaria to the benefit of D. magna. This resulted in D. magna being more dominant in the pesticide than in the control treatment by the end of the experiment. There was no effect of genotypic differences on community patterns, and top-down control of phytoplankton was high in all treatments. Our results suggest that in this community dominance patterns are enhanced in line with the observed among-species differences in sensitivity to the pesticide. Our results also show that the development of the community in pesticide treatment is a complex interaction between direct and indirect effects of the pesticide.

Intraspecific genetic variation is critical to robust toxicological predictions of aquatic contaminants.

Environmental risk assessment is a critical tool for protecting aquatic life and its effectiveness is predicated on predicting how natural populations respond to contaminants. Yet, routine toxicity testing typically examines only one genotype, which may render risk assessments inaccurate as populations are most often composed of genetically distinct individuals. To determine the importance of intraspecific variation in the translation of toxicity testing to populations, we quantified the magnitude of genetic variation within 20 Daphnia magna clones derived from one lake using whole genome sequencing and phenotypic assays. We repeated these assays across two exposure levels of microcystins, a cosmopolitan and lethal aquatic contaminant produced by harmful algal blooms. We found considerable intraspecific genetic variation in survival, growth, and reproduction, which was amplified by microcystins exposure. Finally, using simulations we demonstrate that the common practice of employing a single genotype to calculate toxicity tolerance failed to produce an estimate within the 95% confidence interval over half of the time. These results illuminate the importance of incorporating intraspecific genetic variation into toxicity testing to reliably predict how natural populations will respond to aquatic contaminants.

The role of prey and predator identity in eliciting inducible defenses of Daphnia.

Predators can modify population and community dynamics not only through direct predation, but also through nonconsumptive effects. Predator-induced changes in the traits of prey species are important components of these nonconsumptive effects. While these are well studied in simplified one-predator one-prey settings, relatively little is known about how kairomones act on prey across heterogeneous aquatic ecosystems with diverse identities of predator and prey. Kairomones are, to some extent, predator specific, and can be classified as diet dependent or diet independent. This classification depends on whether the identity of the prey plays a role in eliciting a defense response. In an effort to elucidate how prey and predator identity determines the defense responses in water fleas, we used inducible morphology and life history traits of Daphnia mitsukuri as a model to systematically explore to what extent predator and prey identity, and species composition of the prey community determined the expression of inducible defenses, and to what extent predator-induced responses differed among genotypes. Our results showed that the defense responses of D. mitsukuri mainly relied on diet-dependent kairomones, which were not influenced by fish species identity but were highly dependent on the phylogenetic distances between D. mitsukuri and the prey ingested by fish. This phylogenetic signal is strong, with D. mitsukuri responding only to the kairomones of fish that feed on cladocerans. We also found that the amplitude of the responses to fish kairomones increased with the amount of cladoceran in the dietary community. We observed significant differences in defensive traits among three D. mitsukuri genotypes, but the differences were minor compared with the effects of kairomones themselves. The results of our systematic analyses point to the role of prey phylogeny in eliciting inducible defenses of D. mitsukuri, thereby enriching our understanding of nonconsumptive effects in aquatic ecosystems.

Rapid evolution of unimodal but not of linear thermal performance curves in Daphnia magna.

Species may cope with warming through both rapid evolutionary and plastic responses. While thermal performance curves (TPCs), reflecting thermal plasticity, are considered powerful tools to understand the impact of warming on ectotherms, their rapid evolution has been rarely studied for multiple traits. We capitalized on a 2-year experimental evolution trial in outdoor mesocosms that were kept at ambient temperatures or heated 4°C above ambient, by testing in a follow-up common-garden experiment, for rapid evolution of the TPCs for multiple key traits of the water flea Daphnia magna. The heat-selected Daphnia showed evolutionary shifts of the unimodal TPCs for survival, fecundity at first clutch and intrinsic population growth rate toward higher optimum temperatures, and a less pronounced downward curvature indicating a better ability to keep fitness high across a range of high temperatures. We detected no evolution of the linear TPCs for somatic growth, mass and development rate, and for the traits related to energy gain (ingestion rate) and costs (metabolic rate). As a result, also the relative thermal slope of energy gain versus energy costs did not vary. These results suggest the overall (rather than per capita) top-down impact of D. magna may increase under rapid thermal evolution.

Dispersal capacity underlies scale-dependent changes in species richness patterns under human disturbance.

