Abstract

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.

Highlights

  • Humans ubiquitously impact natural ecosystems in various ways (Hendry et al, 2017; Palumbi, 2001)

  • Daphnia survival was impaired by the acute exposure (48h) to the organophosphate pesticide chlorpyrifos compared to the control (−72.8 percentage points)

  • While survival in response to the chlorpyrifos treatment was strongly impacted by the evolutionary urbanization background of the populations, we found no support for urbanization-­driven survival differences at different exposure temperatures (20°C vs. 24°C)

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Summary

Introduction

Humans ubiquitously impact natural ecosystems in various ways (Hendry et al, 2017; Palumbi, 2001). Strong forms of human-­driven land conversion and habitat and microclimate alterations are concerted in cities (Alberti et al, 2020; Grimm et al, 2008; Parris, 2016); urbanization modifies the physical, chemical, and biological characteristics of natural habitats, structurally and functionally changes connectivity patterns among biological communities, induces disturbances of which many are novel (e.g. chemical contaminants and noise), and alters biotic interactions as a consequence of changes in native species composition and the introduction of non-­ native species. A large number of observations of urban evolution focuses on neutral evolution stemming from the impact of habitat fragmentation, among-­ city connectivity hubs, and population size changes on gene flow and genetic drift (Miles et al, 2019; Munshi-­South & Richardson, 2020). Evidence on adaptive evolution in response to urban temperature gradients (e.g. acorn ants: Diamond et al, 2017; Martin et al, 2019; water fleas: Brans et al, 2018; Brans, Jansen, et al, 2017), fragmentation (e.g. holy hawksbeard: Cheptou et al, 2017), and specific chemical pollution (e.g. polychlorinated biphenyl resistance in tomcod: Wirgin et al, 2011; and killifish: Oziolor & Matson, 2018; Whitehead et al, 2012) is growing incessantly

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