My name is  Dr. Anna Forsman and I am the bird-chasing, microbe-wrangling PI of the Wild Symbioses Lab. Together with my students, I run the UCF Purple Martin Project, which is a long-term monitoring program we established on the UCF campus in 2020. We provide wild purple martins with 168 nesting cavities, arranged on 14 houses and in return, these amazing migratory swallows provide us with the opportunity to study their breeding biology, foraging/movement ecology, and eco-physiology (among many other things).

Check out: Forsman Symbiont News!

Check out: UCF Purple Martin Project!

Check out: Orlando Wetlands Survey Project!

Symbiosis ~ συμβίωσις ~ “Living together”

Merriam-Webster defines symbiosis as “the living together in more or less intimate association or close union of two dissimilar organisms”. Although we often synonymize mutualism and symbiosis, the former refers to only one category of the latter. Symbioses also include commensal and parasitic relationships. Host-associated microbial communities (e.g., gut microbiome) are ubiquitous yet represent a unique type of symbiosis encompassing all possible categories thereof. The focus of the Wild Symbioses Lab at UCF is to understand the complex interactions that arise between vertebrate organisms and the myriad of organisms they associate with on a regular basis, including microbiota, parasites, and disease organisms.

Our primary study systems are wild birds: purple martins, tree swallows, and Florida scrub jays. Although, through some exciting collaborations both at UCF and beyond we have also had the chance to work on host-microbe questions in sea turtles, frogs, and manatees! These animal hosts provide microorganisms with habitat and, thus, they impose selective pressures on microbial communities because of variation in host phenotype. Simultaneously, host-associated microbiota exert significant effects on the physiology, behavior, and ultimately fitness of the host organisms with which they are associated. Migratory birds are especially interesting because they use multiple habitat types throughout the year and presumably come into contact with a larger diversity of microorganisms and parasites than do resident species.

The immune system is the host organism’s defense against pathogens and parasites that seek to benefit at the host’s expense. Immunological surveillance of external and internal surfaces allow for rapid detection of intruders and deployment of appropriate defense mechanisms. The immune system also serves as a mediator between the host and commensal or beneficial microorganisms, ensuring that the line between friend and foe remains sharply defined. Some parasitic organisms have even figured out how to manipulate the host immune system to suppress defenses so that the two may co-exist for extended periods of time. We also know that capacity to recognize foreign antigens and quality of lifetime immune function are highly dependent on antigenic tutoring by host-associated microbiota during early life in such a way that host fitness would be severely curtailed in that absence of these microbial instructors.

The questions that we address in the Wild Symbioses Lab are primarily host-centric. We are interested in understanding how the microorganisms and parasites that live in, on, and around wild birds influence individual immune strategies over both ecological and evolutionary time. Our questions tend to focus on particularly costly life history stages where trade-offs between competing demands may be evidenced. For example, breeding birds are constrained by the amount of time and energy that they have available to allocate between reproductive activities and self-maintenance (e.g., immune responsiveness). The scales may tip in favor of one or the other in response to a variety of factors such as food availability, predation pressure, disease/parasitism risk, mate quality, and likelihood of future reproductive opportunities. Rapidly developing chicks also face developmental trade-offs during the relatively short amount of time available to them before need to be independent, which for altricial species like swallows occurs at fledging. Some of these fascinating trade-offs may not be observable until we take a step back and compare life history strategies across a larger geographic area large enough to encompass significant variation in relevant factors (e.g., pace of life).

To address questions relating to the interactions between wild birds and their associated microbial communities, pathogens, and parasites, my research program consists of two central themes: host physiology (primarily immunology) and microbial ecology. Our work is necessarily interdisciplinary and hence draws upon multiple fields of study to extend theoretical frameworks by applying novel techniques to non-model systems.

