Avian Symbionts of Sulawesi: Identifying and Correlating Malaria Parasites and the Microbiome in Communities of Endemic Avian Hosts

Author

Rachael Joakim, The Graduate Center, City University of New YorkFollow

Date of Degree

2-2024

Document Type

Dissertation

Degree Name

Ph.D.

Program

Biology

Advisor

Susan Perkins

Committee Members

Ana Carnival

Michael Hickerson

Sergios Kolokotronis

Rauri Bowie

Subject Categories

Biodiversity | Computational Biology | Evolution | Molecular Genetics | Ornithology | Other Ecology and Evolutionary Biology | Parasitology

Keywords

Sulawesi, avian malaria, Haemosporida diversity, community ecology, island biogeography, species turnover

Abstract

Since the evolution of complex organisms, there have been communities of symbionts inhabiting them. Thanks to the development of parallel sequencing techniques, DNA of entire microbial communities can be sequenced from a single sample. Some microbes can be parasitic in nature, such as Haemosporida, an order of eukaryotes causing malaria. While most symbionts form a more commensal host relationship in wild systems, host-symbiont dynamics can vary in pathogenicity based on biotic and abiotic factors. In vertebrates, microbial communities in the gut play a major role in host function, including immune responses to Haemosporida. Though this relationship is most commonly explored in mammalian systems, there is a stark gap in knowledge for avian hosts. Further, birds harbor the most diverse range of Haemosporida, accounting for over half of described lineages. My dissertation explores these symbiotic relationships in communities of birds on Sulawesi, Indonesia: an island notorious for its complex geological origins and highly localized endemism. Blood samples and cloacal swabs were collected from birds during six expeditions across the island to i) determine a baseline of intraspecific variability in gut microbiomes across multiple populations, ii) identify and compare haemosporidian parasites recovered from highly dissimilar avian communities, and iii) explore the potential for gut microbiomes to assess parasite pathogenicity in three host genera.

Prior to investigating the role of gut microbiome structure in host immune function, it is necessary understand the stochasticity of commensal microbes in wild systems. As a host’s environment provides the source pool of available microbes, differences in available microbes can shift the diversity and relative abundance of host symbiotic communities, even between populations of the same species. Using the most abundant bird species, Pellorneum celebense (Sulawesi babbler), In Chapter 1, I determined the range of intraspecific microbe communities across three isolated populations. Using statistical models, I also tested the effects of biotic and abiotic factors on avian gut microbiomes in previously studied host tropical communities. Model results suggest hosts inhabiting different mountains, despite the likelihood that no connectivity exists between any two locations, have highly similar gut microbiome composition. Only elevation appears to influence gut microbiome composition in P. celebense populations, where individuals in higher elevations had lower gut microbial diversity.

Until a recent study of Papuan avian communities, Haemosporida parasites in Indonesian birds have been relatively unexplored. In fact, the entire region of Southeast Asia represents only 0.05% of the global avian malaria database, despite the vast species-rich tropical avian communities present. Given the severe lack of data from this region, community-level parasite assessment was conducted for four sampling sites in Chapter 2. Due to the isolated nature of Sulawesi’s endemic communities, in this chapter I quantified community dissimilarity and host-parasite interactions across four sampling locations. Characterizing the avian Haemosporida communities in multiple regions of Sulawesi provides data to the global malaria database from a poorly represented region. The high degree of community dissimilarity, inconsistent host preferences, and evidence of local variance supports current biogeographic theories and provides new context in which to understand the evolutionary processes driving the unique biodiversity of this island.

To evaluate the use of gut microbiome analyses as an indicator of host fitness, Chapter 3 explored microbiome community dynamics in relation to Haemosporida infection status in the three most abundant host genera. Six species of Zosterops, Ficedula, and Myza hosts were used for this study, as they represent a range of dietary preferences and share several Haemosporida lineages. While no discernable patterns in gut microbiome community statistics emerged to suggest a general correlation with Haemosporida presence, parasite presence correlated with microbial variance when considering genus as a factor, suggesting parasite-specific immune-related shifts. Results from this chapter support the general conclusion that lineages from the three genera infecting birds, Leucocytozoon, Parahaemoproteus, and Plasmodium, vary significantly in pathogenicity, but the majority of lineages endemic to a host community pose a limited fitness cost. However, limited occurrences of previously described Plasmodium pathogens correlated with lower microbiome diversity and abundance which may indicate a recent introduction. As this parasite was only identified in three Zosterops spp. from a single location, however, it is difficult to determine the extent and variability of its host preferences.

Recommended Citation

Joakim, Rachael, "Avian Symbionts of Sulawesi: Identifying and Correlating Malaria Parasites and the Microbiome in Communities of Endemic Avian Hosts" (2024). CUNY Academic Works.
https://academicworks.cuny.edu/gc_etds/5709