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.

A global horizon scan for urban evolutionary ecology.

Research on the evolutionary ecology of urban areas reveals how human-induced evolutionary changes affect biodiversity and essential ecosystem services. In a rapidly urbanizing world imposing many selective pressures, a time-sensitive goal is to identify the emergent issues and research priorities that affect the ecology and evolution of species within cities. Here, we report the results of a horizon scan of research questions in urban evolutionary ecology submitted by 100 interdisciplinary scholars. We identified 30 top questions organized into six themes that highlight priorities for future research. These research questions will require methodological advances and interdisciplinary collaborations, with continued revision as the field of urban evolutionary ecology expands with the rapid growth of cities.

Global urban environmental change drives adaptation in white clover.

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

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.

Genetic differentiation in pesticide resistance between urban and rural populations of a nontarget freshwater keystone interactor, Daphnia magna.

There is growing evidence that urbanization drives adaptive evolution in response to thermal gradients. One such example is documented in the water flea Daphnia magna. However, organisms residing in urban lentic ecosystems are increasingly exposed to chemical pollutants such as pesticides through run-off and aerial transportation. The extent to which urbanization drives the evolution of pesticide resistance in aquatic organisms and whether this is impacted by warming and thermal adaptation remains limitedly studied. We performed a common garden rearing experiment using multiple clonal lineages originating from five replicated urban and rural D. magna populations, in which we implemented an acute toxicity test exposing neonates (<24h) to either a solvent control or the organophosphate pesticide chlorpyrifos. Pesticide exposures were performed at two temperatures (20°C vs. 24°C) to test for temperature-associated differences in urbanization-driven evolved pesticide resistance. We identified a strong overall effect of pesticide exposure on Daphnia survival probability (-72.8 percentage points). However, urban Daphnia genotypes showed higher survival probabilities compared to rural ones in the presence of chlorpyrifos (+29.7 percentage points). Our experiment did not reveal strong temperature x pesticide or temperature x pesticide x urbanization background effects on survival probability. The here observed evolution of resistance to an organophosphate pesticide is a first indication Daphnia likely also adapts to pesticide pollution in urban areas. Increased pesticide resistance could facilitate their population persistence in urban ponds, and feed back to ecosystem functions, such as top-down control of algae. In addition, adaptive evolution of nontarget organisms to pest control strategies and occupational pesticide use may modulate how pesticide applications affect genetic and species diversity in urban areas.

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.

Socio-eco-evolutionary dynamics in cities.

Cities are uniquely complex systems regulated by interactions and feedbacks between nature and human society. Characteristics of human society-including culture, economics, technology and politics-underlie social patterns and activity, creating a heterogeneous environment that can influence and be influenced by both ecological and evolutionary processes. Increasing research on urban ecology and evolutionary biology has coincided with growing interest in eco-evolutionary dynamics, which encompasses the interactions and reciprocal feedbacks between evolution and ecology. Research on both urban evolutionary biology and eco-evolutionary dynamics frequently focuses on contemporary evolution of species that have potentially substantial ecological-and even social-significance. Still, little work fully integrates urban evolutionary biology and eco-evolutionary dynamics, and rarely do researchers in either of these fields fully consider the role of human social patterns and processes. Because cities are fundamentally regulated by human activities, are inherently interconnected and are frequently undergoing social and economic transformation, they represent an opportunity for ecologists and evolutionary biologists to study urban "socio-eco-evolutionary dynamics." Through this new framework, we encourage researchers of urban ecology and evolution to fully integrate human social drivers and feedbacks to increase understanding and conservation of ecosystems, their functions and their contributions to people within and outside cities.

Adaptive Evolution in Cities: Progress and Misconceptions.

