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1. Temporal Analysis of Effective Population Size and Mating System in a Social Wasp

   https://doi.org/10.1093/jhered/esab057  

   Dyson, Carl J ; Piscano, Olivia L ; Durham, Rebecca M ; Thompson, Veronica J ; Johnson, Catherine H ; Goodisman, Michael A ( September 2021 , Journal of Heredity)

   Booth, Warren (Ed.)

   Abstract Highly social species are successful because they cooperate in obligately integrated societies. We examined temporal genetic variation in the eusocial wasp Vespula maculifrons to gain a greater understanding of evolution in highly social taxa. First, we wished to test if effective population sizes of eusocial species were relatively low due to the reproductive division of labor that characterizes eusocial taxa. We thus estimated the effective population size of V. maculifrons by examining temporal changes in population allele frequencies. We sampled the genetic composition of a V. maculifrons population at 3 separate timepoints spanning a 13-year period. We found that effective population size ranged in the hundreds of individuals, which is similar to estimates in other, non-eusocial taxa. Second, we estimated levels of polyandry in V. maculifrons in different years to determine if queen mating system varied over time. We found no significant change in the number or skew of males mated to queens. In addition, mating skew was not significant within V. maculifrons colonies. Therefore, our data suggest that queen mate number may be subject to stabilizing selection in this taxon. Overall, our study provides novel insight into the selective processes operating in eusocial species by analyzing temporal genetic changes within populations. 

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2. Multi-queen breeding is associated with the origin of inquiline social parasitism in ants

   https://doi.org/10.1038/s41598-022-17595-0  

   Dahan, Romain A. ; Rabeling, Christian ( August 2022 , Scientific Reports)

   Social parasites exploit the brood care behavior of their hosts to raise their own offspring. Social parasites are common among eusocial Hymenoptera and exhibit a wide range of distinct life history traits in ants, bees, and wasps. In ants, obligate inquiline social parasites are workerless (or nearly-so) species that engage in lifelong interactions with their hosts, taking advantage of the existing host worker forces to reproduce and exploit host colonies’ resources. Inquiline social parasites are phylogenetically diverse with approximately 100 known species that evolved at least 40 times independently in ants. Importantly, ant inquilines tend to be closely related to their hosts, an observation referred to as ‘Emery’s Rule’. Polygyny, the presence of multiple egg-laying queens, was repeatedly suggested to be associated with the origin of inquiline social parasitism, either by providing the opportunity for reproductive cheating, thereby facilitating the origin of social parasite species, and/or by making polygynous species more vulnerable to social parasitism via the acceptance of additional egg-laying queens in their colonies. Although the association between host polygyny and the evolution of social parasitism has been repeatedly discussed in the literature, it has not been statistically tested in a phylogenetic framework across the ants. Here, we conduct a meta-analysis of ant social structure and social parasitism, testing for an association between polygyny and inquiline social parasitism with a phylogenetic correction for independent evolutionary events. We find an imperfect but significant over-representation of polygynous species among hosts of inquiline social parasites, suggesting that while polygyny is not required for the maintenance of inquiline social parasitism, it (or factors associated with it) may favor the origin of socially parasitic behavior. Our results are consistent with an intra-specific origin model for the evolution of inquiline social parasites by sympatric speciation but cannot exclude the alternative, inter-specific allopatric speciation model. The diversity of social parasite behaviors and host colony structures further supports the notion that inquiline social parasites evolved in parallel across unrelated ant genera in the formicoid clade via independent evolutionary pathways.

    

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3. Social structure of perennial Vespula squamosa wasp colonies

   https://doi.org/10.1002/ece3.8569  

   Dyson, Carl J. ; Crossley, Henry G. ; Ray, Charles H. ; Goodisman, Michael A. D. ( February 2022 , Ecology and Evolution)

