Abstract

In eusocial insects, chemical communication is crucial for mediating many aspects of social activities, especially the regulation of reproduction. Though queen signals are known to decrease ovarian activation of workers in highly eusocial species, little is known about their evolution. In contrast, some primitively eusocial species are thought to control worker reproduction through physical aggression by the queen rather than via pheromones, suggesting the evolutionary establishment of chemical signals with more derived sociality. However, studies supporting this hypothesis are largely missing. Socially polymorphic halictid bees, such as Halictus rubicundus, with social and solitary populations in both Europe and North America, offer excellent opportunities to illuminate the evolution of caste-specific signals. Here we compared the chemical profiles of social and solitary populations from both continents and tested whether (i) population or social level affect chemical dissimilarity and whether (ii) caste-specific patterns reflect a conserved queen signal. Our results demonstrate unique odor profiles of European and North American populations, mainly due to different isomers of n-alkenes and macrocyclic lactones; chemical differences may be indicative of phylogeographic drift in odor profiles. We also found common compounds overproduced in queens compared to workers in both populations, indicating a potential conserved queen signal. However, North American populations have a lower caste-specific chemical dissimilarity than European populations which raises the question if both use different mechanisms of regulating reproductive division of labor. Therefore, our study gives new insights into the evolution of eusocial behavior and the role of chemical communication in the inhibition of reproduction.

Highlights

  • Chemical communication plays a crucial role in insects, especially in taxa that live in social groups

  • We demonstrate that H. rubicundus females from European and North American populations are clearly chemically distinct, independent of their caste or physiological life stage

  • Queens and workers of North American populations could not even be distinguished based on their whole cuticular chemical profile, but only due to the amounts of some single compounds. This may indicate a different importance of inter-caste chemical communication systems between North American and European H. rubicundus populations

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Summary

Introduction

Chemical communication plays a crucial role in insects, especially in taxa that live in social groups. J Chem Ecol (2021) 47:406–419 often differ in their chemical signatures and signals produced by queens or dominant females are thought to regulate many aspects of social behavior and reproduction within the colony (Le Conte and Hefetz 2008; Soro et al 2011; Sramkova et al 2008; Steitz and Ayasse 2020; Steitz et al 2018, 2019; Oi et al 2015) These chemical queen signals are known to decrease the ovarian activity of workers and have been the focus of much attention in various eusocial insect species, especially those with highly developed eusocial behavior (Ayasse and Jarau 2014; Holman et al 2013; Holman et al 2016; Monnin 2006; Oi et al 2015; Smith et al 2012, 2016; Sramkova et al 2008; Van Oystaeyen et al 2014). These species with a higher flexibility of eusocial behavior might better represent the transition from solitary living to eusocial behavior and are highly useful to get insights on this transition

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