Hibernation Conditions Contribute to the Differential Resistance to Cadmium between Urban and Forest Ant Colonies.

Claudie Doums,Mathieu Molet,Lauren Jacquier,Céline Bocquet

doi:10.3390/ani11041050

Abstract

Simple SummaryThe resistance of organisms to trace metals can have a genetic or a plastic origin. Indeed, differential environmental conditions experienced before the exposure to trace metals could physiologically condition organisms and plastically enhance their subsequent resistance to trace metals. In this study on the ant Temnothorax nylanderi, we investigated whether the better cadmium resistance of urban colonies relative to forest colonies could originate from the distinct hibernation conditions that they experienced prior to cadmium exposure. We compared the ability of urban and forest colonies to resist cadmium depending on whether they had hibernated in their respective urban or forest habitats or under a laboratory common garden setup. We found that urban colonies resisted cadmium better than forest colonies when they had hibernated under a common garden. Surprisingly, this difference was not observed between urban and forest colonies that had hibernated in the field, in contrast with a previous study. One reason may be that winter was particularly mild on the year of our experiment. Our results therefore support the idea that urban colonies are genetically adapted to resist trace metals, but that this adaptation is only revealed under specific environmental conditions.Trace metals such as cadmium are found in high concentrations in urban environments. Animal and plant populations living in heavily contaminated environments could adapt to trace metals exposure. A recent study shows that urban populations of the acorn ant Temnothorax nylanderi are more resistant to cadmium than their forest counterparts. However, this study was performed using field colonies that had just come out of hibernation. Because urban and forest hibernation environments differ, the differential resistance to trace metals may originate either from differential hibernation conditions or from a different resistance baseline to cadmium. In this study, we tested these two hypotheses using laboratory common garden hibernation conditions. We let urban and forest colonies of the ant T. nylanderi hibernate under the same laboratory conditions for four months. After this hibernation period, we also collected field-hibernating colonies and we compared cadmium resistance between urban and forest colonies depending on the hibernation condition. We found a differential response to cadmium under common garden, with urban colonies displaying less larval mortality and lower size reduction of the produced individuals. This suggests a different resistance baseline of urban colonies to cadmium. However, unexpectedly, we did not detect the differential response between urban and forest colonies in the field, suggesting a more complex scenario involving both genetic and environmental influences.

Highlights

Trace metals at high concentrations have negative impacts on wildlife as they affect cellular and physiological processes (DNA damage, higher oxidative stress, brain inflammation [1,2,3]) and life history traits
Common garden experiments prove that the higher resistance to trace metals in populations from heavily contaminated soils is a stable response that is not directly induced by the stressful environment and reflects a different baseline resistance that could result from genetic adaptation
In the ant T. nylanderi, Jacquier et al [28] showed that urban popupopulations are less sensitive to cadmium than their forest counterparts, with a lower lations are less sensitive to cadmium than their forest counterparts, with a lower larvae larvae mortality rate, a lower decrease in emergence rate, and a lower size reduction of lab mortality rate, a lower decrease in emergence rate, and a lower size reduction of lab workworkers when exposed to cadmium

Summary

Introduction

Trace metals at high concentrations have negative impacts on wildlife as they affect cellular and physiological processes (DNA damage, higher oxidative stress, brain inflammation [1,2,3]) and life history traits (body size reduction, decreased birth rate and hatching rate for eggs, higher mortality rate [2,3,4,5,6,7]). In response to metal exposure, some invertebrate populations have higher expression of metallothionein (Orchesella cincta, Collembola [12]) heat shock protein (Chironomus tentans, Diptera [13]) or antioxidant enzymes, more stable expression of calcium-related stress signaling (Lumbricus rubellus, Annelida [14]), and higher secretion or higher turnover of metallothionein protein (Eisenia fetida, Annelida [15], and Hediste diversicolor, Annelida [11]) These effects have been tested on individuals that had been reared under common garden environments in the laboratory [12,13] or on individuals collected in the field one or two weeks before the start of ecotoxicological assays [11,14,15]. This method does not allow for the addressing of the question of a modulation of this genetic adaptation by interactions with environmental conditions

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