   Many social species show variation in their social structure in response to different environmental conditions. For example, colonies of the yellowjacket waspVespula squamosaare typically headed by a single reproductive queen and survive for only a single season. However, in warmer climates,V. squamosacolonies sometimes persist for multiple years and can grow to extremely large size. We used genetic markers to understand patterns of reproduction and recruitment within these perennial colonies. We genotypedV. squamosaworkers, pre‐reproductive queens, and males from perennial colonies in the southeastern United States at 10 polymorphic microsatellite loci and one mitochondrial DNA locus. We found thatV. squamosafrom perennial nests were produced by multiple reproductives, in contrast to typical annual colonies. Relatedness of nestmates from perennial colonies was significantly lower than relatedness of nestmates from annual colonies. Our analyses of mitochondrial DNA indicated that mostV. squamosaperennial colonies represented semiclosed systems whereby all individuals belonged to a single matriline despite the presence of multiple reproductive females. However, new queens recruited into perennial colonies apparently mated with non‐nestmate males. Notably, perennial and annual colonies did not show significant genetic differences, supporting the hypothesis that perennial colony formation represents an instance of social plasticity. Overall, our results indicate that perennialV. squamosacolonies show substantial changes to their social biology compared to typical annual colonies and demonstrate variation in social behaviors in highly social species.

    

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4. Early queen joining and long‐term queen associations in polygyne colonies of an invasive wasp revealed by longitudinal genetic analysis

   https://doi.org/10.1111/eva.13324  

   Scarparo, Giulia ; Sankovitz, Madison ; Loope, Kevin J. ; Wilson‐Rankin, Erin ; Purcell, Jessica ( November 2021 , Evolutionary Applications)

   Invasive social insects rank among the most damaging of terrestrial species. They are responsible for extensive damage and severely threaten the biodiversity of environments where they are introduced. Variation in colony social form commonly occurs in introduced populations of yellowjacket wasps (genusVespula). In particular, invasive colonies may contain multiple queens (i.e., polygyne) and persist several years, while in the native range, the colonies are usually annual and harbor a single queen (i.e., monogyne). In this study, we used genome‐wide loci obtained by double digest restriction site‐associated DNA sequencing (RADseq) to investigate the genetic structure and queen turnover in colonies of the western yellowjacket,Vespula pensylvanica, in their introduced range in Hawaii. Of the 27 colonies monitored over four months (October–January), 19 were polygyne and already contained multiple queens on the first day of sampling. Contrary to previous speculation, this finding suggests that polygyny often arises early in the annual colony cycle, before the production of new queens in the fall. Furthermore, polygyne colonies exhibited a prolonged average lifespan relative to those headed by a single queen. As a result, there is no clear window during which colony eradication efforts would be more effective than upon first discovery. The relatedness among nestmate queens was slightly above zero, indicating that these colonies are generally composed of nonrelatives. The queen turnover within each colony was low, and we detected some full‐sibling workers sampled up to four months apart. Finally, we did not detect any population structure among colonies, suggesting that queens disperse up to several kilometers. Taken together, our results provide the first insights into the requeening dynamics in this invasive and incipiently polygyne population and illuminate the early establishment of multiple long‐lasting queens in these damaging colonies.

    

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5. The benefits of being big and diverse: early colony survival in harvester ants

   https://doi.org/10.1002/ecy.3556  

   Cole, Blaine J. ; Jordan, Dayne ; LaCour‐Roy, Montrel ; O’Fallon, Sean ; Manaker, Logan ; Ternest, John J. ; Askew, Megan ; Garey, Daniel ; Wiernasz, Diane C. ( November 2021 , Ecology)

   In sessile organisms such as plants and benthic invertebrates, founding propagules typically suffer extremely high rates of mortality due to both extrinsic and intrinsic factors. Many social insect species share similarities with these groups, but factors influencing early colony survival are relatively unstudied. We used a field experiment to measure the importance of environmental quality relative to intrinsic colony properties in the harvester ant,Pogonomyrmex occidentalis, by monitoring the survival of 584 experimental colonies. We measured survival of transplanted colonies over four months in each of three years (2014–2016) at a site in western Colorado. Colony survival was primarily determined by colony features. Multiple mating by the queen and larger colony size at the time of transplant increased survival, but queen size, maternal lineage and the composition of plant species in the vicinity of the colony did not. Food supplementation increased survival significantly when natural food was scarce, but was not consistently beneficial, in contrast to predictions. Our results emphasize the general importance of rapid growth and early attainment of large size in the survival of sessile species. However, attributes specific to ants that are a consequence of their sociality also strongly affected survival. Colonies with multiply‐mated queens were more likely to survive over a wide range of circumstances, highlighting the importance of this trait even at the early stages of colony life.

    

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