Donohue: A phylogenetic Approach to Microbiome Composition Using the Lemurs of Madagascar

There have been few formal attempts to understand the factors driving prokaryote diversification in a phylogenetic context. Diverse prokaryotic communities have inhabited every ecosystem on earth for over 3 billion years, yet little is known about the relative contribution of ecological and evolutionary forces influencing their diversity and composition [1]. Phylogeny provides a powerful approach for disentangling the combined roles that evolutionary history and other abiotic and biotic factors play in shaping these microbial communities. The gut microbiome offers a particularly interesting microbial system, as investigations across host species from divergent clades in the tree of life can reveal information about host diversification, ecology, and diet through evolutionary time [2]. While numerous methods exist for the study of species diversification and biodiversity for eukaryotic organisms, few have been developed for prokaryotes. This deficit is due in large part to the complexities of reconstructing prokaryotic phylogenies, which arise from difficulty in calibrating microbial divergence times, rampant horizontal gene transfer, and low taxonomic resolution [2]. A novel phylogenetically informed approach developed in [2], beta diversity through time (BDTT), provides an important first step towards understanding the systematics of prokaryotic communities. BDTT explores the factors driving patterns of gut microbiome composition similarity within more closely related taxa, referred to as “phylosymbiosis.” Phylosymbioses arise from a combination of vertical inheritance (coevolution) and the horizontal inheritance of common bacteria given similar host behavioral and/or environmental traits (convergent evolution). BDTT is unique in that it builds uncertainty about bacterial transmission into the model, and is dependent on accurate reconstructions of branching order, not divergence times, to reveal information about prokaryotic diversification. Implementing BDTT in diverse host systems with rapid host radiations will provide new insight into microbiome systematics. Whether host evolutionary history or ecology exerts a stronger influence in shaping the gut microbiome remains controversial [2,3,4]. [2] employed BDTT to determine whether phylosymbioses in 33 mammal species were best explained by host phylogeny or major dietary shifts, finding that diet drives the horizontal acquisition of ancient bacterial clades while host phylogeny best explains the presence of recently acquired OTUs (operational taxonomic units). Although no other studies to my knowledge have applied prokaryote-specific phylogenetically informed methods to microbiome research, coarse surveys across divergent hosts reveal similar patterns [5,6,7]. A more complex set of factors is expected to be involved in structuring microbiomes among more closely related species. Initial research, which relies on host identity (species classification) as a proxy for phylogeny, shows evidence for the coevolution of hosts and gut microbes, with origins independent of diet, in bears [8], great apes [9], and bats [10]. For instance, giant pandas still harbor gut microbiomes more similar to other bears than other bamboo specialists [8]. This pattern of phylosymbiosis among recently diverged and closely related taxa aligns with large-scale findings across mammals [2] and the invertebrate phylum Porifera [11]. However, it is unclear whether this pattern holds given variables such as rapid host radiation, stochastic environmental change, and niche diversity. [4] provides a first attempt at unraveling these complicated dynamics, finding that on the island nation of Madagascar, habitat type influences microbial composition more than host identity or diet in 3 widely distributed species of brown lemurs. The first chapter of my dissertation aims to utilize recently developed phylogenetic comparative methods to expand our understanding of microbiome evolution in lemurs. By incorporating taxonomically and environmentally robust datasets, I aim to determine the relative role of ecological and phylogenetic factors driving phylosymbiosis in these diverse but closely related primates. To meet this goal, I will address the following questions: (1) What are the relative contributions of host ecology and evolutionary history in shaping the community composition of the lemur gut microbiome through time? (2) Are similarities in microbiome communities driven primarily by coevolution or convergent evolution? Finally, (3) are phylogenetic signals of microbiome composition stable through time? I hypothesize that based on the literature reviewed above, (H1) host phylogeny exerts a stronger influence on microbiome composition in recently diverged clades through coevolution, while host habitat and diet determine the composition of ancient and persistent OTUs through convergent evolution and (H2) phylogenetic signals of microbiome composition degrade over time.