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 (CT ) 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 CT . We found a higher CT 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 CT . 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.
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.
Please cite this article in press as: Tü zü n N, Stoks R: Evolution of geographic variation in thermal performance curves in the face of climate change and implications for biotic interactions, Curr Opin Insect Sci (2018),
• We tested for effects of urbanisation on vulnerability to chlorpyrifos in a damselfly.• Behavioural responses to chlorpyrifos differed between urban and rural populations.• Exposed rural larvae decreased activity and feeding at 20• C and 24• C.• Exposed urban larvae increased activity and only reduced feeding at 24• C.• Results suggest local adaptation to higher pesticide levels in urban populations.Please cite this article in press as: Tüzün, N. The degree of urbanisation is rapidly increasing worldwide. Due to anthropogenic impact, urban populations are exposed to higher levels of contaminants and higher temperatures. Despite this, urbanisation is a largely overlooked spatial component in ecotoxicology. We tested in a common garden rearing experiment whether replicated urban and rural populations of the damselfly Coenagrion puella differ in their vulnerability to sublethal levels of a widespread pesticide, chlorpyrifos, in terms of ecologically relevant behaviours (exploration behaviour, activity, boldness and food intake), and to what extent these patterns are affected by temperature (20 and 24• C). Except boldness, all behaviours were affected by previous pesticide exposure. While the pesticide did not affect exploration behaviour at 20• C, it was associated with increased exploration at 24• C, which may reflect an increased toxicity of chlorpyrifos at higher temperatures. Importantly, rural and urban larvae showed consistently different, sometimes even opposite behavioural responses to pesticide exposure. When exposed to the pesticide, rural larvae decreased activity and food intake at both temperatures; urban larvae instead increased activity at both temperatures and only reduced food intake at the high temperature. This suggests that urban larvae were less affected by the pesticide, which would be consistent with a scenario of local adaptation to higher contaminant levels. Our results highlight that urbanisation may be an important factor to arrive at a spatially explicit ecological risk assessment, and may be an ignored reason why studies on the same species may generate widely different vulnerabilities to pesticides.
How thermal evolution may affect trophic interactions and its implications for trophic system stability remains unstudied. To advance insights in how global warming shapes trophic interactions, we need to consider besides increases in mean temperatures, also daily thermal fluctuations (DTF) and heat waves (HW), and how their effects are modulated by thermal evolution. Using a common‐garden approach, we tested how each thermal factor affected predator metabolic rate and functional response parameters, and used these responses to predict long‐term predator–prey interaction strength between larvae of the damselfly Ischnura elegans and the water flea Daphnia magna. Using high‐ and low‐latitude predator populations with the latter being exposed to higher mean temperatures, higher DTF and more frequent HW, we assessed the potential impact of thermal evolution at the high latitude using a space‐for‐time substitution. In line with thermal adaptation, growth rates were faster and handling times shorter in low‐latitude compared to high‐latitude larvae at 24°C while the opposite was true at 20°C. Warming weakened the long‐term interaction strength, except for the high‐latitude trophic system at DTF and HW where plastic responses therefore may not stabilize the high‐latitude system. This extends the emerging insight that temperature variation may make ectotherms more vulnerable to warming. The contributions of metabolic rate, search rate and handling time in shaping thermal effects on interaction strength differed between latitudes. A key finding was that thermal evolution may further weaken the long‐term interaction strength of the high‐latitude trophic system under increases in mean temperatures, even at DTF and potentially also at HW. Our results underscore the importance of daily thermal fluctuations and heat waves in shaping predator–prey interactions, and may suggest an overall stabilizing contribution of predator thermal evolution ameliorating thermal plastic effects on food web stability. A free Plain Language Summary can be found within the Supporting Information of this article.
Urbanization is among the most important and globally rapidly increasing anthropogenic processes and is known to drive rapid evolution. Habitats in urbanized areas typically consist of small, fragmented and isolated patches, which are expected to select for a better locomotor performance, along with its underlying morphological traits. This, in turn, is expected to cause differentiation in selection regimes, as populations with different frequency distributions for a given trait will span different parts of the species’ fitness function. Yet, very few studies considered differentiation in phenotypic traits associated with patterns in habitat fragmentation and isolation along urbanization gradients, and none considered differentiation in sexual selection regimes. We investigated differentiation in flight performance and flight‐related traits and sexual selection on these traits across replicated urban and rural populations of the scrambling damselfly Coenagrion puella. To disentangle direct and indirect paths going from phenotypic traits over performance to mating success, we applied a path analysis approach. We report for the first time direct evidence for the expected better locomotor performance in urban compared to rural populations. This matches a scenario of spatial sorting, whereby only the individuals with the best locomotor abilities colonize the isolated urban populations. The covariation patterns and causal relationships among the phenotypic traits, performance and mating success strongly depended on the urbanization level. Notably, we detected sexual selection for a higher flight endurance only in urban populations, indicating that the higher flight performance of urban males was reinforced by sexual selection. Taken together, our results provide a unique proof of the interplay between sexual selection and adaptation to human‐altered environments.
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