Most animals depend on their gut microbes for digestive help. The caterpillar, however, seems to lack resident gut microbes all together.
By characterizing the microbial composition across 124 species of caterpillars from North America and Costa Rica, Tobin Hammer and colleagues at the University of Colorado Boulder found that caterpillars do not have microbial friends living in their gut. Fecal material from the caterpillars contained several orders of magnitude fewer microbes compared to other organisms.
What they could identify from caterpillar feces, however, was different from caterpillar to caterpillar. This variability between individuals reflects the diversity of microbes found on the leaves they ate. If the caterpillar were to have a resident microbial community, the microbes across the different caterpillar individuals should be more consistent.
Hammer and co-workers took their experiment one step further – they wanted to make sure that their results actually had biological meaning. In many insects, such as the honey bee, killing off their microbial partners meant poor growth and low survival. For the caterpillar, however, antibiotics had no effect. Caterpillars grew, developed, and survived just as well with antibiotics than without suggesting that there were no beneficial microbes to kill off in the first place.
Both of these experiments show that the caterpillar’s gut is devoid of a “resident” microbial community and any microbes found in the gut are those just passing through.
So what makes the caterpillar so unfriendly for microbial persistence?
The caterpillar hindgut, where most of digestion occurs, is highly alkaline. With a pH above 10, the hindgut becomes a place nearly inhospitable for microbes. It also contains a wealth of host-produced antimicrobial peptides that kill microbes when they enter the gut. The surface of the hindgut, without nooks and crannies, makes it difficult for microbes to attach. As if that isn’t enough, the short food transit time (about 2 hours) and the continually replaced gut lining makes establishing a permanent microbial home nearly impossible.
It seems like caterpillars are keen on preventing microbes from colonizing its gut. But why would one want to block itself off from potential microbial helpers? While gut microbes do aid in digestion, they can limit the host to certain food sources or habitats, preventing diversification. The limitations of the caterpillar gut also reduce the chance of infection by pathogenic microbes. Instead of recruiting microbes to help digest food, the caterpillar produces digestive enzymes and the high pH helps them extract nutrients.
As humans, our microbial partners make up half of “our” cells. But many species besides the caterpillar have banished microbes from their bellies. In a time where the “microbiome is everything,” it is important to consider how and why some organisms became microbially independent.