Museum specimens of teeth from mammals that lived before and after human-driven population declines will reveal how the loss of genetic diversity has disrupted the microbial communities essential to host health. Most studies of wildlife population declines have ignored the microbiome—the bacteria, fungi, and other microorganisms living in and on animals that handle digestion, immunity, and reproduction. Small, isolated populations show reduced microbial diversity, but researchers could not tell whether those changes were caused by the decline itself or by long-term unrelated processes. This project solves that problem by extracting ancient DNA from dental calculus—a microbial fossil that remains intact for centuries—from the same species before and after decline, and from stable control populations. If successful, the work will show whether population declines consistently damage host-associated microbiomes, and whether host genetics or environment drives those changes. It will also identify specific host genes and microbial species that shift together over time, and link them to oral disease in wild mammals. This is fundamental science about co-evolution under human pressure, with no immediate practical application. But understanding how microbiomes respond to genetic bottlenecks could eventually inform wildlife conservation strategies and, because many mammalian microbiomes are similar, offer clues about human microbiome disruption.
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Human actions are having a staggering impact on all life on the planet, leading to the new geological epoch, the Anthropocene. One of the greatest hallmarks of the Anthropocene is biodiversity loss, including rapid population declines of vertebrate populations, which often lead to loss of genetic diversity. Host-associated microbiomes, collection of microorganisms that live in and on the host, are central to host survival, as they provide many essential biological functions, ranging from digestion to immunity to reproductions. Disruptions of microbial communities can have severe consequences, reducing host fitness and causing disease. Microbiomes are themselves impacted by host genetics and the environment. Recognising this intimate connection between the hosts and their microbiomes, this project asks a central question: How did human-driven population declines during the last two centuries impact host-associated microbiomes and what consequences does it have for the hosts? Surprisingly, despite the fundamental importance of microbiomes, their role has rarely been considered in the context of widespread population declines. The few existing studies suggest that small, isolated populations show reduced microbial diversity and altered community composition. Experiments confirm these observations and link the resulting microbiome changes to negative fitness consequences for the host. However, the cross-sectional approach applied to wild study systems so far suffers from the inability to distinguish the microbiome responses to recent change from long-term processes that are not related to population declines. Doing this requires microbiomes from the past that pre-date the population declines. These have been unattainable until very recently because most host-associated microbiomes decompose after host death. However, microbial 'time travel' is now possible via metagenomic analysis of dental calculus, a unique microbial fossil that persists virtually unchanged through time, is abundant on teeth of diverse mammals, and is readily available from museum specimens across the last 200 years, the period of greatest human impact. By applying ancient DNA techniques and jointly analysing host genomes and microbiomes from the same individual, this project will generate fundamental new knowledge about host-microbiome co-evolution during population declines. First, by comparing microbiomes from the same population from before and after population decline (and in non-declined control populations) in 12 mammalian species, this project will investigate if population declines lead to changes in host-associated microbiomes and evaluate the relative contribution of host genomics and the environment to this change. Second, through individual-level joint analyses of host genomics and the microbiomes, we will explore the association between host heterozygosity, inbreeding and genetic load - typical genomic markers of population decline - and microbiomes and how these translate into population-level changes. Finally, we will identify specific host genes and microbial species that change through time in a concerted fashion and are related to presence of oral disease in wild mammals. This project will provide fundamental insights into anthropogenic impacts on microbiomes of wild mammals, with implications for wildlife conservation, animal and human health.
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