Changes in the species richness of (meta-)communities emerge from changes in the relative species abundance distribution (SAD), the total density of individuals, and the amount of spatial aggregation of individuals from the same species. Yet, how human disturbance affects these underlying diversity components at different spatial scales and how this interacts with important species traits, like dispersal capacity, remain poorly understood. Using data of carabid beetle communities along a highly replicated urbanization gradient, we reveal that species richness in urban sites was reduced due to a decline in individual density as well as changes in the SAD at both small and large spatial scales. Changes in these components of species richness were linked to differential responses of groups of species that differ in dispersal capacity. The individual density effect on species richness was due to a drastic 90% reduction of low-dispersal individuals in more urban sites. Conversely, the decrease in species richness due to changes in the SAD at large (i.e., loss of species from the regional pool) and small (i.e., decreased evenness) spatial scales were driven by species with intermediate and high dispersal ability, respectively. These patterns coincide with the expected responses of these dispersal-type assemblages toward human disturbance, namely, (i) loss of low-dispersal species by local extinction processes, (ii) loss of higher-dispersal species from the regional species pool due to decreased habitat diversity, and (iii) dominance of a few highly dispersive species resulting in a decreased evenness. Our results demonstrate that dispersal capacity plays an essential role in determining scale-dependent changes in species richness patterns. Incorporating this information improves our mechanistic insight into how environmental change affects species diversity at different spatial scales, allowing us to better forecast how human disturbance will drive local and regional changes in biodiversity patterns.

Bacterioplankton Assembly Along a Eutrophication Gradient Is Mainly Structured by Environmental Filtering, Including Indirect Effects of Phytoplankton Composition.

Biotic interactions are suggested to be key factors structuring bacterioplankton community assembly but are rarely included in metacommunity studies. Eutrophication of ponds and lakes provides a useful opportunity to evaluate how bacterioplankton assembly is affected by specific environmental conditions, especially also by biotic interactions with other trophic levels such as phytoplankton and zooplankton. Here, we evaluated the importance of deterministic and stochastic processes on bacterioplankton community assembly in 35 shallow ponds along a eutrophication gradient in Belgium and assessed the direct and indirect effects of phytoplankton and zooplankton community variation on bacterioplankton assembly through a path analysis and network analysis. Environmental filtering by abiotic factors (suspended matter concentration and pH) explained the largest part of the bacterioplankton community variation. Phytoplankton community structure affected bacterioplankton structure through its effect on variation in chlorophyll-a and suspended matter concentration. Bacterioplankton communities were also spatially structured through pH. Overall, our results indicate that environmental variation is a key component driving bacterioplankton assembly along a eutrophication gradient and that indirect biotic interactions can also be important in explaining bacterioplankton community composition. Furthermore, eutrophication led to divergence in community structure and more eutrophic ponds had a higher diversity of bacteria.

Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magna.

Exposure to pesticides can have detrimental effects on aquatic communities of non-target species. Populations can evolve tolerance to pesticides which may rescue them from extinction. However, the evolution of tolerance does not always occur and insights in the underlying mechanisms are scarce. One understudied mechanism to obtain pesticide tolerance in hosts are shifts toward pesticide-degrading bacteria in their microbiome. We carried out experimental evolution trials where replicated experimental populations of the water flea Daphnia magna were exposed to the pesticide chlorpyrifos or a solvent control, after which we performed acute toxicity assays to evaluate the evolution of chlorpyrifos tolerance. Additionally, we quantified changes in the microbiota community composition of whole body and gut samples to assess which sample type best reflected the pesticide tolerance of the Daphnia host. As expected, chlorpyrifos-selected clones became more tolerant to chlorpyrifos as shown by the higher EC5048 h (36% higher) compared with the control clones. This was associated with shifts in the microbiome composition whereby the abundance of known organophosphate-degrading bacterial genera increased on average ~4 times in the chlorpyrifos-selected clones. Moreover, the abundances of several genera, including the organophosphate-degrading bacteria Pseudomonas, Flavobacterium and Bacillus, were positively correlated with the EC5048 h of the host populations. These shifts in bacterial genera were similar in magnitude in whole body and gut samples, yet the total abundance of organophosphate-degrading bacteria was ~6 times higher in the whole body samples, suggesting that the gut is not the only body part where pesticide degradation by the microbiome occurs. Our results indicate that the microbiome is an important mediator of the development of tolerance to pesticides in Daphnia.

Scared to evolve? Non-consumptive effects drive rapid adaptive evolution in a natural prey population.

Predators can strongly influence prey populations through both consumptive and non-consumptive effects. Nevertheless, most studies have focused on the consumptive effects in driving evolutionary changes. By integrating experimental evolution and resurrection ecology, we tested the roles of non-consumptive and consumptive effects in driving evolution in a Daphnia magna population that experienced strong changes in fish predation pressure. All resurrected genotypes were pooled, inoculated in outdoor mesocosms, and exposed to free-fish or caged-fish treatments. Non-consumptive effects induced rapid, repeatable changes in the clonal composition and associated genotypic trait changes that were similar in magnitude and direction to those imposed by killing. Both non-consumptive and consumptive effects caused a shift towards a dominance of the high-fish period clones that can perform better under fish predation, and this may be explained by the higher intrinsic growth rate of the high-fish period clones under predation risk. The genotypic trait changes (e.g. reduced body sizes, earlier maturation, more and smaller offspring) of the Daphnia in the mesocosm experiments were in the same direction as the adaptive trait shifts observed in situ through resurrection ecology. Our results demonstrate that non-consumptive effects can induce rapid adaptive evolution and may represent an overlooked driver of eco-evolutionary dynamics.

