The build-up of dominance hierarchies in eusocial insects

Reproductive division of labour is a hallmark of eusocial insects. However, its stability can often be hampered by the potential for reproduction by otherwise sterile nest-mates. Dominance hierarchy has a crucial role in some species in regulating which individuals reproduce. Compared with those in vertebrates, the dominance hierarchies in eusocial insects tend to involve many more individuals, and should require additional selective forces unique to them. Here, we provide an overview of a series of studies on dominance hierarchies in eusocial insects. Although reported from diverse eusocial taxa, dominance hierarchies have been extensively studied in paper wasps and ponerine ants. Starting from molecular physiological attributes of individuals, we describe how the emergence of dominance hierarchies can be understood as a kind of self-organizing process through individual memory and local behavioural interactions. The resulting global structures can be captured by using network analyses. Lastly, we argue the adaptive significance of dominance hierarchies from the standpoint of sterile subordinates. Kin selection, underpinned by relatedness between nest-mates, is key to the subordinates' acceptance of their positions in the hierarchies. This article is part of the theme issue ‘The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies’.

Defense in Social Insects: Diversity, Division of Labor, and Evolution

All social insects defend their colony from predators, parasites, and pathogens. In Oster and Wilson's classic work, they posed one of the key paradoxes about defense in social insects: Given the universal necessity of defense, why then is there so much diversity in mechanisms? Ecological factors undoubtedly are important: Predation and usurpation have imposed strong selection on eusocial insects, and active defense by colonies is a ubiquitous feature of all social insects. The description of diverse insect groups with castes of sterile workers whose main duty is defense has broadened the purview of social evolution in insects, in particular with respect to caste and behavior. Defense is one of the central axes along which we can begin to organize and understand sociality in insects. With the establishment of social insect models such as the honey bee, new discoveries are emerging regarding the endocrine, neural, and gene regulatory mechanisms underlying defense in social insects. The mechanisms underlying morphological and behavioral defense traits may be shared across diverse groups, providing opportunities for identifying both conserved and novel mechanisms at work. Emerging themes highlight the context dependency of and interaction between factors that regulate defense in social insects.

Telomerase as a possible key to bypass the cost of reproduction effect

Telomerase activity and telomere restoration in certain somatic cells of human adults maintain the proliferative capacity of these cells and contribute to their regenerative potential, and telomerase activity and telomere length are commonly considered lifespan predictors. Eusocial insects provide excellent model systems for aging research based on their extraordinary caste-related lifespan differences that contradict the typical fecundity/lifespan trade-off. In agreement with the common presumption, telomerase activity is upregulated in the reproductive, long-lived individuals of eusocial insects such as queens and kings, proposing that telomerase activity acts as a key factor in their extended longevity. But, as documented by the presence of telomerase in somatic tissues of numerous invertebrate and vertebrate species, the connection between telomerase activity and the predicted lifespan is not clear. Here, I ask whether somatic telomerase activity in eusocial reproductives may serve its non-canonical function to protect its individuals against the exacerbated metabolic stress upon reproduction and be a reflection of a more common phenomenon among species. I propose a hypothesis that the presence of telomerase activity in somatic cells reflects a different reproduction strategy of the species.

Decoupled evolution of mating biology and social structure in Acromyrmex leaf-cutting ants

Insect societies vary greatly in their social structure, mating biology, and life history. Polygyny, the presence of multiple reproductive queens in a single colony, and polyandry, multiple mating by females, both increase the genetic variability in colonies of eusocial organisms, resulting in potential reproductive conflicts. The co-occurrence of polygyny and polyandry in a single species is rarely observed across eusocial insects, and these traits have been found to be negatively correlated in ants. Acromyrmex leaf-cutting ants are well-suited for investigating the evolution of complex mating strategies because both polygyny and polyandry co-occur in this genus. We used microsatellite markers and parentage inference in five South American Acromyrmex species to study how different selective pressures influence the evolution of polygyny and polyandry. We show that Acromyrmex species exhibit independent variation in mating biology and social structure, and polygyny and polyandry are not necessarily negatively correlated within genera. One species, Acromyrmex lobicornis, displays a significantly lower mating frequency compared to others, while another species, A. lundii, appears to have reverted to obligate monogyny. These variations appear to have a small impact on average intra-colonial relatedness, although the biological significance of such a small effect size is unclear. All species show significant reproductive skew between patrilines, but there was no significant difference in reproductive skew between any of the sampled species. We find that the evolution of social structure and mating biology appear to follow independent evolutionary trajectories in different species. Finally, we discuss the evolutionary implications that mating biology and social structure have on life history evolution in Acromyrmex leaf-cutting ants. Significance statement Many species of eusocial insects have colonies with multiple queens (polygyny), or queens mating with multiple males (polyandry). Both behaviors generate potentially beneficial genetic diversity in ant colonies as well as reproductive conflict. The co-occurrence of both polygyny and polyandry in a single species is only known from few ant species. Leaf-cutting ants have both multi-queen colonies and multiply mated queens, providing a well-suited system for studying the co-evolutionary dynamics between mating behavior and genetic diversity in colonies of eusocial insects. We used microsatellite markers to infer the socio-reproductive behavior in five South American leaf-cutter ant species. We found that variation in genetic diversity in colonies was directly associated with the mating frequencies of queens, but not with the number of queens in a colony. We suggest that multi-queen nesting and mating frequency evolve independently of one another, indicating that behavioral and ecological factors other than genetic diversity contribute to the evolution of complex mating behaviors in leaf-cutting ants.

