For the red flour beetle, life happens almost entirely in flour. From egg to larva, pupa and adult, these tiny insects live and feed in the same environment, sharing their habitat with a community of bacteria. But unlike some animals that inherit a stable set of microbes from their mothers, flour beetles appear to acquire much of their microbiome from their surroundings.
A recent study at NCBS has now revealed just how changeable this microbial community can be. Researchers found that the microbiome of the red flour beetle (Tribolium castaneum) can shift dramatically over time, between individuals and even between populations maintained under nearly identical laboratory conditions.
To understand where this variation comes from, researchers from Dr Deepa Agashe’s lab followed beetle populations over several years and conducted a series of experiments examining many experimental and beetle-associated factors.
One of the first clues came from the beetles themselves. “We found little evidence that bacteria are consistently passed from mother to offspring through the eggs or ovaries,” says Dr Pratibha Sanjenbam, the lead author of the study. “Instead, newly hatched beetles appear to acquire microbes from the flour around them.” This makes the flour much more than food. It acts as a microbial reservoir through which bacteria are acquired and exchanged between beetles. One bacterial genus (Izhakiella) repeatedly emerged as a strong coloniser of the beetles.
But not all stages of the beetle life cycle contribute equally. Larvae host a relatively high load and consistent bacterial communities. As they feed actively, their faeces add bacteria back into the flour, creating a rich source of microbes for others. Even a short period of exposure to larval faeces was enough to increase and make beetle microbiomes more similar to one another.
Adults on the other hand, carry very low bacterial loads, leading to higher variation in bacterial communities. They also secrete chemical compounds called quinones from specialised stink glands. These compounds have antimicrobial properties and can suppress bacteria in the flour. The researchers found that different bacteria respond differently to these chemicals, suggesting that quinones may help determine which microbes survive.
The result is a constantly shifting microbial landscape. Larvae can build up bacterial communities, while adults can suppress them.
Pratibha and team found another source of bacterial community instability hiding in a routine laboratory practice - changing the flour. “Fresh flour contains very little bacterial inoculum. When used flour is replaced, much of the accumulated microbial community is removed,” says Pratibha. This replacement often happens when there are few feeding larvae left, meaning there are fewer sources of fresh bacterial inoculum. As new adults emerge, their quinones can further suppress the remaining bacteria.
The team observed that bacterial levels in the flour dropped sharply after a flour change and then gradually increased again as larvae became more abundant.
These cycles help explain why two beetle populations that began with the same ancestors and were maintained in the same laboratory can end up with noticeably different microbiomes. This kind of change, driven by chance events in which microbes colonise, survive or disappear, is known as ecological drift.
Earlier work had suggested that the flour microbiome could improve beetle fitness, including reproduction and survival. But if this microbiome is beneficial, why has the beetle not evolved a more stable relationship with them? To find out whether these effects held up over time, the researchers repeated their earlier experiments over multiple years. This time, the results were different: in most experiments, disrupting the microbiome did not significantly change female fecundity, and adding larval faecal microbes did not consistently improve fitness either.
“We think that microbiome drift may have contributed to this changing outcome. A beneficial bacterial community present in an earlier population may simply have been lost over time,” says Pratibha. This does not mean that the beetle microbiome is unimportant. Instead, the study suggests that the beetle’s lifestyle may mean it can never develop a lasting partnership with the flour microbiome.
“This particular project was a very long and winding journey, requiring years of experiments and hard thinking by many lab members,” says Dr Deepa Agashe, the Principal Investigator of the study.
“Our early results were very perplexing, because we were approaching it from the mindset that there was a specific, beneficial microbiome! I am still surprised by the wild fluctuations in the bacterial community in controlled laboratory conditions that we observed. To me, it drives home the possibility that many other host species — like our beetles — may have life histories that are not conducive to establishing a stable mutualism with microbes. So many factors seem to oppose deterministic community assembly that the evolution of tight relationships may be a relatively rare event. I would love to know if this is true.”
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