Current narratives suggest that urban adaptation - the adaptive evolution of organisms to cities - is pervasive across taxa and cities. However, in reviewing hundreds of studies, we find only six comprehensive examples of species adaptively evolving to urbanization. We discuss the utility and shortcomings of methods for studying urban adaptation. We then review diverse systems offering preliminary evidence for urban adaptation and outline a research program for advancing its study. Urban environments constitute diverse, interacting selective agents that test the limits of adaptation. Understanding urban adaptation therefore offers unique opportunities for addressing fundamental questions in evolutionary biology and for better conserving biodiversity in cities. However, capitalizing on these opportunities requires appropriate research methods and dissemination of accurate narratives.

Urbanization drives cross-taxon declines in abundance and diversity at multiple spatial scales.

The increasing urbanization process is hypothesized to drastically alter (semi-)natural environments with a concomitant major decline in species abundance and diversity. Yet, studies on this effect of urbanization, and the spatial scale at which it acts, are at present inconclusive due to the large heterogeneity in taxonomic groups and spatial scales at which this relationship has been investigated among studies. Comprehensive studies analysing this relationship across multiple animal groups and at multiple spatial scales are rare, hampering the assessment of how biodiversity generally responds to urbanization. We studied aquatic (cladocerans), limno-terrestrial (bdelloid rotifers) and terrestrial (butterflies, ground beetles, ground- and web spiders, macro-moths, orthopterans and snails) invertebrate groups using a hierarchical spatial design, wherein three local-scale (200 m × 200 m) urbanization levels were repeatedly sampled across three landscape-scale (3 km × 3 km) urbanization levels. We tested for local and landscape urbanization effects on abundance and species richness of each group, whereby total richness was partitioned into the average richness of local communities and the richness due to variation among local communities. Abundances of the terrestrial active dispersers declined in response to local urbanization, with reductions up to 85% for butterflies, while passive dispersers did not show any clear trend. Species richness also declined with increasing levels of urbanization, but responses were highly heterogeneous among the different groups with respect to the richness component and the spatial scale at which urbanization impacts richness. Depending on the group, species richness declined due to biotic homogenization and/or local species loss. This resulted in an overall decrease in total richness across groups in urban areas. These results provide strong support to the general negative impact of urbanization on abundance and species richness within habitat patches and highlight the importance of considering multiple spatial scales and taxa to assess the impacts of urbanization on biodiversity.

Freshwater Bacterioplankton Metacommunity Structure Along Urbanization Gradients in Belgium.

Urbanization is transforming and fragmenting natural environments worldwide, driving changes in biological communities through alterations in local environmental conditions as well as by changing the capacity of species to reach specific habitats. While the majority of earlier studies have been performed on higher plants and animals, it is crucial to increase our insight on microbial responses to urbanization across different spatial scales. Here, using a metacommunity approach, we evaluated the effects of urbanization on bacterioplankton communities in 50 shallow ponds in Belgium (Flanders region), one of the most urbanized areas in Northwest Europe. We estimated the relative importance of local environmental factors (35 abiotic and biotic variables), regional spatial factors and urbanization (built-up area) quantified at two spatial scales (200 m × 200 m and 3 km × 3 km). We show that urbanization at local or regional scales did not lead to strong changes in community composition and taxon diversity of bacterioplankton. Urbanization at regional scale (3 km × 3 km) explained only 2% of community composition variation while at local scale (200 m × 200 m), no effect was detected. Local environmental factors explained 13% (OTUs with relative abundance ≥ 0.1%) to 24% (12 dominant OTUs -≥ 1%) of community variation. Six local environmental variables significantly explained variation in bacterioplankton community composition: pH, alkalinity, conductivity, total phosphorus, abundance of Daphnia and concentration of copper (Cu), of which pH was partly mediated by urbanization. Our results indicate that environmental rather than spatial factors accounted for the variation in bacterioplankton community structure, suggesting that species sorting is the main process explaining bacterioplankton community assembly. Apparently, urbanization does not have a direct and strong effect on bacterioplankton metacommunity structure, probably due to the capacity of these organisms to adapt toward and colonize habitats with different environmental conditions and due to their fast adaptation and metabolic versatility. Thus, bacterioplankton communities inhabiting shallow ponds may be less affected by environmental conditions resulting from urbanization as compared to the impacts previously described for other taxa.