DNA methylation clocks tick in naked mole rats but queens age more slowly than nonbreeders

Naked mole rats (NMRs) live an exceptionally long life, appear not to exhibit age-related decline in physiological capacity and are resistant to age-related diseases. However, it has been unknown whether NMRs also evade aging according to a primary hallmark of aging: epigenetic changes. To address this question, we profiled n = 385 samples from 11 tissue types at loci that are highly conserved between mammalian species using a custom array (HorvathMammalMethylChip40). We observed strong epigenetic aging effects and developed seven highly accurate epigenetic clocks for several tissues (pan-tissue, blood, kidney, liver, skin clocks) and two dual-species (human–NMR) clocks. The skin clock correctly estimated induced pluripotent stem cells derived from NMR fibroblasts to be of prenatal age. The NMR epigenetic clocks revealed that breeding NMR queens age more slowly than nonbreeders, a feature that is also observed in some eusocial insects. Our results show that despite a phenotype of negligible senescence, the NMR ages epigenetically.

A fungus infected environment does not alter the behaviour of foraging ants

Eusocial insects are exposed to a wide range of pathogens while foraging outside their nest. We know that opportunistic scavenging ants are able to assess the sanitary state of food and to discriminate a prey which died from infection by the entomopathogenic fungus Metarhizium brunneum. Here, we investigate whether a contamination of the environment can also influence the behaviour of foragers, both at the individual and collective level. In a Y-maze, Myrmica rubra ants had the choice to forage on two prey patches, one of which containing sporulating items. Unexpectedly, the nearby presence of sporulating bodies did not deter foragers nor prevent them from retrieving palatable prey. Ant colonies exploited both prey patches equally, without further mortality resulting from foraging on the contaminated area. Thus, a contamination of the environment did not prompt an active avoidance by foragers of which the activity depended primarily on the food characteristics. Generalist entomopathogenic fungi such as M. brunneum in the area around the nest appear more to be of a nuisance to ant foragers than a major selective force driving them to adopt avoidance strategies. We discuss the cost–benefit balance derived from the fine-tuning of strategies of pathogen avoidance in ants.

Reproductive Potential Impacts Body Maintenance Parameters and Global DNA Methylation in Honeybee Workers (Apis mellifera L.)

The widely accepted hypothesis in life history evolution about the trade-off between fecundity and longevity is not confirmed by long-living and highly fecund queens in eusocial insects. The fact that the queens and facultatively sterile workers usually arise from genetically identical eggs but differ in DNA methylation makes them a good model for studies on senescence, eusocial evolution, and epigenetics. Therefore, honeybees seem to be especially useful here because of long living rebel-workers (RW) with high reproductive potential recently described. Longevity, ovariole number, nosema tolerance, and global DNA methylation have been assayed in normal workers (NW) versus RW in hives and cages. RW always lived longer than NW and unexpectedly extended longevity of NW when they were together, similarly as the presence of a queen did. RW lived longer despite the fact that they had higher Nosema spore load; surprisingly they became infected more easily but tolerated the infection better. Global DNA methylation increased with age, being lower in RW than in NW. Therefore, RW are queen-like considering global DNA methylation and the link between fecundity, longevity, and body maintenance. Presented features of RW expands possibilities of the use of honeybees as a model for studies on senescence, nosemosis, eusocial evolution, and epigenetics.

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.

Worker-dependent gut symbiosis in an ant

The hallmark of eusocial insects, honeybees, ants, and termites, is division of labor between reproductive and non-reproductive worker castes. In addition, environmental adaption and ecological dominance are also underpinned by symbiotic associations with beneficial microorganisms. Microbial symbionts are generally considered to be maintained in an insect colony in two alternative ways: shared among all colony members or inherited only by a specific caste. Especially in ants, the reproductive caste plays a crucial role in transmission of the symbionts shared among colony members over generations. Here, we report an exceptional case, the worker-dependent microbiota in an ant, Diacamma cf. indicum from Japan. By collecting almost all the individuals from 22 colonies in the field, we revealed that microbiota of workers is characterized by a single dominant bacterium localized at the hindgut. The bacterium belonging to an unclassified member within the phylum Firmicutes, which is scarce or mostly absent in the reproductive castes. Furthermore, we show that the gut symbiont is acquired at the adult stage. Collectively, our findings strongly suggest that the specific symbiont is maintained by only workers, demonstrating a novel pattern of ant-associated bacterial symbiosis, and thus further our understanding of host-microbe interactions in the light of sociobiology.

Telomerase-Positive Somatic Tissues of Honeybee Queens (Apis mellifera) Display No DNA Replication

Telomere biology is closely linked to the process of aging. The restoration of telomere length by maintaining telome­rase activity in certain cell types of human adults allows for the proliferative capacity of the cells and preserves the regeneration potential of the tissue. The absence of telome­rase, that leads to telomere attrition and irreversible cell cycle arrest in most somatic cells, acts as a protective mechanism against uncontrolled cancer growth. Nevertheless, there have been numerous studies indicating noncanonical functions of telomerase besides those involved in telomere lengthening. Eusocial insects serve as a great system for aging research. This is because eusocial reproductives, such as queens and kings, have a significantly extended lifespan compared to nonreproductive individuals of the same species. We report that the somatic tissues of honeybee queens (<i>Apis mellifera</i>) are associated with upregulated telomerase activity; however, this upregulation does not fully correlate with the rate of DNA replication in the tissues. This indicates a noncanonical role of telomerase in the somatic tissues of honeybee queens.