Eco-Immunology

The central theme of my research program addresses the physiological development and immunological function of host organisms in the context of their interactions with associated microbiota. Host immune defenses have evolved to identify and manage pathogenic agents either through resistance or tolerance. The immune system applies similar scrutiny to potential microbial symbionts and other “non-self” agents, effectively delineating the distinction between friend and foe. The adaptive immune system of vertebrates is flexible and its function is highly dependent on early life experiences with antigens in the neonatal environment that serve to calibrate the recognition of and interactions with microorganisms later in life. Thus, host-associated microbial communities likely contribute significant organizational effects to developing hosts in addition to activational effects throughout the host lifetime. In a recent project we modified the composition of the tree swallow nest microbiome to test the hypothesis that exposure to a reduced diversity of environmental bacteria depresses neonatal immune function, either directly through endogenous activities or through immune-based maternal effects. I am also currently involved in a collaborative study addressing the organizational effects of host-associated microbiota on amphibian gene expression.  This project utilizes massively parallel DNA sequencing of cDNA shotgun

libraries to describe the transcriptome and to quantify relative differences in gene expression between individuals. Such RNAseq studies illustrate a powerful approach to understanding host interactions and responses to their microbial environments. I am also involved in several research projects investigating the relationships between adult host immune function and host-associated microbial communities that may result from real-time activational effects or coevolution. One such study of wild tree swallows, with both comparative and experimental components, tests the hypothesis that the degree of maternal exposure to environmental microbes influences egg-mediated maternal effects.

Microbial Ecology

I am also interested in understanding how host-associated microbial communities are assembled and maintained, and how they vary over space, time, and host-defined habitat. High-throughput DNA sequencing of 16S rRNA amplicons prepared from microbial samples produce the data from which community composition is assessed and measures of alpha- and beta-diversity are calculated. Several of my ongoing projects are tasked with collecting such baseline data describing the structure of microbiota associated with wild tree swallows, sea turtles, amphibians, and manatees. Baseline data from wild systems are critical at this stage because the assembly and structure of host-associated microbiota of free-living organisms are still poorly described. Although there is a rich history of work on the biogeography of microorganisms, there is accumulating evidence that the factors that govern dispersal and assemblage dynamics differ across scales of measure. To this end, one current project is investigating the relative effects of spatial, temporal, and climatic variables on the composition of bacterial communities found in the active nests of tree swallows (Tachycineta bicolor) breeding

throughout North America at local (i.e., meters apart) and continental scales. This project is being conducted in collaboration with the Earth Microbiome Project and the Cornell Laboratory of Ornithology. A second set of projects is characterizing alpha- and beta-diversity of the adult skin microbiome and pre-metamorphic gut microbiome between and within host amphibian species and across space and time in central Florida, in collaboration with Dr. Anna Savage here at UCF. A similar study, characterizing the gut microbiome of Florida sea turtles is being conducted in collaboration with Dr. Erin Seney and Dr. Katherine Mansfield through UCF’s Marine Turtle Research Group. In addition to investigating the structure of naturally occurring microbial assemblages, my research also addresses questions pertaining to initial colonization of naïve hosts, microbial assemblage, succession, and community dynamics in the context of host-related and environmental variation. One such study is characterizing the development of the neonatal gut microbiome in wild tree swallows over the first two weeks post hatch. A second objective of this project is to investigate how colonization dynamics change with experimental modification of the bacterial communities inhabiting the surrounding nesting material that eggs and hatchlings are exposed to. Extensive research in various animal systems point to the importance of the gut microbiome to host health and, thus, gaining a better understanding of the factors that contribute to dysbiosis may help improve rehabilitation and conservation efforts.

The advent of massively parallel sequencing technology (e.g., Illumina) has revealed that microorganisms inhabit nearly every surface on earth, including external surfaces and internal tissues of living organisms. and their eukaryotic hosts. One unifying aspect underlying my group’s research activities is DNA metabarcoding, which includes the preparation and sequencing of 16S rRNA gene amplicon libraries to characterize microbial communities. More recently, the Wild Symbioses Lab has also been using DNA metabarcoding to characterize diet composition of insectivorous purple martins and house wrens and omnivorous sea turtles by instead targeting a portion of the mitochondrial genome (COI).