Accounting for temporal change in multiple biodiversity patterns improves the inference of metacommunity processes.

In metacommunity ecology, a major focus has been on combining observational and analytical approaches to identify the role of critical assembly processes, such as dispersal limitation and environmental filtering, but this work has largely ignored temporal community dynamics. Here, we develop a "virtual ecologist" approach to evaluate assembly processes by simulating metacommunities varying in three main processes: density-independent responses to abiotic conditions, density-dependent biotic interactions, and dispersal. We then calculate a number of commonly used summary statistics of community structure in space and time and use random forests to evaluate their utility for inferring the strength of these three processes. We find that (i) both spatial and temporal data are necessary to disentangle metacommunity processes based on the summary statistics we test, and including statistics that are measured through time increases the explanatory power of random forests by up to 59% compared to cases where only spatial variation is considered; (ii) the three studied processes can be distinguished with different descriptors; and (iii) each summary statistic is differently sensitive to temporal and spatial sampling effort. Including repeated observations of metacommunities over time was essential for inferring the metacommunity processes, particularly dispersal. Some of the most useful statistics include the coefficient of variation of species abundances through time and metrics that incorporate variation in the relative abundances (evenness) of species. We conclude that a combination of methods and summary statistics is probably necessary to understand the processes that underlie metacommunity assembly through space and time, but we recognize that these results will be modified when other processes or summary statistics are used.

Cryptic eco-evolutionary feedback in the city: Urban evolution of prey dampens the effect of urban evolution of the predator.

Most research on eco-evolutionary feedbacks focuses on ecological consequences of evolution in a single species. This ignores the fact that evolution in response to a shared environmental factor in multiple species involved in interactions could alter the net cumulative effect of evolution on ecology. We empirically tested whether urbanization-driven evolution in a predator (nymphs of the damselfly Ischnura elegans) and its prey (the water flea Daphnia magna) jointly shape the outcome of predation under simulated heatwaves. Both interactors show genetic trait adaptation to urbanization, particularly to higher temperatures. We cross-exposed common-garden reared damselflies and Daphnia from replicated urban and rural populations, and quantified predation rates and functional response traits. Urban damselfly nymphs showed higher encounter and predation rates than rural damselflies when exposed to rural prey, but this difference disappeared when they preyed on urban Daphnia. This represents a case of a cryptic evo-to-eco feedback, where the evolution of one species dampens the effects of the evolution of another species on their interaction strength. The effects of evolution of each single species were strong: the scenario in which only the predator or prey was adapted to urbanization resulted in a c. 250% increase in encounter rate and a c. 25% increase in predation rate, compared to the rural predator-rural prey combination. Our results provide unique evidence for eco-evolutionary feedbacks in cities, and underscore the importance of a multi-species approach in eco-evolutionary dynamics research.

A global agenda for advancing freshwater biodiversity research.

Global freshwater biodiversity is declining dramatically, and meeting the challenges of this crisis requires bold goals and the mobilisation of substantial resources. While the reasons are varied, investments in both research and conservation of freshwater biodiversity lag far behind those in the terrestrial and marine realms. Inspired by a global consultation, we identify 15 pressing priority needs, grouped into five research areas, in an effort to support informed stewardship of freshwater biodiversity. The proposed agenda aims to advance freshwater biodiversity research globally as a critical step in improving coordinated actions towards its sustainable management and conservation.

Adaptive Evolution Can Both Prevent Ecosystem Collapse and Delay Ecosystem Recovery.

AbstractThere is growing concern about the dire socioecological consequences of abrupt transitions between alternative ecosystem states in response to environmental changes. At the same time, environmental change can trigger evolutionary responses that could stabilize or destabilize ecosystem dynamics. However, we know little about how coupled ecological and evolutionary processes affect the risk of transition between alternative ecosystem states. Using shallow lakes as a model ecosystem, we investigate how trait evolution of a key species affects ecosystem resilience under environmental stress. We find that adaptive evolution of macrophytes can increase ecosystem resilience by shifting the critical threshold, which marks the transition from a clear-water state to a turbid-water state to a higher level of environmental stress. However, following the transition, adaptation to the turbid-water state can delay the ecosystem recovery back to the clear-water state. This implies that restoration could be more effective when implemented early enough after a transition occurs and before organisms adapt to the alternative state. Our findings provide new insights into how to prevent and mitigate the occurrence of regime shifts in ecosystems and highlight the need to understand ecosystem responses to environmental change in the context of coupled ecological and evolutionary processes.

