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1. Trachymyrmex septentrionalis Ant Microbiome Assembly Is Unique to Individual Colonies and Castes

   https://doi.org/10.1128/msphere.00989-21  

   Green, Emily A.; Klassen, Jonathan L. (August 2022, mSphere)

   Imperiale, Michael J. (Ed.)

   ABSTRACT Within social insect colonies, microbiomes often differ between castes due to their different functional roles and between colony locations. Trachymyrmex septentrionalis fungus-growing ants form colonies throughout the eastern United States and northern Mexico that include workers, female and male alates (unmated reproductive castes), larvae, and pupae. How T. septentrionalis microbiomes vary across this geographic range and between castes is unknown. Our sampling of individual ants from colonies across the eastern United States revealed a conserved T. septentrionalis worker ant microbiome and revealed that worker ant microbiomes are more conserved within colonies than between them. A deeper sampling of individual ants from two colonies that included all available castes (pupae, larvae, workers, and female and male alates), from both before and after adaptation to controlled laboratory conditions, revealed that ant microbiomes from each colony, caste, and rearing condition were typically conserved within but not between each sampling category. Tenericute bacterial symbionts were especially abundant in these ant microbiomes and varied widely in abundance between sampling categories. This study demonstrates how individual insect colonies primarily drive the composition of their microbiomes and shows that these microbiomes are further modified by developmental differences between insect castes and the different environmental conditions experienced by each colony. IMPORTANCE This study investigates microbiome assembly in the fungus-growing ant Trachymyrmex septentrionalis , showing how colony, caste, and lab adaptation influence the microbiome and revealing unique patterns of mollicute symbiont abundance. We find that ant microbiomes differ strongly between colonies but less so within colonies. Microbiomes of different castes and following lab adaptation also differ in a colony-specific manner. This study advances our understanding of the nature of individuality in social insect microbiomes and cautions against the common practice of only sampling a limited number of populations to understand microbiome diversity and function. 

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2. Conversion of social organization in fire ants induced by few colony members: Unmasking indirect genetic effects

   https://doi.org/10.1073/pnas.2501740122  

   Zeng, Haolin; Ross, Kenneth G; Sasaki, Takao (May 2025, Proceedings of the National Academy of Sciences)

   Genes and the environment jointly shape individual traits, but the influence of indirect genetic effects (IGEs), arising from the genetic composition of interacting conspecific individuals, is often ignored or underemphasized. Moreover, because of practical challenges in characterizing IGEs, empirical research has fallen behind theoretical advancement. The fire antSolenopsis invictaoffers a uniquely suitable study system due to its distinct colony-level phenotypic variation (monogyne and polygyne social forms) attributed to IGEs of a social-supergene variant (ballele). A minority ofb-carrying workers (Bbgenotype) can trigger colony-level conversion from monogyne (single queen per colony) to polygyne (multiple queens per colony) behavior. This study investigated the mechanisms underlying this process via 400-ant microcolonies. We first showed that assimilatedBbworkers reduce aggression by hostBBworkers towardBbqueens, thus inducing polygyny, at rates observed earlier in experiments that used full-size (>20,000 ants) colonies. We then demonstrated that social conversion is facilitated by cuticular contact between the worker types, and verified the presence of nonvolatile cuticular pheromones that are necessary but not sufficient components underpinning this process. Follow-up experiments suggested that a second, polygyne worker-produced pheromone that is only released once such workers detect aBbqueen is also necessary but again insufficient, for full expression of the conversion phenomenon. Thus, multiple pheromonal components linked to presence of thebsupergene allele in colony workers appear to be involved in shaping social environments and thereby inducing, via IGEs, the transformation from monogyne to polygyne fire ant societies. 

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

   https://doi.org/10.1007/s00265-021-03113-1  

   Dahan, Romain A.; Grove, Nathan K.; Bollazzi, Martin; Gerstner, Benjamin P.; Rabeling, Christian (January 2022, Behavioral Ecology and Sociobiology)

   Abstract 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. 

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4. Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages

   https://doi.org/10.1128/msystems.01182-23  

   Caesar, Lílian; Rice, Danny W.; McAfee, Alison; Underwood, Robyn; Ganote, Carrie; Tarpy, David R.; Foster, Leonard J.; Newton, Irene L. (February 2024, mSystems)

   Klassen, Jonathan L. (Ed.)

   The queen caste plays a central role in colony success in eusocial insects, as queens lay eggs and regulate colony behavior and development. Queen failure can cause colonies to collapse, which is one of the major concerns of beekeepers. Thus, understanding the biology behind the queen’s health is a pressing issue. Previous studies have shown that the bee microbiome plays an important role in worker bee health, but little is known about the queen microbiome and its functionin vivo. Here, we characterized the queen microbiome, identifying for the first time the present species and their putative functions. We show that the queen microbiome has predicted nutritional and protective roles in queen association and comprises only four consistently present bacterial species. Additionally, we bring to attention the spread of phages in the queen microbiome, which increased in abundance in failing queens and may impact the fate of the colony. 

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5. Novel insights into paternity skew in a polyandrous social wasp

   https://doi.org/10.1111/1744-7917.13343  

   Orr, Sarah E; Hedrick, Nicole A; Murray, Kayla A; Pasupuleti, Abhinav K; Goodisman, Michael_A D (February 2024, Insect Science)

   Females of many species are polyandrous. However, polyandry can give rise to conflict among individuals within families. We examined the level of polyandry and paternity skew in the common eastern yellowjacket wasp,Vespula maculifrons, in order to gain a greater understanding of conflict in social insects. We collected 10 colonies ofV. maculifronsand genotyped workers and prereproductive queens at highly variable microsatellite markers to assign each to a patriline. Genotypic data revealed evidence of significant paternity skew among patrilines. In addition, we found that patrilines contributed differentially to caste production (worker vs. queen), suggesting an important role for reproductive conflict not previously discovered. We also investigated if patterns of paternity skew and mate number varied over time. However, we found no evidence of changes in levels of polyandry when compared to historical data dating back almost 40 years. Finally, we measured a suite of morphological traits in individuals from the most common and least common patrilines in each colony to test if males that showed highly skewed reproductive success also produced offspring that differed in phenotype. Our data revealed weak correlation between paternity skew and morphological phenotype of offspring sired by different males, suggesting no evidence of evolutionary tradeoffs at the level investigated. Overall, this study is the first to report significant paternity and caste‐associated skew inV. maculifrons, and to investigate the phenotypic consequences of skew in a social wasp. Our results suggest that polyandry can have important consequences on the genetic and social structure of insect societies. 

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