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Small and fragmented populations are at high risk of local extinction, in part because of elevated inbreeding and subsequent inbreeding depression. A major conservation priority is to identify the mechanisms and extent of inbreeding depression in small populations. The eastern massasauga (Sistrurus catenatus) rattlesnake is listed as Federally Threatened in the United States, having experienced significant habitat fragmentation and concomitant population declines over the past 200 years. Here, we use long-term monitoring of two wild populations of eastern massasaugas in Michigan to estimate the extent of inbreeding in each population, identify mechanisms that generate inbreeding, and test for the impact of inbreeding on fitness. Using targeted genomic data and spatial coordinates of capture locations from over 1000 individuals, we find evidence of inbreeding and link inbreeding to spatial kinship structure within populations, possibly driven by limited dispersal. We reconstruct multigenerational pedigrees for each population to measure reproductive output and use long-term capture–recapture data to estimate individual survival (i.e., the two major components of fitness). We find evidence of inbreeding depression in both fitness metrics. The 5% most inbred individuals are 13.5% less likely to have any surviving offspring and have 11.6% lower annual survival compared to all less inbred individuals. By combining genomics and long-term monitoring data, we are able to link the life history of eastern massasaugas to inbreeding and detect relationships between fitness and inbreeding. These insights provide important conservation context for future management and for understanding how spatial structure can generate inbreeding depression even at fine spatial scales. 

ABSTRACT The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution.