The queen, but not the brood, drives brain gene expression in bumble bee workers

Worker reproduction in social insects is often regulated by the queen, but can be regulated by the brood and nestmates, who may use different mechanisms to induce the same outcomes in subordinates. Analysis of brain gene expression patterns in bumble bee workers (Bombus impatiens) in response to the presence of the queen, the brood, both or neither, identified 18 differentially expressed genes, 17 of them are regulated by the queen and none are regulated by the brood. Overall, brain gene expression differences in workers were driven by the queen’s presence, despite recent studies showing that brood reduces worker egg laying and provides context to the queen pheromones. The queen affected important regulators of reproduction and brood care across insects, such as neuroparsin and vitellogenin, and a comparison with similar datasets in the honeybee and the raider ant revealed that neuroparsin is differentially expressed in all species. These data emphasize the prominent role of the queen in regulating worker physiology and behavior, and the need to consider components other than the queen when examining regulators of worker sterility. Genes that serve as key regulators of workers’ reproduction are likely to play an important role in the evolution of sociality.

Major Evolutionary Transitions in Social Insects, the Importance of Worker Sterility and Life History Trade-Offs

The evolution of eusociality in social insects, such as termites, ants, and some bees and wasps, has been regarded as a major evolutionary transition (MET). Yet, there is some debate whether all species qualify. Here, we argue that worker sterility is a decisive criterion to determine whether species have passed a MET (= superorganisms), or not. When workers are sterile, reproductive interests align among group members as individual fitness is transferred to the colony level. Division of labour among cooperating units is a major driver that favours the evolution of METs across all biological scales. Many METs are characterised by a differentiation into reproductive versus maintenance functions. In social insects, the queen specialises on reproduction while workers take over maintenance functions such as food provisioning. Such division of labour allows specialisation and it reshapes life history trade-offs among cooperating units. For instance, individuals within colonies of social insects can overcome the omnipresent fecundity/longevity trade-off, which limits reproductive success in organisms, when increased fecundity shortens lifespan. Social insect queens (particularly in superorganismal species) can reach adult lifespans of several decades and are among the most fecund terrestrial animals. The resulting enormous reproductive output may contribute to explain why some genera of social insects became so successful. Indeed, superorganismal ant lineages have more species than those that have not passed a MET. We conclude that the release from life history constraints at the individual level is a important, yet understudied, factor across METs to explain their evolutionary success.

RNA-seq analysis of workers' brain reveals that queen and brood affect bumble bee worker reproduction via similar genetic pathways

Worker reproduction in social insects is often regulated by the queen’s presence but can be regulated by other colony members, such as the brood and nestmates. Adults and brood may induce the same outcomes in subordinates but may use different mechanisms. Here, we compared gene expression patterns in bumble bee workers (Bombus impatiens) in response to the queen, the brood, both or none. RNA‐seq analysis of workers’ brain identified 27 differentially expressed genes regulated by the queen and the brood. Expression levels of 8 candidate genes were re-tested using qRT-PCR in worker brain and fat body. Our results show that the brood’s effect on gene expression is substantially weaker than the queen, and a greater impact on gene expression was caused by the combined presence of the queen and the brood. All the genes that were explained by the brood presence were also regulated by the queen presence. A significant amount of the variation in gene expression was explained by the queen, that regulated the expression of key regulators of reproduction and brood care across insects, such as neuroparsin and vitellogenin. A comparison of the data with similar datasets in the honeybee and the raider ant revealed that neuroparsin is the only differentially expressed gene shared by all species. These data highlight the need to consider components other than the queen when examining mechanisms regulating worker sterility and provide information on key genes regulating reproduction that are likely to play an important role in the evolution of sociality.

Irreversible sterility of workers and high-volume egg production by queens in the stingless bee Tetragonula carbonaria

ABSTRACTSocial insects are characterised by a reproductive division of labour between queens and workers. However, in the majority of social insect species, the workers are only facultatively sterile. The Australian stingless bee Tetragonula carbonaria is noteworthy as workers never lay eggs. Here, we describe the reproductive anatomy of T. carbonaria workers, virgin queens and mated queens. We then conduct the first experimental test of absolute worker sterility in the social insects. Using a controlled microcolony environment, we investigate whether the reproductive capacity of adult workers can be rescued by manipulating the workers' social environment and diet. The ovaries of T. carbonaria workers that are queenless and fed unrestricted, highly nutritious royal jelly remain non-functional, indicating they are irreversibly sterile and that ovary degeneration is fixed prior to adulthood. We suggest that T. carbonaria might have evolved absolute worker sterility because colonies are unlikely to ever be queenless.

