Queen Recognition Signals in Two Primitively Eusocial Halictid Bees: Evolutionary Conservation and Caste-Specific Perception

Abstract

Queen signals are known to regulate reproductive harmony within eusocial colonies by influencing worker behavior and ovarian physiology. However, decades of research have resulted in the identification of just a few queen signals, and studies of their mode of action are rare. Our aim was to identify queen recognition signals in the halictid bee Lasioglossum pauxillum and to analyze caste differences in the olfactory perception of queen signals in L. pauxillum and the closely related species L. malachurum. We performed chemical analyses and bioassays to test for caste differences in chemical profiles and worker behavior influenced by queen-specific compounds in L. pauxillum. Our results indicated that caste differences in the chemical profiles were mainly attributable to higher amounts of macrocyclic lactones in queens. Bioassays demonstrated a higher frequency of subordinate behavior in workers elicited by queen-specific amounts of macrocyclic lactones. Thus, macrocyclic lactones function as queen recognition signals in L. pauxillum, as in L. malachurum. Using electrophysiological analyses, we have demonstrated that queens of both tested species lack antennal reactions to certain macrocyclic lactones. Therefore, we assume that this is a mechanism to prevent reproductive self-inhibition in queens. Our results should stimulate debate on the conservation and mode of action of queen signals.

Chemical Variation among Castes, Female Life Stages and Populations of the Facultative Eusocial Sweat Bee Halictus rubicundus (Hymenoptera: Halictidae)

“…Our results also clearly demonstrate that nest foundresses from social and solitary European populations are chemically more similar than social and solitary breeding females or queens. This leads us to the hypothesis that breeding females of social nests exhibit a queen-specific signal of sociality, as was recently shown in another eusocial halictine bee, L. pauxillum (Steitz et al 2019). Even if it is hypothesized that queen signals evolved from chemicals associated with ovarian development (Oi et al 2015;Smith and Liebig 2017;Steitz et al 2018), the occurrence of this social signal in H. rubicundus cannot solely be explained by the development of ovaries, but also seems to be affected by social behavior as solitary breeding females change their odor composition to a different extent.…”

“…In eusocial insects, chemical communication is known to be involved not only in nestmate and kin recognition but also in regulating reproductive division of labor and task allocation of individuals in the society (Ayasse et al 2001 ; Kocher and Grozinger 2011 ; Rottler-Hoermann et al 2016 ; Steitz and Ayasse 2020 ; Steitz et al 2018 , 2019 ). The castes, namely the reproductive queens and the non-reproductive workers, 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 ).…”

“…In eusocial insects, chemical communication is known to be involved not only in nestmate and kin recognition but also in regulating reproductive division of labor and task allocation of individuals in the society (Ayasse et al 2001 ; Kocher and Grozinger 2011 ; Rottler-Hoermann et al 2016 ; Steitz and Ayasse 2020 ; Steitz et al 2018 , 2019 ). The castes, namely the reproductive queens and the non-reproductive workers, 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 ).…”

“…Moreover, n-alkanes and macrocyclic lactones have been found in larger quantities in breeding queens compared with workers in L. malachurum (Ayasse et al 1993 , 1999 ; Steitz et al 2018 ; Steitz and Ayasse 2020 ), though macrocyclic lactones are sufficient to influence worker behavior, distracting workers from activating their ovaries and therefore functioning as a queen signal in this species (Steitz and Ayasse 2020 ). Indeed, macrocyclic lactones are the single compound class which is at higher titer in queens compared to workers in several eusocial halictid bee species, suggesting that it may function as a queen pheromone among several species in this taxon (Steitz et al 2018 , 2019 ). Additionally, queens and workers are chemically more distinct in obligate eusocial compared to socially polymorphic species like H. rubicundus , indicating a more complex caste-specific chemical profile with a more complex degree of social organization in halictid bees (Steitz et al 2018 ).…”

Differential gene expression underlying the biosynthesis of Dufour’s gland signals in Bombus impatiens

“…For instance, hydrocarbons serve primely to prevent insect desiccation (Menzel et al, 2019), but evolved as signals reflecting species, caste, age, task, reproductive and social status in many species (Blomquist & Bagnères, 2010; Derstine, Gries, Zhai, Jimenez, & Gries, 2018; Dietemann, Peeters, Liebig, Thivet, & Holldobler, 2003; Endler et al, 2004; Oi et al, 2015; Smith, Holldober, & Liebig, 2009; Smith, Millar, Hanks, & Suarez, 2013). Likewise, various wax esters comprise the brood pheromone of honey bees (Yves Le Conte, Mohammedi, & Robinson, 2001), and play a role in the reproductive signaling of worker bumble bees (Amsalem, Twele, Francke, & Hefetz, 2009), and macrocyclic lactones (cyclic esters) serve as queen pheromones in halictid bees (Steitz & Ayasse, 2020; Steitz, Brandt, Biefel, Minat, & Ayasse, 2019). Furthermore, the main component of the honey bee queen mandibular pheromone is a fatty acid derived hydroxy-acid which regulates worker reproduction (Erika Plettner, Slessor, & Winston, 1998; Slessor, Kaminski, King, & Winston, 1990).…”