skip to main content


Title: Cooperation among unrelated ant queens provides persistent growth and survival benefits during colony ontogeny
Abstract

The fitness consequences of cooperation can vary across an organism’s lifespan. For non-kin groups, especially, social advantages must balance intrinsic costs of cooperating with non-relatives. In this study, we asked how challenging life history stages can promote stable, long-term alliances among unrelated ant queens. We reared single- and multi-queen colonies of the primary polygynous harvester ant,Pogonomyrmex californicus, from founding through the first ten months of colony growth, when groups face high mortality risks. We found that colonies founded by multiple, unrelated queens experienced significant survival and growth advantages that outlasted the colony founding period. Multi-queen colonies experienced lower mortality than single-queen colonies, and queens in groups experienced lower mortality than solitary queens. Further, multi-queen colonies produced workers at a faster rate than did single-queen colonies, even while experiencing lower per-queen worker production costs. Additionally, we characterized ontogenetic changes in the organization of labor, and observed increasing and decreasing task performance diversity by workers and queens, respectively, as colonies grew. This dynamic task allocation likely reflects a response to the changing role of queens as they are increasingly able to delegate risky and costly tasks to an expanding workforce. Faster worker production in multi-queen colonies may beneficially accelerate this behavioral transition from a vulnerable parent–offspring group to a stable, growing colony. These combined benefits of cooperation may facilitate the retention of multiple unrelated queens in mature colonies despite direct fitness costs, providing insight into the evolutionary drivers of stable associations between unrelated individuals.

 
more » « less
NSF-PAR ID:
10221991
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Scientific Reports
Volume:
11
Issue:
1
ISSN:
2045-2322
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Bumble bee queens initiate nests solitarily and transition to living socially once they successfully rear their first cohort of offspring. Bumble bees are disproportionately important for early season pollination, and many populations are experiencing dramatic declines. In this system, the onset of the social stage is critical for nest survival, yet the mechanisms that facilitate this transition remain understudied. Further, the majority of conservation efforts target the social stage of the bumble bee life cycle and do not address the solitary founding stage. We experimentally manipulated the timing of worker emergence in young nests of bumble bee (Bombus impatiens) queens to determine whether and how queen fecundity and survival are impacted by the emergence of workers in the nest. We found that queens with workers added to the nest exhibit increased ovary activation, accelerated egg laying, elevated juvenile hormone (JH) titres and also lower mortality relative to solitary queens. We also show that JH is more strongly impacted by the social environment than associated with queen reproductive state, suggesting that this key regulator of insect reproduction has expanded its function in bumble bees to also influence social organization. We further demonstrate that these effects are independent of queen social history, suggesting that this underlying mechanism promoting queen fecundity is reversible and short lived. Synchronization between queen reproductive status and emergence of workers in the nest may ultimately increase the likelihood of early nesting success in social systems with solitary nest founding. Given that bumble bee workers regulate queen physiology as we have demonstrated, the timing of early worker emergence in the nest likely impacts queen fitness, colony developmental trajectories and ultimately nesting success. Collectively, our findings underline the importance of conservation interventions for bumble bees that support the early nesting period and facilitate the production and maintenance of workers in young nests 
    more » « less
  2. Abstract

    Evaluating the factors that promote invasive ant abundance is critical to assess their ecological impact and inform their management. Many invasive ant species show reduced nestmate recognition and an absence of boundaries between unrelated nests, which allow populations to achieve greater densities due to reduced intraspecific competition. We examined nestmate discrimination and colony boundaries in introduced populations of the red imported fire ant (Solenopsis invicta; hereafter, fire ant). Fire ants occur in two social forms: monogyne (colonies with a single egg‐laying queen) and polygyne (colonies with multiple egg‐laying queens). In contrast with monogyne nests, polygyne nests are thought to be interconnected due to the reduced antagonism between non‐nestmate polygyne workers, perhaps because polygyne workers habituate the colony to an odour unique toGp9b‐carrying adults. However, colony boundaries and nestmate discrimination are poorly documented, particularly for worker‐brood interactions. To delimit boundaries between field colonies, we correlated the exchange of a15N‐glycine tracer dissolved in a sucrose solution with social form. We also evaluated nestmate discrimination between polygyne workers and larvae in the laboratory. Counter to our expectations, polygyne colonies behaved identically to monogyne colonies, suggesting both social forms maintain strict colony boundaries. Polygyne workers also preferentially fed larval nestmates and may have selectively cannibalized non‐nestmates. The levels of relatedness among workers in polygyne colonies was higher than those previously reported in North America (mean ± standard error: 0.269 ± 0.037). Our study highlights the importance of combining genetic analyses with direct quantification of resource exchange to better understand the factors influencing ant invasions.

     
    more » « less
  3. Abstract

    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.

     
    more » « less
  4. Abstract

    Size‐number trade‐offs in reproduction are commonly observed in nature. Bumblebee (Bombusspp.) colonies produce workers that vary considerably in size. This variation suggests that colonies face potential size‐number trade‐offs when producing workers.

    Here, we estimated size‐based vital rates ofBombus vosnesenskiiworkers using colonies reared from wild‐caught queens. We conducted a mark–recapture study to estimate worker survival as a function of body size. We also collected data on pollen and nectar loads as well as foraging trips using a radiofrequency identification system to estimate daily resource return as a function of body size. We integrated survival and daily resource return to estimate lifetime resource collection and offset these estimates by the size‐based worker production costs.

    We found size‐based trade‐offs among workers of different sizes. Smaller workers had higher survival, but larger workers returned with more resources per day. The largest workers made slightly fewer foraging trips per day.

    Overall, larger workers made the greatest lifetime contribution to both nectar and pollen collection. However, once the benefits of larger workers are offset by their higher production costs, intermediate‐sized workers were the optimal for net resource contribution according to our models. Many previous studies have found that larger workers outperformed smaller workers with foraging and in‐nest tasks, yet these studies have not integrated multiple fitness components or worker production costs to quantify net resource contribution towards colony growth.

    Accounting for trade‐offs between costs and performance changed our conclusions about optimal body size from being large to being near the observed average.  Similar approaches of integrating multiple vital rates may resolve apparently suboptimal life histories in other taxa.

    Aplain language summaryis available for this article.

     
    more » « less
  5. Schloss, P. D. (Ed.)
    ABSTRACT The European honey bee ( Apis mellifera ) is used extensively to produce hive products and for crop pollination, but pervasive concerns about colony health and population decline have sparked an interest in the microbial communities that are associated with these important insects. Currently, only the microbiome of workers has been characterized, while little to nothing is known about the bacterial communities that are associated with queens, even though their health and proper function are central to colony productivity. Here, we provide a large-scale analysis of the gut microbiome of honey bee queens during their developmental trajectory and through the multiple colonies that host them as part of modern queen-rearing practices. We found that queen microbiomes underwent a dramatic shift in size and composition as they aged and encountered different worker populations and colony environments. Queen microbiomes were dominated by enteric bacteria in early life but were comprised primarily of alphaproteobacteria at maturity. Furthermore, queen gut microbiomes did not reflect those of the workers who tended them and, indeed, they lacked many of the bacteria that are considered vital to workers. While worker gut microbiotas were consistent across the unrelated colony populations sampled, the microbiotas of the related queens were highly variable. Bacterial communities in mature queen guts were similar in size to those of mature workers and were characterized by dominant and specific alphaproteobacterial strains known to be associated with worker hypopharyngeal glands. Our results suggest a model in which queen guts are colonized by bacteria from workers' glands, in contrast to routes of maternal inoculation for other animal microbiomes. 
    more » « less