Bees recognize each other through their microbiome
<p>Members of an “Apis mellifera” colony share the same olfactory signature, emitted by their cuticular hydrocarbons and linked to a specific intestinal bacterial flora.</p>
Abstract
A recent US study (Cassondra L. Vernier et al., 2020) has shown that in the honey bee, the genetically related members of a colony innately develop colony-specific profiles of cuticular hydrocarbons that serve as recognition cues for the pheromonal identity of that population. However, despite the high degree of relatedness within a colony, the innate development of individual, colony-specific chemical signatures is largely determined by the environment within the hive, rather than depending solely on the genetic variants shared by the individuals of that colony. This raises the question of how a non-genetic factor can give rise to the innate development of a quantitative trait shared by all members of the same colony. The researchers provide an answer to this puzzle by showing that, in honey bees, colony membership recognition cues are defined, at least in part, by shared characteristics of the gut microbiome among members of the same colony. These findings illustrate the importance of host–microbiome interactions as a source of variation in animal behavioural traits.
The comings and goings of foragers leaving and returning to their colony are closely monitored by the guard bee (Image: Susanne Jutzeler)
“Your papers, please!” Stationed at the entrance of the hive, guard bees check the identity of individuals seeking access. The guard inspects the “identity card” of the honey bee by sniffing its cuticular hydrocarbons, a waterproof layer covering its exoskeleton (the cuticle). “Each colony has its own olfactory profile, a distinctive scent,” explains Martin Giurfa, Professor of Neuroscience at the University of Paul Sabatier (Toulouse). “In social insects—not only bees—colony identity allows each individual to recognise both nestmates and intruders. During periods of food scarcity, bees may attack other colonies.”
Yet one mystery remains. “During the famous nuptial flight, many drones mate with the queen. One single mother and… dozens of different fathers! How, then, is it possible that within a colony with such high genetic diversity, all bees ultimately share the same chemical signature?”
A US study published in Science Advances on 14 October provides initial answers: it is the bees’ intestinal bacterial flora—the microbiome—that influences the profile of cuticular hydrocarbons. “Each bee colony actually has a specific microbiome. This had never been demonstrated before!” says Cassondra Vernier (Washington University in St. Louis, USA), lead author of the study. “We knew that many factors could influence this profile, such as genetics, diet, age, or temperature. But we did not know exactly why colonies display different chemical signatures.” By constantly sharing food, bees also exchange their microbial communities.
A flora that influences behaviour.
However, the mechanism by which the bacterial flora modifies the bees’ olfactory profile remains unclear: the bacteria cannot access the oenocytes, the subcutaneous cells responsible for synthesising cuticular hydrocarbons. The researcher suggests that “it is more likely that the microbiome influences the quality of the chemical signature by modifying the expression of enzymes involved in these biochemical reactions or by providing different compounds to the oenocytes.” By metabolising sugars, bacteria produce molecules that bees can use to synthesise cuticular hydrocarbons—pheromones involved not only in colony recognition but also in sexual and social interactions (fanners, guards, cleaners, etc.).
That host–bacterial flora interactions play an important role is well established in other animals. “Certain aspects of animal behaviour in general, and sociability in particular, may have evolved through a codependence between animal hosts and their microbes,” explains Cassondra Vernier. An international study published in 2019 showed that antibiotic treatment affects recognition and aggression behaviours in leaf-cutting ants, “suggesting a correlation between chemical profiles and the presence of certain microbial species in the gut.” Numerous studies have demonstrated that bacterial flora can regulate the bioavailability of a wide range of molecules influencing social behaviour in animals, including glucocorticoids, sex hormones, and neurotransmitters.
“The microbiome is a fashionable topic,” admits Martin Giurfa. He himself is investigating to what extent bacterial flora may affect learning and memory capacities in bees. While many questions remain unanswered, Cassondra Vernier is certain of one thing: “The effect of the microbiome on host behaviour is becoming a fundamental rule of life.”
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