Whether or how societies are able to sense poor-performing group compositions and respond to them adaptively across different environments remains unknown. Group composition, or the relative representation of individuals with different traits, is often thought to be a major determinant of social group organization and success. Some groups naturally exhibit compositions which help them flourish and others express mixtures that yield their demise. A tractable society (social spiders) will be used to assess how variation in group composition influences the growth, reproductive rate, and extinction risk of entire societies. Societies of different mixtures will be generated and deployed at different field sites, and the success of these societies will be tracked over time. Additionally, the shifts in societies' composition will be monitored over time, in order to see whether societies are able to sense their ailing compositions and shift them adaptively.
The proposed work will further our understanding of how societies, as collective entities, evolve and adjust adaptively to current challenges. This has implications in fields ranging from medicine, to agriculture, and conservation. Virtually every aspect of biology is interested in understanding the drivers of extinction: farmers want to eradicate pests and preserve cultivars; epidemiologists want to drive world pathogens to extinction; while conservation biologists hope to eradicate invasive pest species while preserving dwindling natives. Understanding how groups of organisms (like social spiders) sense and respond to pending extinction risk under normal circumstances might help us predict the factors that can accelerate, slow, or circumvent extinction in other taxa where rigorous experiments are not generally possible. Finally, numerous undergraduates and K-12 students will be involved with elements of the project's implementation as well as the dissemination of the findings. Each year more than a dozen high school teachers help to collect, analyze, and disseminate the findings of these studies, and undergraduates from the University of Pittsburgh gain on-site training on field ecologists and the scientific method.
Intellectual Merit: This proposal explored how group composition influences group success in different habitats. The social spider Anelosimus studiosus lives in multi-female societies where females cooperate together in web construction, prey capture, and care of offspring. Females of this species also exhibit one of two discrete personality types: either an active ‘aggressive’ form or an inactive ‘docile’ form. We tested how the mixture of docile versus aggressive females influenced colony growth and extinction risk in high- and low-resource environments by creating experimental colonies of various mixtures. Naturally-occurring colonies of A.studiosus vary greatly in their personality compositions, but different sites exhibits different characteristic mixtures. We found that our experimental colonies grew faster and were less likely to go extinct when they exhibited personality mixtures like those of colonies that occurred naturally at each site. Importantly, the mixes that beget success at one site can doom a colony at other sites and vice versa. We demonstrate that the reason that this occurs is because the drivers of colony extinction differ across sites. At high-resource sites, social parasites infiltrate colonies and drive them extinct. In contrast, at low-resource sites, food deprivation and cannibalism drive colonies extinct. The ideal mix of the colony depends on the factors that are most likely to drive it extinct. We further showed that when colonies have slightly maladaptive mixtures, they can adjust their compositions in ways that enhance their survival. We provide some evidence that the mechanisms that colonies use to regulate their compositions are genetically influenced. Finally, we implicated one mechanism that allows colonies to adjust their composition and circumvent extinction: selective cessation of reproduction. That is, individuals that possess a personality type that is presently overabundant in a colony are more likely to forgo reproduction and instead help their fellow colony mates. These results are important because they link variation in behavior to the rise, proliferation, and demise of societies in ways that are impossible to study in most social systems, including humans. This has implications for understanding human societies and the risk of societal extinction. The results further stress that natural selection at the colony level has promoted one or more adaptations in group-level traits. This may seem intuitive, but this turns out to be one of the most hotly debated topics in evolutionary biology for the past 50 years. Broader Impacts: This proposal aided in the training of three graduate students, 1 postdoctoral researcher, and more than 20 undergraduate researchers. Many of the results describe above were published in top-tier scientific journals, including one of the most influential scientific journals in the world, Nature. Spiders used in the studies described above were also used in K-12 outreach at rural middle schools and high schools throughout western Pennsylvania (>2000 students in 2014-2015) and at the USA Science and Engineering Festival (>30,000 visitors to the NSF pavilion). Students were able to observe spider behavior, design experiments, and interact with some of our world’s most captivating but maligned organisms.
