My gut microbiota made me do it!

Our bodies are teeming with bacteria: for every one human cell in your body, there are at least 10 microbial cells. That’s about 100,000,000,000,000 microbes – what are they all doing?

The communities of microorganisms that live on or in a particular host are called the microbiota, and are responsible for a lot of physiological and biochemical functions. It’s probably no surprise that the gut microbiota digest complex molecules we’ve eaten and they keep pathogens from colonizing our bodies (most of the time). They synthesize vitamins and amino acids that we can’t make ourselves. Recent studies have shown that variation in gut microbiota are associated with obesity, diabetes, normal brain development and insulin signaling (which has a downstream affects on body size and developmental rate). But there’s one effect that variation in microbiota can have on their host that is particularly fascinating to me: they can influence host mate choice.

In 1989, Diane Dodd reared fruit flies (Drosophila pseudoobscura) from a common stock on two different food sources: starch and maltose. She found that after multiple generations of isolation on their separate substrates, starch-flies preferred to mate with starch-flies and maltose-flies preferred to mate with maltose-flies. The result was robust and repeatable, but the reason why and its mechanism were unknown.

Fast-forward to 2010, and a new group of researchers (Sharon et al.) asked whether it might have something to do with gut microbiota.  They conducted three experiments to get at this question. First, they repeated Dodd’s experiment, this time using a different, but closely related species, Drosophila melanogaster, and got the same outcome – rearing populations of flies on different media (in this case, starch and molasses) results in assortative mating (the scientific term for choosing mates like yourself, EXPERIMENT 1 in the figure below). Second, to find out if the preference was driven by gut microbiota, they treated the flies with antibiotics before the mating trials (i.e., killing the microbiota). The preference disappeared (EXPERIMENT 2). WOW! Finally, they extracted the microbiota from the starch and molasses media that flies had been reared on, inoculated sterile molasses media with that bacteria then released germ-free flies into the environments –  the preference reappeared (EXPERIMENT 3). Even though they were both eating molasses, the bacteria in the tubes colonized the flies and caused assortative mating.

They also found that the microbes achieve this behavioral response through sex pheromones – they analyzed cuticular hydrocarbons (chemical compounds found on most terrestrial arthropods) and discovered four significantly different compounds in females and three in males that in most cases ceased to be different after antibiotic treatment.

How species form is a key question in evolutionary biology. Many researchers consider reproductive isolation necessary for two groups to be considered different species – if starch-flies mate with starch-flies, this could provide a relatively straight shot at reproductive isolation. These could literally be the first steps toward a maltose-dependent fly species (or starch-dependent) – all because there are different optimal microbial communities for different diets.

Another interesting aspect of this study pertains to the Hologenome Theory of Evolution (Zilber-Rosenberg and Rosenberg, 2008).  This theory posits that the “supraorganism”, or a host plus all it’s associated microorganisms, is the fundamental unit of selection in biology – that the association between a plant or animal and its microbiota is so strong that they exist as a single biological entity. Sharon et al.’s result seems to support this.  I know this is controversial territory (group selection and all that), but if the microbiota are vertically transmitted from parent to offspring, it is in the “best interest” of the microbiota to ensure optimal host fitness. In this case, that may be achieved by helping the host select a mate with a similar diet.  Regardless of where you fall out on the Hologenome Theory, it’s clear that in flies, the gut microbiota can influence mating behavior, and it is precisely this behavior that is thought to be important in speciation. That’s just neat.

Dodd, D. M. B. 1989. Reproductive isolation as a consequence of adaptive divergence in Drosophila pseudoobscura. Evolution 43:1308-1311.

Sharon, G., D. Segal, J. M. Ringo, A. Hefetz, I. Zilber-Rosenberg, and E. Rosenberg. 2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences 107:20051-20056.

Zilber-Rosenberg, I. and E. Rosenberg. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiology Reviews 32:723-735.

A cartoon of the experiments done by Sharon et al. (2011)

3 comments on “My gut microbiota made me do it!

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