On the use of microbiome science for captive breeding management practices in species conservation

Blog post by Pauline van Leeuwen and Jasmine Veitch. Read the full paper here. Featured image of Peromyscus sp. by H. Wilson.

A tiny white-footed mouse covertly scours the woodland forest, looking for a tasty snack. As she makes her way through the forest, the tall maple hardwood stands of the Rouge Valley (Greater Toronto Area) stretch far above her towards the open sky. The moonlight peers through the branches, reflecting off of this small creature’s white coat that extends from the mouse’s bottom lip, across her belly, towards petite foot pads. Huge black eyes blink out from her furry face, her keen sense of hearing and smell on high alert as she surveys her landscape. These features make her remarkably efficient as a nocturnal animal. However, as she continues her journey across the forest floor she is not alone.

Invisible to the naked eye, billions of microbes are moving throughout the forest as well. Some of these microbes are simply spectators to the agile mouse, while others are tiny hitchhikers along for the ride. And what a small world! Viruses, protozoa, fungi, archea, bacteria, all forming communities within an animal, called the microbiota. However, with all these passengers, what can we consider an animal? Is it only the host, or all its microbes as well? With advances in microbiome science, old theoretical questions have been brought back to light from another perspective.

In fact, just as large-scale ecosystems provide services to humankind, the microbiota contribute many vital services for its host. These services, or functions, are beneficial for the host and can be essential for survival (McKenney et al., 2018). In the case of the gut microbiota, it plays a substantial role in breaking down food so the host’s body can absorb and digest it. However, that’s not the only role these microbes play – they also support the body’s resistance towards invasive pathogens through direct competition and modulation of the immune system.

Peromyscus sp. by N. Hrynko

So animals are composed of both animal and microbial cells – but where do these microbes come from? We know that there are two types of microbial transmission. The first one is vertical, where a mother passes on her microbiota to her offspring, mainly during vaginal childbirth for mammals. The second type of transmission is horizontal, where microbes can be acquired throughout an individual’s life; such as from the external environment, social interactions, and diet, to name a few.

We used to think that all microbes were equally distributed across the globe but endemicity and biogeography can influence their dispersal. Some microbes are unique to specific body systems and hosts. Like Darwin’s finches in the Galápagos Islands, each host can represent an island with specific finches (or in this case microbes). Local extinctions of microbes can lead to modification of the services they provide for the host, which can have implications for a host’s survival. A good example is humans. Research on the gut microbiome in humans has already given us a sense that the transition from hunter‐gatherer and nomad societies to farming, sedentary, and then urban lifestyles has altered which microbes hang out in our gut. Especially in Western diets, the lack of fibrous foods and increased consumption of processed foods has resulted in reduction of gut bacteria diversity. Loss of these microbes has been implicated in diseases linked to impaired immune responses (asthma, allergies) and metabolic disorders (obesity, type 2 diabetes; Blaser & Falkow, 2009).

However, this phenomenon also applies to other animals and it can become critical when we consider those on the brink of extinction. Many endangered species are under our care and depend on human intervention for their survival. One tool that we possess to help these vulnerable animal populations is captive breeding programs. Offspring are raised in facilities and then released into the wild to prevent populations from collapsing in their natural habitats. Keeping animals in captivity can be somewhat similar to converting to a human westernized lifestyle, but on a much smaller time scale. Since microbes can be acquired through their external environment, captivity can change microbial communities of a host through standardized diets, reduction in natural and seasonal habitat features, and veterinary care.

Research to date shows that the transition from captivity to the wild leads to changes in the microbiome. Captive animals tend to have less diverse microbes and lower abundance, but not in all cases. If animals with distinct food strategies or gut physiology react differently to captivity, it is important to look at these microbiological processes from a wide variety of animals.

Simulating a captive breeding with white-footed mice by P. van Leeuwen

In our study, we investigated how the microbiome of a generalist and omnivorous rodent, the white-footed mouse, varies according to diet change in captivity and upon relocation to its natural habitat. The goal was to determine if a captive version of a wild diet, with non-processed foods, would foster higher gut microbial diversity compared to dry standardized pellets, once the mice where relocated in their natural habitat. Thus, this experiment simulated the effects of a captive breeding program on the animal’s microbes. We discovered that captive animals under the wild non-processed diet had more bacteria in common with their wild counterparts. Moreover, these bacteria might be beneficial for the mice in terms of food degradation and assimilation.

These results are encouraging and show that management practices in captive breeding programs can be modified to limit the impacts of captivity on an animal’s microbiome and potentially its survival back into the wild. However, questions remain on the actual survival and reproductive success of these relocated mice. More work is needed to look at the specific function of each microbe to its host and to monitor relocated animals in the wild to investigate if changes in management practices have long-term effects. Moreover, similar research into different species with other feeding strategies is highly encouraged. For example, our future work will investigate how herbivorous rodents might experience different changes in their microbiome, like the endangered Vancouver Island Marmot. Thinking back to the tiny white-footed mouse cruising about the woodland forest, one might think twice about what defines the boundaries of an individual. Does she alone make up an animal, or do all her invisible passengers make her what she is?

Back to wild by Pauline van Leeuwen

Blaser, M. J., & Falkow, S. (2009). What are the consequences of the disappearing human microbiota? Nature Reviews Microbiology, 7(12), 887–894. doi: 10.1038/nrmicro2245

McKenney, E. A., Koelle, K., Dunn, R. R., & Yoder, A. D. (2018). The ecosystem services of animal microbiomes. Molecular Ecology, 27(February), 2164–2172. doi: 10.1111/mec.14532

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