“Even if a transient microbiome is not associated with you,” says Alison Ravenscraft, a microbial ecologist and entomologist at the University of Texas at Arlington, “if you’re swallowing bacteria adapted to the environment, it’s possible that you could still derive a benefit from them. It would just be much harder to measure.”
Even in humans, she points out, the microbiome (including transient microbes) can shift with changes in diet or behavior. Studying living systems that don’t depend on a stable microbiome could help scientists disentangle the effects of those shifts. It could also allow them to better pinpoint the costs of having a microbiome and gain new insights into its evolution.
“If you think about it, there’s lots of reasons not to have an established microbiome,” Agashe says. “It’s actually not surprising that there are animals that have gone a different route. … But the key thing is, we don’t know why”—what factors lead to and enable the formation and maintenance of a microbiome, and conversely, what factors might prevent those relationships.
Caterpillars, dragonflies, certain ants, and other animals provide a way to investigate the potential disadvantages of long-lasting symbiotic relationships with live-in microbes; such disadvantages tend to be difficult to measure and test. Researchers suspect that these animals might be selectively avoiding certain potential penalties of symbiosis: Bacteria might compete with their host for nutrients, for instance, or aggravate the immune system.
For some animals, those risks might outweigh the potential benefits. If they have already evolved whatever enzymes or behaviors they need to live on their own, they’re no longer bound by selective pressures to acquire a microbiome. That might be the case for Hammer’s caterpillars, which eke out their herbivorous lifestyle simply by eating massive amounts of plant material. A microbiome might theoretically enable the caterpillars to manufacture additional important nutrients or go after more nutrient-dense vegetation, but the insects can make up for quality with quantity.
Another factor that might bear on the presence or absence of microbes seems to be anatomy (although Agashe does not consider it a plausible explanation, given the blurred line between cause and effect). Many of the organisms carrying few bacteria have a short, simple gut structure, essentially a tube through which food gets rapidly swept and processed. That doesn’t give microbes the time or space to gain a foothold and grow.
Ecological factors must also be considered. “If you think about how a symbiosis should or could get up,” Agashe says, “it’s actually pretty incredibly amazing.” Generation after generation, an organism has to encounter another species often enough to start a partnership that’s consistently and mutually beneficial, even under changing conditions. Agashe speculates that because her butterflies and dragonflies are constantly flitting from place to place, consuming diets that change with the location and the season, they may not meet up frequently enough with the same bacteria to establish a stable microbiome.