NSFDEB-BSF: Uneasy Alliances: Emergent Properties and Feedback Mechanisms among Manipulative Endosymbiotic Communities

Many arthropods are infected with maternally transmitted endosymbionts that can manipulate the reproduction of their hosts to promote symbiont spread within the host population. It is becoming clear that co-infection of hosts by multiple strains of such endosymbionts is much more common than previously appreciated, yet we know very little about how such endosymbionts interact within a host, whether they influence host phenotype in non-additive ways, and how their interactions feedback to influence symbiont spread and persistence in host populations. Here we propose to address this knowledge gap using the bacterial endosymbionts in a Linyphiid spider, Mermessus fradeorum, which is naturally co-infected with up to five strains of endosymbiotic bacteria. Our preliminary data shows that spiders co-infected with all five symbionts have all-female, feminized offspring, which is an emergent property because this trait cannot be simply attributed to any one of the symbiont strains. We have also found that one of the symbionts, a strain of Rickettsiella, is a novel lineage that can induce and rescue a separate reproductive manipulation, cytoplasmic incompatibility (CI). We therefore have symbionts that induce at least two contrasting reproductive manipulations co-infecting the same host individuals, and hosts bearing different realized reproductive phenotypes coexisting within the population. Theoretical predictions suggest that one or the other of these manipulations should quickly displace the other, yet we find empirically that both phenotypes have persisted in the host population over several years of observation. Our central hypothesis is that within-host symbiont community dynamics and among-host population dynamics are bi-directionally linked though feedback pathways that may act to stabilize co-infections and promote maintenance of a diversity of reproductive phenotypes within a host population. Accordingly, our specific objectives for this proposal are 1) To quantify the localization, titer and transmission of each member of the bacterial community in relation to the other symbionts within the host, to form a predictive basis for expectations of interaction strength, 2) to experimentally manipulate infection to determine the contribution of each symbiont to the emergent host phenotype, 3) to empirically test bidirectional linkages between the within-host community and the host population through long-term experimental population studies, and 4) to test whether feedback between organizational levels promotes coexistence of symbionts and phenotypes using a model that links within-host to among-host dynamics. Intellectual Merit: The endosymbiont community of M. fradeorum represents an unparalleled opportunity for exploring symbiotic interactions among reproductive manipulators within a shared host, emergent phenotypic outcomes for the host, and linkage of symbiont interactions within-hosts to population dynamics among-hosts. Bidirectional feedbacks between these organizational levels have the potential to alter expectations for symbiont spread and coexistence within host populations, and represent a substantial paradigm shift in conceptualization relative to current theory. Moreover, this relatively simple host-associated microbial community will allow us to develop a framework for evaluating competitive versus cooperative selection pressures, and can serve as a model for more complicated microbial assemblages. Broader impacts: Spiders act as an engaging vehicle for science communication. We have developed several outreach and educational initiatives that use our small and harmless spiders to emphasize the important ecological role of these creatures. These initiatives will include 1) classroom and individual undergraduate research experiments, with particular emphasis on inclusion of underrepresented groups, 2) undergraduate summer outreach interns that will be trained in and present a diversity of public engagement activities, 3) spider-oriented outreach events at schools and public events, including development of an “itsy bitsy spider” series at the University of Kentucky Arboretum’s Children’s Garden, and 4) production of internet resources and infographics. This NSF-BSF project will foster cross-cultural experiences for graduate students in the US and Israel, and strengthen international collaborations. Finally, the knowledge gained by this project will fill an important gap in understanding interactions among symbionts in arthropod hosts, which is critical context for ongoing public health initiatives that are developing arthropod symbionts for use in controlling vector borne diseases