A new study of fruitflies found that the friendly bacteria that live in and on their bodies can influence mating preference, which is sustained over generations, suggesting that such “commensal” bacteria can push the evolution of their host species; the finding also adds weight to the idea that the host animal (or plant) and all of its associated microorganisms are the unit of selection in evolution.

The new study is the work of Gil Sharon, from the department of Molecular Biology at Tel-Aviv University in Israel, and colleagues, and was published online before print on 1 November in the Proceedings of the National Academy of Sciences, PNAS.

Commensal bacteria live in mutually beneficial symbiosis with their hosts: the human body for example contains more of these beneficial bacterial cells than human cells, helping us to digest food and acquire nutrients like vitamins B and K, and helping our immune system fight bacteria that cause diseases.

The mainstream theory in modern evolutionary biology is that the unit of selection in evolution is the individual or gene. However, there is a competing theory, put forward by Wilson and Sober in the 1980s, that “superorganisms” comprising large groups or communities of co-operating species are also functionally organized to survive and adapt as a unit, and not all adaptations occur at the level of the gene or the individual.

Another theory that fits the superorganism framework is the “hologenome theory of evolution”, put forward a couple of years ago by Israel-based husband and wife team Eugene Rosenberg and Ilana Zilber-Rosenberg, who are also co-authors of this latest fruitfly study.

The hologenome theory says the “holobiont”, the animal or plant with all of its on-board microorganisms is the unit of selection in evolution, and that all of the diverse microbiota are part of this evolving superorganism. The hologenome is therefore the sum of the genomes of all the species in the holobiont, comprising all the genetic information of the host and its microbiota.

For the context of the fruitfly study, Sharon and colleagues started with the widely held idea that changes in mating preference are an early step in the evolution of new species.

They divided a population of Drosophila melanogaster and reared one half on a molasses medium and the other half on a starch medium, thus creating a significant change in their environment.

When they then mixed the populations together, they found that flies reared on molasses preferred to mate with others also reared on molasses, and the same with the starch-reared flies.

They found that this mating preference appeared after only one generation and held for at least 37 generations.

When they treated the flies with antibiotics, this preference vanished, suggesting it was something to do with the commensal bacteria living on and in the flies. They confirmed this by reinfecting the antibiotic-treated flies with bacteria-rich samples taken from them before they were treated.

By analysing the genetic information of the bacteria, they came up with a candidate that was most likely responsible for the mating preference change: Lactobacillus plantarum, which made up 26 per cent of the commensal bacteria in the starch flies and only 3 per cent of the bacteria in the molasses flies.

Their suspicions were confirmed when they again treated the flies with antibiotics and then reinfected them with a mixed culture of Lactobacillus species and a pure culture of Lactobacillus plantarum isolated from the starch-fed flies.

After some further analysis, which they still need to work on, Sharon and colleagues have tentatively proposed that the bacteria were changing the levels and chemical mix of the sex pheromones emitted by the flies to attract mates.

The crux of the experiment, as far as lending support to the superorganism concept and the hologenome theory, is the fact that the mating preference effect lasted for 37 generations.

This “very rapid and long lasting effect” could be enough to influence speciation, Mike Ritchie, an evolutionary biologist at the University of St Andrews in the UK, told Nature News.

Further research is now needed, to answer a wealth of other questions, for instance, to find out how the bacteria are passed onto new generations, and if the same process occurs in the wild.

“Commensal bacteria play a role in mating preference of Drosophila melanogaster.”
Gil Sharon, Daniel Segal, John M. Ringo, Abraham Hefetz, Ilana Zilber-Rosenberg, and Eugene Rosenberg.
PNAS, Published online before print 1 November 2010.
DOI: 10.1073/pnas.1009906107

Additional sources: Nature News, ROAR, Zilber-Rosenberg & Rosenberg (FEMS Microbiol Rev, 2008), Wilson & Sober (J Theor Biol., 1989).

Written by: Catharine Paddock, PhD