It is widely accepted that all animals and plants host diverse microbial communities that are vitally important for their functioning and survival. In many cases, these microbiomes can be at least partially heritable, being passed from parent to offspring. Thus, when environmental changes occur, we would expect to see alterations not only in hosts’ physiology over subsequent generations, but also in their microbiomes.
Husband-and-wife team Eugene Rosenberg and Ilana Zilber-Rosenberg of Tel Aviv University in Israel proposed this concept a decade ago (FEMS Microbiol Rev, 32:723–35, 2008). A host organism and its resident microbes—the so-called holobiont—functions as a whole on multiple levels, they argued, from the gene and chromosome to the organism’s anatomy and physiology, and acts as an independent unit of selection.
A famous example of this concept is the relationship between corals and their symbionts, the zooxanthellae. Researchers have demonstrated that some corals can evolve to tolerate higher water temperatures by changing the makeup of their symbiont communities. Because microbes have much shorter generation times than coral polyps, the genetic composition of the symbiont populations can evolve much more rapidly than that of their hosts, and these changes can confer higher tolerance on the holobiont unit.
Over the last decade, it has become evident that the idea of the evolutionary concept of the hologenome, which views the holobiont as the unit of selection, can be applied across the tree of life, with examples cropping up in plants and insects. This revelation motivated us to explore the relevance of the microbiome to the adaptation of so-called poikilothermic animals, which are unable to maintain a stable body temperature using internal mechanisms. Specifically, we set out to answer whether host selection for an environmental stressor such as cold exposure results in selection of fishes’ associated microbes.
We bred tropical blue tilapia, which are typically found in marine environments with high water temperatures of 24–28 °C. Over three generations, we selected for fish whose siblings had high survival rates in low-temperature conditions. We then compared the gut microbiomes of genetically cold-resistant fish to those of cold-sensitive fish. Despite having never experienced low-temperature environments themselves, these two groups had different gut microbiomes as a result of the selection. Moreover, when we challenged all these fish in low-temperature conditions, cold-resistant fish’s gut microbiomes were more stable, as were the fish’s transcriptomes. Thus, our selection regime shaped both the host and its associated microbiome to be more resilient to drops in temperature (eLife, 7:e36398, 2018).
These findings are no doubt just one example of coordination between a host and its microbes. As the evolutionary concept of the hologenome matures, researchers will likely document many more plant and animal communities that evolve with their microbiomes. It remains to be determined whether a microbiome’s compositional changes directly affect its host’s physiological response to changing environmental conditions. But the hologenome concept will undoubtedly influence our understanding of the evolution and ecology of all organisms.
Clarification (July 2): This story has been updated to account for the possibility that others may have proposed the hologenome idea before Eugene Rosenberg and Ilana Zilber-Rosenberg, though the husband-and-wife team popularized the concept through several peer-reviewed publications.