Larval pheromones act as colony-wide regulators of collective foraging behavior in honeybees

Ma, Rong; Villar, Gabriel; Grozinger, Christina M.; Rangel, Juliana

doi:10.1093/beheco/ary090

Cited by 13 publications

(7 citation statements)

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“…The present study did not measure the aggregate colony-level foraging activity and focused instead on changes in gene expression within individuals. Previous studies demonstrated that larval pheromones increase colony-level pollen foraging behavior using an identical experimental paradigm for pheromone treatments [44–46, 51]. Larval pheromones have the greatest effect on pollen foraging for the first 3 hours following exposure [44], so the present study sampled foragers as they initiated foraging during this critical time window.…”

Section: Discussionmentioning

confidence: 99%

“…Consequently, we seek to more precisely characterize the transcriptional differences associated with rapid, pheromonally-regulated changes in honey bee foraging, and to juxtapose these rapid changes with more stable differences in gene expression associated with task specialization, specifically in integration centers of the brain (i.e., mushroom bodies). Given that foragers have similar behavioral responses to BP and EBO [51], we hypothesized that these two pheromones regulate a common set of foraging genes in the brain (i.e., a foraging “toolkit”). Because BP and EBO have more pronounced effects on pollen foraging than nectar foraging [42, 45], we further hypothesized that larval pheromones affect foragers differentially depending on foraging task specialization.…”

Section: Introductionmentioning

confidence: 99%

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Honey bee (Apis mellifera) larval pheromones may regulate gene expression related to foraging task specialization

Rangel

Grozinger

2019

BMC Genomics

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Background Foraging behavior in honey bees ( Apis mellifera ) is a complex phenotype that is regulated by physiological state and social signals. How these factors are integrated at the molecular level to modulate foraging behavior has not been well characterized. The transition of worker bees from nursing to foraging behaviors is mediated by large-scale changes in brain gene expression, which are influenced by pheromones produced by the queen and larvae. Larval pheromones can also stimulate foragers to leave the colony to collect pollen. However, the mechanisms underpinning this rapid behavioral plasticity in foragers that specialize in collecting pollen over nectar, and how larval pheromones impact these different behavioral states, remains to be determined. Here, we investigated the patterns of gene expression related to rapid behavioral plasticity and task allocation among honey bee foragers exposed to two larval pheromones, brood pheromone (BP) and (E)-beta-ocimene (EBO). We hypothesized that both pheromones would alter expression of genes in the brain related to foraging and would differentially impact brain gene expression depending on foraging specialization. Results Combining data reduction, clustering, and network analysis methods, we found that foraging preference (nectar vs. pollen) and pheromone exposure are each associated with specific brain gene expression profiles. Furthermore, pheromone exposure has a strong transcriptional effect on genes that are preferentially expressed in nectar foragers. Representation factor analysis between our study and previous landmark honey bee transcriptome studies revealed significant overlaps for both pheromone communication and foraging task specialization. Conclusions Our results suggest that, as social signals, pheromones alter expression patterns of foraging-related genes in the bee’s brain to increase pollen foraging at both long and short time scales. These results provide new insights into how social signals and task specialization are potentially integrated at the molecular level, and highlights the possible role that brain gene expression may play in honey bee behavioral plasticity across time scales. Electronic supplementary material The online version of this article (10.1186/s12864-019-5923-7) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Honey bee (Apis mellifera) larval pheromones may regulate gene expression related to foraging task specialization

Rangel

Grozinger

2019

BMC Genomics

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“…While all of these brood-produced compounds consistently elicit nursing responses, there is still much to learn about brood pheromones, as demonstrated by the recent identification of a new compound, allo-ocimene, which may be an additional brood pheromone component (Wu et al, 2019). It is clear that brood pheromones play key roles in determining the resources foraged for by a colony (Traynor et al, 2015;Ma et al, 2016) and in modulating nurse bee physiology and behavior (Traynor et al, 2014(Traynor et al, , 2017Ma et al, 2018Ma et al, , 2019. Although the signals that elicit feeding of queen larvae done by nurse workers has not been thoroughly examined, the duration of nurse visits to feed worker larvae and the signals that mediate the amount and type of feeding are probably similar to those used by nurses to feed queen larvae.…”

