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The microbiome comprises a multitude of bacteria, viruses and fungi that exist in and on a multicellular organism. The interactions of body cells and the microbiome form a structural and often functional unit, the so-called metaorganism. These interactions significantly influence the biology of both the host and the associated microbes.

The Collaborative Research Center (CRC) 1182 Origin and Function of Metaorganisms at Kiel University has been investigating these interactions in detail over the last decade. One aspect that has received little attention so far is how these interactions really shape the evolution of hosts and their associated microorganisms.

To rectify this knowledge gap, researchers of the CRC, including Dr. Bob Week and Professor Hinrich Schulenburg, who is also spokesperson of the CRC 1182, joined forces with international colleagues, including Professor Brendan Bohannan from the University of Oregon and a Mercator fellow of the CRC 1182.

Based on a critical survey of existing theory, this international group of scientists are proposing several novel theoretical approaches and conceptual frameworks to stimulate and guide new research on how host–microbiome interactions shape the process and dynamics of evolution. These novel concepts are today in Nature Ecology and Evolution.

Microbiomes form a significant factor in heredity

The study of host–microbe interactions and their involvement in central life processes is at the core of current research in the life sciences. Researchers have shown in a wide range of studies that host-associated microbiomes can influence many key functions of their hosts and thereby affect the organisms' evolutionary fitness. Indeed, several studies strongly suggest that the microbiome decisively supports the host's ability to adapt to new environmental conditions and thereby shapes host evolution.

This far-reaching influence is surprising, because host-associated microbes are not necessarily transmitted from parents to offspring, while some kind of inheritance from one generation to the next is required for evolution to occur. This then raises the question of how traits mediated by the microbiome are really passed on from generation to generation.

Theoretical models show high potential to disentangle such complex relationships, identify key contributing factors, and thereby generate hypotheses for new research. In spite of the particular current interest in metaorganism research, dedicated theoretical frameworks on host–microbiome evolution are surprisingly scarce.

"Currently most biologists consider the evolutionary influence of the microbiome as a kind of extended inheritance phenomenon, for which there are already various theoretical frameworks available in evolutionary biology," emphasized Bohannan.

"However, most evolutionary theory was not developed with microbiomes in mind, and I don't think current theory is sufficient to provide a comprehensive understanding of the impact of microbiomes on metaorganism evolution. The goal of our new work is to take the first steps toward developing evolutionary theory that has host–microbiome biology at its core."

Expanding existing evolutionary concepts

The international team of authors, which also includes Professor Shelbi Russell from the University of California, Santa Cruz, and Professor Marjolein Bruijning from the University of Amsterdam, therefore scrutinized the most frequently discussed theoretical concepts to explore their application for describing microbiome-mediated evolution.

One example is a phenomenon termed niche construction. "Niche construction is comparable to farming, where a farmer grows crops and livestock to ensure the availability of food," explains first author Dr. Week, scientist in the Schulenburg group.

"In the context of the metaorganism, niche construction occurs when a host organism influences the presence of microorganisms in its environment, thereby ensuring the availability of beneficial microbes, not only during its own lifetime but possibly also during the next generation.

"Such niche construction of the environmental microbiome can thus mediate the successful transmission of microbiome-dependent functions from one host generation to the next, as an important prerequisite for the microbiome's influence on host evolution."

Creating new theoretical foundations for empirical research

In addition to the example described, the new publication highlights a total of four theoretical frameworks that show particular promise for enhancing our understanding of host-microbiome evolution.

"In order to better capture the biological diversity of these systems and enable experimental testing, the frameworks we have now presented should be carefully expanded in close collaboration with colleagues working empirically," emphasizes Prof. Schulenburg, who is also active within the priority research area Kiel Life Science (KLS).

"This is exactly one of the research foci of our CRC 1182. And with our new publication, we now provide critical theoretical building blocks that should stimulate novel research on the evolutionary consequences of host-microbiome associations in the future."