Urbanization drives genetic differentiation in physiology and structures the evolution of pace-of-life syndromes in the water flea Daphnia magna.

Natural and human-induced stressors elicit changes in energy metabolism and stress physiology in populations of a wide array of species. Cities are stressful environments that may lead to differential selection on stress-coping mechanisms. Given that city ponds are exposed to the urban heat island effect and receive polluted run-off, organisms inhabiting these ecosystems might show genetic differentiation for physiological traits enabling them to better cope with higher overall stress levels. A common garden study with 62 Daphnia magna genotypes from replicated urban and rural populations revealed that urban Daphnia have significantly higher concentrations of total body fat, proteins and sugars. Baseline activity levels of the antioxidant defence enzymes superoxide dismutase (SOD) and glutathione-S-transferase (GST) were higher in rural compared with city populations, yet urban animals were equally well protected against lipid peroxidation. Our results add to the recent evidence of urbanization-driven changes in stress physiology and energy metabolism in terrestrial organisms. Combining our results with data on urban life history evolution in Daphnia revealed that urban genotypes show a structured pace-of-life syndrome involving both life-history and physiological traits, whereas this is absent in rural populations.

Body-size shifts in aquatic and terrestrial urban communities.

Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes 3 . Urban environments are, however, also characterized by substantial habitat fragmentation 4 , which favours mobile species. Here, using a replicated, spatially nested sampling design across ten animal taxonomic groups, we show that urban communities generally consist of smaller species. In addition, although we show urban warming for three habitat types and associated reduced community-weighted mean body sizes for four taxa, three taxa display a shift to larger species along the urbanization gradients. Our results show that the general trend towards smaller-sized species is overruled by filtering for larger species when there is positive covariation between size and dispersal, a process that can mitigate the low connectivity of ecological resources in urban settings 5 . We thus demonstrate that the urban-heat-island effect and urban habitat fragmentation are associated with contrasting community-level shifts in body size that critically depend on the association between body size and dispersal. Because body size determines the structure and dynamics of ecological networks 1 , such shifts may affect urban ecosystem function.

Genetic adaptation as a biological buffer against climate change: Potential and limitations.

Climate change profoundly impacts ecosystems and their biota, resulting in range shifts, novel interactions, food web alterations, changed intensities of host-parasite interactions, and extinctions. An increasing number of studies have documented evolutionary changes in traits such as phenology and thermal tolerance. In this opinion paper, we argue that, while evolutionary responses have the potential to provide a buffer against extinctions or range shifts, a number of constraints and complexities blur this simple prediction. First, there are limits to evolutionary potential both in terms of genetic variation and demographic effects, and these limits differ strongly among taxa and populations. Second, there can be costs associated with genetic adaptation, such as a reduced evolutionary potential towards other (human-induced) environmental stressors or direct fitness costs due to tradeoffs. Third, the differential capacity of taxa to genetically respond to climate change results in novel interactions because different organism groups respond to a different degree with local compared to regional (dispersal and range shift) responses. These complexities result in additional changes in the selection pressures on populations. We conclude that evolution can provide an initial buffer against climate change for some taxa and populations but does not guarantee their survival. It does not necessarily result in reduced extinction risks across the range of taxa in a region or continent. Yet, considering evolution is crucial, as it is likely to strongly change how biota will respond to climate change and will impact which taxa will be the winners or losers at the local, metacommunity and regional scales.

Microgeographic differentiation in thermal performance curves between rural and urban populations of an aquatic insect.