Irreversible sterility of workers and high-volume egg production by queens in the stingless bee Tetragonula carbonaria

ABSTRACTSocial insect reproduction is characterised by a division of labour. Typically, the queen is the sole reproductive female in the colony and the female workers are non-reproductive. However, in the majority of social insect species the workers are only facultatively sterile and remain capable of laying eggs under some conditions, such as when the queen dies. The Australian stingless bee Tetragonula carbonaria is noteworthy as workers never lay eggs, even if a colony loses its queen. Here we describe the reproductive anatomy of T. carbonaria workers (deactivated ovaries), virgin queens (semi-activated ovaries), and mated queens (activated ovaries). T. carbonaria mated queens have high-volume egg production compared to other female insects as each of their eight ovarioles (filaments of the ovary) produces approximately 40 eggs per day. We then conduct the first experimental test of absolute worker sterility in the social insects. Using a controlled microcolony environment, we investigate whether the reproductive capacity of adult workers can be rescued by manipulating the workers’ social environment (separating them from a queen) and diet (feeding them unrestricted highly nutritious honey bee royal jelly), both conditions which cause ovary activation in bee species where workers are facultatively sterile. The ovaries of T. carbonaria workers that are queenless and fed royal jelly remain non-functional, indicating they are irreversibly sterile and that ovary degeneration is fixed prior to adulthood. We suggest that T. carbonaria might have evolved absolute worker sterility because colonies under natural conditions are unlikely to ever be queenless.

Monogamy promotes altruistic sterility in insect societies

Monogamy is associated with sibling-directed altruism in multiple animal taxa, including insects, birds and mammals. Inclusive-fitness theory readily explains this pattern by identifying high relatedness as a promoter of altruism. In keeping with this prediction, monogamy should promote the evolution of voluntary sterility in insect societies if sterile workers make for better helpers. However, a recent mathematical population-genetics analysis failed to identify a consistent effect of monogamy on voluntary worker sterility. Here, we revisit that analysis. First, we relax genetic assumptions, considering not only alleles of extreme effect—encoding either no sterility or complete sterility—but also alleles with intermediate effects on worker sterility. Second, we broaden the stability analysis—which focused on the invasibility of populations where either all workers are fully sterile or all workers are fully reproductive—to identify where intermediate pure or mixed evolutionarily stable states may occur. Third, we consider a broader range of demographically explicit ecological scenarios relevant to altruistic worker non-reproduction and to the evolution of eusociality more generally. We find that, in the absence of genetic constraints, monogamy always promotes altruistic worker sterility and may inhibit spiteful worker sterility. Our extended analysis demonstrates that an exact population-genetics approach strongly supports the prediction of inclusive-fitness theory that monogamy promotes sib-directed altruism in social insects.

The evolution of queen control over worker reproduction in the social Hymenoptera

A trademark of eusocial insect species is reproductive division of labor, in which workers forego their own reproduction while the queen produces almost all offspring. The presence of the queen is key for maintaining social harmony, but the specific role of the queen in the evolution of eusociality remains unclear. A long-discussed scenario is that a queen either behaviorally or chemically sterilizes her workers. However, the demographic and ecological conditions that enable such manipulation are unknown. Accordingly, we propose a simple model of evolutionary dynamics that is based on haplodiploid genetics. We consider a mutation that acts in a queen, causing her to control the reproductive behavior of her workers. Our mathematical analysis yields precise conditions for the evolutionary emergence and stability of queen-induced worker sterility. These conditions do not depend on the queen's mating frequency. Moreover, we find that queen control is always established if it increases colony reproductive efficiency and can evolve even if it decreases colony efficiency. We further outline the conditions under which queen control is evolutionarily stable against invasion by mutant, reproductive workers.

Monogamy promotes worker sterility in insect societies

Inclusive-fitness theory highlights monogamy as a key driver of altruistic sib-rearing. Accordingly, monogamy should promote the evolution of worker sterility in social insects when sterile workers make for better helpers. However, a recent population-genetics analysis (Olejarzet al.2015) found no clear effect of monogamy on worker sterility. Here, we revisit this analysis. First, we relax genetic assumptions, considering not only alleles of extreme effect—encoding either no sterility or complete sterility—but also alleles with intermediate worker-sterility effects. Second, we broaden the stability analysis—which focused on the invasibility of populations where either all workers are fully-sterile or all workers are fully-reproductive—to identify where intermediate pure or mixed evolutionarily-stable states may occur. Finally, we consider additional, demographically-explicit ecological scenarios relevant to worker non-reproduction. This extended analysis demonstrates that an exact population-genetics approach strongly supports the prediction of inclusive-fitness theory that monogamy promotes sib-directed altruism in social insects.