Differential local genetic adaptation to pesticide use in organic and conventional agriculture in an aquatic non-target species.

Pesticide application is an important stressor to non-target species and can profoundly affect ecosystem functioning. Debates continue on the choice of agricultural practices regarding their environmental impact, and organic farming is considered less detrimental compared to conventional practices. Nevertheless, comparative studies on the impacts of both agricultural approaches on the genetic adaptation of non-target species are lacking. We assessed to what extent organic and conventional agriculture elicit local genetic adaptation of populations of a non-target aquatic species, Daphnia magna. We tested for genetic differences in sensitivity of different D. magna populations (n = 7), originating from ponds surrounded by conventional and organic agriculture as well as nature reserves, to pesticides used either in conventional (chlorpyrifos) or organic agriculture (deltamethrin and copper sulfate). The results indicate that D. magna populations differentially adapt to local pesticide use. Populations show increased resistance to chlorpyrifos as the percentage of conventional agriculture in the surrounding landscape increases, whereas populations from organic agriculture sites are more resistant to deltamethrin. While organic agriculture is considered less harmful for non-target species than conventional, both types of agriculture shape the evolution of pesticide resistance in non-target species in a specific manner, reflecting the differences in selection pressure.

Transient Eco-Evolutionary Dynamics and the Window of Opportunity for Establishment of Immigrants.

AbstractTo what extent does landscape genetic structure bear the signature of arrival order of lineages during population assembly? Rapid genetic adaptation of resident populations founded by early colonists to local conditions might prevent establishment of later-arriving lineages, resulting in an evolution-mediated priority effect. This might result in a limited window of opportunity for establishment during which the resident population did not have sufficient time yet to monopolize the patch through local adaptation. The length of this window of opportunity is expected to depend on the degree to which early colonists and immigrants are preadapted to local habitat conditions. We present an intraspecific competition model of the initial transient population and evolutionary dynamics that quantifies the window of opportunity for establishment for asexual species. The model explicitly addresses the long-lasting effects of evolution-mediated priority effects by tracking lineages through time. Our results show that the difference in initial preadaptation between early colonists and late immigrants and the speed of evolution codetermine the window of opportunity for establishment. Our results also suggest that local populations should often be dominated by descendants of just a few early colonist lineages and that landscape genetic structure should often reflect the legacy of colonization history.

Extensive standing genetic variation from a small number of founders enables rapid adaptation in Daphnia.

We lack a thorough understanding of the origin and maintenance of standing genetic variation that enables rapid evolutionary responses of natural populations. Whole genome sequencing of a resurrected Daphnia population shows that standing genetic variation in over 500 genes follows an evolutionary trajectory that parallels the pronounced and rapid adaptive evolution of multiple traits in response to predator-driven natural selection and its subsequent relaxation. Genetic variation carried by only five founding individuals from the regional genotype pool is shown to suffice at enabling the observed evolution. Our results provide insight on how natural populations can acquire the genomic variation, through colonization by a few regional genotypes, that fuels rapid evolution in response to strong selection pressures. While these evolutionary responses in our study population involved hundreds of genes, we observed no evidence of genetic erosion.

Resurrecting the metabolome: Rapid evolution magnifies the metabolomic plasticity to predation in a natural Daphnia population.

Populations rely on already present plastic responses (ancestral plasticity) and evolution (including both evolution of mean trait values, constitutive evolution, and evolution of plasticity) to adapt to novel environmental conditions. Because of the lack of evidence from natural populations, controversy remains regarding the interplay between ancestral plasticity and rapid evolution in driving responses to new stressors. We addressed this topic at the level of the metabolome utilizing a resurrected natural population of the water flea Daphnia magna that underwent a human-caused increase followed by a reduction in predation pressure within ~16 years. Predation risk induced plastic changes in the metabolome which were mainly related to shifts in amino acid and sugar metabolism, suggesting predation risk affected protein and sugar utilization to increase energy supply. Both the constitutive and plastic components of the metabolic profiles showed rapid, probably adaptive evolution whereby ancestral plasticity and evolution contributed nearly equally to the total changes of the metabolomes. The subpopulation that experienced the strongest fish predation pressure and showed the strongest phenotypic response, also showed the strongest metabolomic response to fish kairomones, both in terms of the number of responsive metabolites and in the amplitude of the multivariate metabolomic reaction norm. More importantly, the metabolites with higher ancestral plasticity showed stronger evolution of plasticity when predation pressure increased, while this pattern reversed when predation pressure relaxed. Our results therefore highlight that the evolution in response to a novel pressure in a natural population magnified the metabolomic plasticity to this stressor.