The queen, but not the brood, drives early changes in 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 honey bee and the clonal 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. Genes that serve as key regulators of workers’ reproduction are likely to play an important role in the evolution of sociality.

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.

Worker-Born Males Are Smaller but Have Similar Reproduction Ability to Queen-Born Males in Bumblebees

Queen-worker conflict over the reproduction of males exists in the majority of haplodiplioidy hymenpteran species such as bees, wasps, and ants, whose workers lose mating ability but can produce haploid males in colony. Bumblebee is one of the representatives of primitively eusocial insects with plastic division labor and belongs to monandrous and facultative low polyandry species that have reproductive totipotent workers, which are capable of competing with mother queen to produce haploid males in the queenright colony compared to higher eusocial species, e.g., honeybees. So, bumblebees should be a better material to study worker reproduction, but the reproductive characteristics of worker-born males (WMs) remain unclear. Here, we choose the best-studied bumblebee Bombus terrestris to evaluate the morphological characteristics and reproductive ability of WMs from the queenless micro-colonies. The sexually matured WMs showed smaller in forewing length and weight, relatively less sperm counts but equally high sperm viability in comparison with the queen-born males (QMs) of the queenright colony. Despite with smaller size, the WMs are able to successfully mate with the virgin queens in competition with the QMs under laboratory conditions, which is quite different from the honeybees reported. In addition, there was no difference in the colony development, including the traits such as egg-laying rate, colony establishment rate, and populations of offspring, between the WM- and the QM-mated queens. Our study highlights the equivalent reproductive ability of worker-born males compared to that of queens, which might exhibit a positive application or special use of bumblebee rearing, especially for species whose males are not enough for copulation. Further, our finding contributes new evidence to the kin selection theory and suggests worker reproduction might relate to the evolution of sociality in bees.

Individual-based modeling of genome evolution in haplodiploid organisms

Ants, bees, wasps, bark beetles, and other species have haploid males and diploid females. Although such haplodiploid species play key ecological roles and are threatened by environmental changes, no general framework exists for simulating their genetic evolution. Here, we use the SLiM simulation environment to build a novel model for individual-based forward simulation of genetic evolution in haplodiploid populations. We compare the fates of adaptive and deleterious mutations and find that selection is more effective in haplodiploid species than in diploid species. Our open-source model will help understand the evolution of sociality and how ecologically important species may adapt to changing environments.

Matriphagy in five species of the genus Anelosimus (Araneae: Theridiidae)

Parental care has evolved numerous times in many taxonomic groups of animals. Matriphagy, as an extreme example of parental care, is present in many social species, subsocial species, and even in solitary spiders. Here, we describe matriphagy in five species of Anelosimus of different levels of sociality: social (A. dubiosus), intermediate social (A. jabaquara), subsocial (A. vierae, A. baeza), and solitary (A. nigrescens). Each group contained a female and its brood, maintained under standardized laboratory conditions. All species showed matriphagy, regardless of their social level. Further studies are necessary to clarify whether matriphagy is a necessary precondition for the evolution of sociality in spiders, or if it is phylogenetically conserved in some families.

Filling in the holes: The reproductive biology of the understudied Mahali mole-rat (Cryptomys hottentotus mahali)

African mole-rats have provided great insight into mammalian evolution of sociality and reproductive strategy. However, some species have not received attention, and these may provide further insights into these evolutionary questions. The cooperatively breeding Mahali mole-rat (Cryptomys hottentotus mahali (Roberts, 1913)) is one such species. Body mass, reproductive-tract morphometrics, gonad histology, and plasma reproductive hormone concentrations were studied for breeding and non-breeding males and females over 1 year. This study aimed to discern if this species exhibits a seasonal or aseasonal breeding pattern and whether there is a relaxation of reproductive suppression at any point in the year in non-breeding animals. The pattern of reproductive relaxation during the wetter months is similar to other African mole-rat species. Interestingly, births and pregnant breeding females were recorded throughout the year, thus indicating an aseasonal breeding strategy, despite inhabiting a region that experiences seasonal rainfall. However, there were periods of the year favouring increased reproduction to enable an increased likelihood of offspring survival. This suggests that the Mahali mole-rat may be an opportunistic breeder possibly brought about by the benefits of living in a cooperatively breeding group and potentially moving into more arid environments that were previously unexploited by the genus Cryptomys Gray, 1864.

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.

Venom and Social Behavior: The Potential of Using Spiders to Evaluate the Evolution of Sociality under High Risk

Risks of sociality, including competition and conspecific aggression, are particularly pronounced in venomous invertebrates such as arachnids. Spiders show a wide range of sociality, with differing levels of cannibalism and other types of social aggression. To have the greatest chance of surviving interactions with conspecifics, spiders must learn to assess and respond to risk. One of the major ways risk assessment is studied in spiders is via venom metering, in which spiders choose how much venom to use based on prey and predator characteristics. While venom metering in response to prey acquisition and predator defense is well-studied, less is known about its use in conspecific interactions. Here we argue that due to the wide range of both sociality and venom found in spiders, they are poised to be an excellent system for testing questions regarding whether and how venom use relates to the evolution of social behavior and, in return, whether social behavior influences venom use and evolution. We focus primarily on the widow spiders, Latrodectus, as a strong model for testing these hypotheses. Given that successful responses to risk are vital for maintaining sociality, comparative analysis of spider taxa in which venom metering and sociality vary can provide valuable insights into the evolution and maintenance of social behavior under risk.

Molecular regulation of lifespan extension in fertile ant workers

The evolution of sociality in insects caused a divergence in lifespan between reproductive and non-reproductive castes. Ant queens can live for decades, while most workers survive only weeks to a few years. In most organisms, longevity is traded-off with reproduction, but in social insects, these two life-history traits are positively linked. Once fertility is induced in workers, e.g. by queen removal, worker lifespan increases. The molecular regulation of this positive link between fecundity and longevity and generally the molecular underpinnings of caste-specific senescence are not well understood. Here, we investigate the transcriptomic regulation of lifespan and reproduction in fat bodies of three worker groups in the ant Temnothorax rugatulus . In a long-term experiment, workers that became fertile in the absence of the queen showed increased survival and upregulation of genes involved in longevity and fecundity pathways. Interestingly, workers that re-joined their queen after months exhibited intermediate ovary development, but retained a high expression of longevity and fecundity genes. Strikingly, the queen's presence causes a general downregulation of genes in worker fat bodies. Our findings point to long-term consequences of fertility induction in workers, even after re-joining their queen. Moreover, we reveal longevity genes and pathways modulated during insect social evolution. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’