Termites need certain gut bacteria to digest wood. Aphids require the bacteria Buchnera to provide essential amino acids. Many microbes affect host traits related to survival and reproduction.
But how exactly the microbiome might shape evolution is a mystery. The bacterial species wriggling inside a host can vary radically from generation to generation, meaning natural selection for the most beneficial microbes might not be effective. Nevertheless, the microbiome can in fact play a big role in evolution, particularly when it comes to increasing long-term host fitness, according to a recent study in Nature Ecology & Evolution.
The key boils down to environmental variation, explains lead author Marjolein Bruijning, a postdoc and evolutionary ecologist at Princeton University in New Jersey. Using evolutionary models, Bruijning and coauthors demonstrated that passing the microbiome perfectly from parent to offspring is beneficial in constant environments. But in unpredictable environments, it might be more beneficial for offspring to have a random set of microbes, Bruijning explains, “to ensure that at least some of your offspring have the right microbes for that environment.”
The controversial “Hologenome” theory, first proposed around 2008, posits that animals are a mosaic of genomes, including the host’s DNA and the DNA of all the microbes living in and on the host (See also News Feature: Do hosts and their microbes evolve as a unit?). That theory generally assumes that the microbiome affects host evolution via vertical transmission, meaning perfect transmission from mother to offspring, he says. But these latest findings break away from that assumption. “We showed that such imperfect transmission might actually be beneficial under certain conditions,” says senior author Julien Ayroles, an evolutionary geneticist at Princeton
To understand why a species would or wouldn’t pass on its microbiome to offspring, Ayroles, Bruijning, and coauthors developed an evolutionary model simulating the fitness of a population of hosts over time. The models had two key variables: First, the environment could vary from one time point to the next in the simulations, or the environment could remain constant. Second, the fidelity of microbiome transmission varied between zero (meaning that offspring always received a random set of microbes from the environment) and one (meaning that offspring always had identical microbiomes to their parents).
“We found that, in constant environments, it’s most beneficial to transmit all your microbes to your offspring,” Bruijning says, because “a host with a perfect microbial community will faithfully give it to their offspring and this will optimize fitness.” But in the changing environment scenario, populations with one microbiome could suddenly die out when conditions became unfavorable.
In the past, researchers typically assumed that the best place for offspring to acquire beneficial microbes was from their parents, and that any lack of transmission from parent to offspring was unintentional, says evolutionary biologist Kevin Foster at the University of Oxford in England. But the new study shows why it can be beneficial for a parent to “have offspring that pick up microbes from a variety of sources,” he says. “It will now be interesting to look for data to support the idea that parents are actively increasing the diversity of bacteria that offspring receive.”
Microbial ecologist Britt Koskella, a collaborator of Bruijning’s based at University of California, Berkeley, wonders how the model predictions might change if the mechanisms of microbial transfer from parent to child are included, a possibility as researchers uncover more data on transmission of the microbiome. For those species that don’t transmit a perfect copy of their microbiome, but do transfer some of it to offspring, Koskella would like to know whether the same subset of microbiota is transmitted each time, or whether a random draw is selected upon. This, she notes, would indicate whether the host is actively selecting which microbes to pass on, or truly transferring a random sample.
Ayroles’ research group is now testing the model’s predictions experimentally. Beginning with genetically identical populations of fruit flies, each with a different microbiome, the researchers will expose the flies to constant or variable stresses over time, and then measure how closely the microbiomes of the surviving offspring resemble those of their parents. “We’re going to do exactly what the model suggests,” Ayroles says. “We’re just getting that started.”
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