Section: Introductionmentioning

confidence: 99%

Pesticide Exposure During Development Does Not Affect the Larval Pheromones, Feeding Rates, or Morphology of Adult Honey Bee (Apis mellifera) Queens

et al. 2021

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Recent work demonstrated that honey bee (Apis mellifera L.) queens reared in pesticide-laden beeswax exhibit significant changes in the composition of the chemicals produced by their mandibular glands including those that comprise queen mandibular pheromone, which is a critical signal used in mating as well as queen tending behavior. For the present study, we hypothesized that pesticide exposure during development would alter other queen-produced chemicals, including brood pheromone in immature queens, thus resulting in differential feeding of queen larvae by nurse workers, ultimately impacting adult queen morphology. We tested these hypotheses by rearing queens in beeswax containing field-relevant concentrations of (1) a combination of tau-fluvalinate and coumaphos, (2) amitraz, or (3) a combination of chlorothalonil and chlorpyrifos. These pesticides are ubiquitous in most commercial beekeeping operations in North America. We observed nurse feeding rates of queen larvae grafted into pesticide-laden beeswax, analyzed the chemical composition of larval queen pheromones and measured morphological markers in adult queens. Neither the nurse feeding rates, nor the chemical profiles of immature queen pheromones, differed significantly between queens reared in pesticide-laden wax compared to queens reared in pesticide-free wax. Moreover, pesticide exposure during development did not cause virgin or mated adult queens to exhibit differences in morphological markers (i.e., body weight, head width, or thorax width). These results were unexpected given our previous research and indicate that future work is needed to fully understand how pesticide exposure during development affects honey bee queen physiology, as well as how various adult queen quality metrics relate to each other.

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“…Previous studies have identified local factors that may determine foraging activity in various species of social insects. These factors include chemical cues and the rate of interactions with other individuals ( Davidson et al, 2016 ; Pinter-Wollman et al, 2013 ; Mailleux et al, 2011 ; Greene and Gordon, 2007 ; de Biseau and Pasteels, 2000 ; Pless et al, 2015 ; Prabhakar et al, 2012 ; Pagliara et al, 2018 ), the foragers’ own nutritional state ( Toth et al, 2005 ; Mayack and Naug, 2013 ), and larval hunger signals in the nest ( Howard and Tschinkel, 1980 ; Cassill and Tschinkel, 1995 ; Lee Cassill and Tschinkel, 1999 ; Cornelius and Grace, 1997 ; Pankiw, 2004 ; Dussutour and Simpson, 2009 ; Ulrich et al, 2016 ; Schultner et al, 2017 ; Ma et al, 2018 ; Kraus et al, 2019 ; Chandra and Kronauer, 2021 ). Such factors were shown to relate the foragers’ activity to external variables such as food quality or availability, and to the internal colony nutritional requirements ( Seeley, 1989 ; Cassill, 2003 ).…”

Section: Discussionmentioning

confidence: 99%

Emergent regulation of ant foraging frequency through a computationally inexpensive forager movement rule

Baltiansky

Frankel

Feinerman

2023

eLife

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Ant colonies regulate foraging in response to their collective hunger, yet the mechanism behind this distributed regulation remains unclear. Previously, by imaging food flow within ant colonies we showed that the frequency of foraging events declines linearly with colony satiation (Greenwald et al., 2018). Our analysis implied that as a forager distributes food in the nest, two factors affect her decision to exit for another foraging trip: her current food load and its rate of change. Sensing these variables can be attributed to the forager’s individual cognitive ability. Here, new analyses of the foragers’ trajectories within the nest imply a different way to achieve the observed regulation. Instead of an explicit decision to exit, foragers merely tend toward the depth of the nest when their food load is high and toward the nest exit when it is low. Thus, the colony shapes the forager’s trajectory by controlling her unloading rate, while she senses only her current food load. Using an agent-based model and mathematical analysis, we show that this simple mechanism robustly yields emergent regulation of foraging frequency. These findings demonstrate how the embedding of individuals in physical space can reduce their cognitive demands without compromising their computational role in the group.

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Larval pheromones act as colony-wide regulators of collective foraging behavior in honeybees

Cited by 13 publications

References 54 publications

Honey bee (Apis mellifera) larval pheromones may regulate gene expression related to foraging task specialization

Honey bee (Apis mellifera) larval pheromones may regulate gene expression related to foraging task specialization

Pesticide Exposure During Development Does Not Affect the Larval Pheromones, Feeding Rates, or Morphology of Adult Honey Bee (Apis mellifera) Queens

Emergent regulation of ant foraging frequency through a computationally inexpensive forager movement rule

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