The rapidly increasing rate of urbanization has a major impact on the ecology and evolution of species. While increased temperatures are a key aspect of urbanization ("urban heat islands"), we have very limited knowledge whether this generates differentiation in thermal responses between rural and urban populations. In a common garden experiment, we compared the thermal performance curves (TPCs) for growth rate and mortality in larvae of the damselfly Coenagrion puella from three urban and three rural populations. TPCs for growth rate shifted vertically, consistent with the faster-slower theoretical model whereby the cold-adapted rural larvae grew faster than the warm-adapted urban larvae across temperatures. In line with costs of rapid growth, rural larvae showed lower survival than urban larvae across temperatures. The relatively lower temperatures hence expected shorter growing seasons in rural populations compared to the populations in the urban heat islands likely impose stronger time constraints to reach a certain developmental stage before winter, thereby selecting for faster growth rates. In addition, higher predation rates at higher temperature may have contributed to the growth rate differences between urban and rural ponds. A faster-slower differentiation in TPCs may be a widespread pattern along the urbanization gradient. The observed microgeographic differentiation in TPCs supports the view that urbanization may drive life-history evolution. Moreover, because of the urban heat island effect, urban environments have the potential to aid in developing predictions on the impact of climate change on rural populations.

The heat is on: Genetic adaptation to urbanization mediated by thermal tolerance and body size.

Worldwide, urbanization leads to tremendous anthropogenic environmental alterations, causing strong selection pressures on populations of animals and plants. Although a key feature of urban areas is their higher temperature ("urban heat islands"), adaptive thermal evolution in organisms inhabiting urban areas has rarely been studied. We tested for evolution of a higher heat tolerance (CTMAX ) in urban populations of the water flea Daphnia magna, a keystone grazer in freshwater ecosystems, by carrying out a common garden experiment at two temperatures (20°C and 24°C) with genotypes of 13 natural populations ordered along a well-defined urbanization gradient. We also assessed body size and haemoglobin concentration to identify underlying physiological drivers of responses in CTMAX . We found a higher CTMAX in animals isolated from urban compared to rural habitats and in animals reared at higher temperatures. We also observed substantial genetic variation in thermal tolerance within populations. Overall, smaller animals were more heat tolerant. While urban animals mature at smaller size, the effect of urbanization on thermal tolerance is only in part caused by reductions in body size. Although urban Daphnia contained higher concentrations of haemoglobin, this did not contribute to their higher CTMAX . Our results provide evidence of adaptive thermal evolution to urbanization in the water flea Daphnia. In addition, our results show both evolutionary potential and adaptive plasticity in rural as well as urban Daphnia populations, facilitating responses to warming. Given the important ecological role of Daphnia in ponds and lakes, these adaptive responses likely impact food web dynamics, top-down control of algae, water quality, and the socio-economic value of urban ponds.

Eco-evolutionary dynamics in urbanized landscapes: evolution, species sorting and the change in zooplankton body size along urbanization gradients.

Urbanization causes both changes in community composition and evolutionary responses, but most studies focus on these responses in isolation. We performed an integrated analysis assessing the relative contribution of intra- and interspecific trait turnover to the observed change in zooplankton community body size in 83 cladoceran communities along urbanization gradients quantified at seven spatial scales (50-3200 m radii). We also performed a quantitative genetic analysis on 12 Daphnia magna populations along the same urbanization gradient. Body size in zooplankton communities generally declined with increasing urbanization, but the opposite was observed for communities dominated by large species. The contribution of intraspecific trait variation to community body size turnover with urbanization strongly varied with the spatial scale considered, and was highest for communities dominated by large cladoceran species and at intermediate spatial scales. Genotypic size at maturity was smaller for urban than for rural D. magna populations and for animals cultured at 24°C compared with 20°C. While local genetic adaptation likely contributed to the persistence of D. magna in the urban heat islands, buffering for the phenotypic shift to larger body sizes with increasing urbanization, community body size turnover was mainly driven by non-genetic intraspecific trait change.This article is part of the themed issue 'Human influences on evolution, and the ecological and societal consequences'.