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Desiccation Resistance and Micro-Climate Adaptation: Cuticular Hydrocarbon Signatures of Different Argentine Ant Supercolonies Across California

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Abstract

Cuticular hydrocarbons (CHCs), the dominant fraction of the insects’ epicuticle and the primary barrier to desiccation, form the basis for a wide range of chemical signaling systems. In eusocial insects, CHCs are key mediators of nestmate recognition, and colony identity appears to be maintained through a uniform CHC profile. In the unicolonial Argentine ant Linepithema humile, an unparalleled invasive expansion has led to vast supercolonies whose nestmates can still recognize each other across thousands of miles. CHC profiles are expected to display considerable variation as they adapt to fundamentally differing environmental conditions across the Argentine ant’s expanded range, yet this variation would largely conflict with the vastly extended nestmate recognition based on CHC uniformity. To shed light on these seemingly contradictory selective pressures, we attempt to decipher which CHC classes enable adaptation to such a wide array of environmental conditions and contrast them with the overall CHC profile uniformity postulated to maintain nestmate recognition. n-Alkanes and n-alkenes showed the largest adaptability to environmental conditions most closely associated with desiccation, pointing at their function for water-proofing. Trimethyl alkanes, on the other hand, were reduced in environments associated with higher desiccation stress. However, CHC patterns correlated with environmental conditions were largely overriden when taking overall CHC variation across the expanded range of L. humile into account, resulting in conserved colony-specific CHC signatures. This delivers intriguing insights into the hierarchy of CHC functionality integrating both adaptation to a wide array of different climatic conditions and the maintenance of a universally accepted chemical profile.

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Acknowledgements

This work was supported by the US National Science Foundation (IOS-1557934/1557961), USDA National Institute of Food and Agriculture (2016-67013-24749), USDA Hatch Project (CA-B-INS-0087-H), and the UC Berkeley Bakar Fellows program. Furthermore, the authors would like to thank Thomas Schmitt for his valuable help in CHC identification, Katelyn Sanko and Naomichi Yamamoto for assistance in data analysis, Maria A Tonione for support with obtaining, integrating and analyzing climatic data, Mareike Koppik and Maik Bartelheimer for helpful discussions and assistance in statistical analysis and data representation, two anonymous reviewers for their valuable suggestions and input on the first draft of the manuscript, and Wittko Francke for editing the final version of the manuscript.

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Correspondence to Jan Buellesbach.

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The authors declare that they have no competing interests.

Research Involving Human Participants and/or Animals

There is no ethics committee overseeing experimental research on Argentine Ants. However, all efforts were made to treat the animals as humanely as possible.

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Supplementary Fig. 1

Density distributions per identified CHC class, indicating the variance in the data based on the total CHC amounts in the sampled L. humile populations. Results from shapiro-tests for normal distribution in each respective compound class are indicated as well. (PDF 298 kb)

Supplementary Fig. 2

Overview of all individual CHCs for which a significant correlation could be detected with average monthly temperature (in °C, left) as well as average monthly precipitation (in mm, right) per month and collection location for the tested L. humile populations. The main L. humile super colony is indicated in gold, the secondary colonies in shades of blue and violet, different symbols represent the different L. humile populations that were sampled. Only significant correlations (p < 0.05) are shown, which were assessed through Benjamini-Hochberg corrected Spearman rank correlations tests per CHC class (see Supplementary Tab. 1). (PDF 89.4 kb)

Supplementary Table 1

Benjamini-Hochberg corrected Spearman rank correlations test statistics for individual CHCs showing significant correlations with average monthly temperature (left) and with average monthly precipitation (right) across all sampled L. humile populations. Values for ρ (rho) and P are given, CHC IDs include co-eluting trace compounds and their unique retention indices (compare to Fig. 4). (DOCX 14.6 kb)

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Buellesbach, J., Whyte, B.A., Cash, E. et al. Desiccation Resistance and Micro-Climate Adaptation: Cuticular Hydrocarbon Signatures of Different Argentine Ant Supercolonies Across California. J Chem Ecol 44, 1101–1114 (2018). https://doi.org/10.1007/s10886-018-1029-y

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  • DOI: https://doi.org/10.1007/s10886-018-1029-y

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