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Not Exactly Rocket Science
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Gut bacteria change the sexual preferences of fruit flies

Mating_drosophila

Imagine taking a course of antibiotics and suddenly finding that your sexual preferences have changed. Individuals who you once found attractive no longer have that special allure. That may sound far-fetched, but some fruit flies at Tel Aviv University have just gone through that very experience. They’re part of some fascinating experiments by Gil Sharon, who has shown that the bacteria inside the flies’ guts can actually shape their sexual choices.

The guts of all kinds of animals, from flies to humans, are laden with bacteria and other microscopic passengers. This ‘microbiome’ acts as a hidden organ. It includes trillions of genes that outnumber those of their hosts by hundreds of times. They affect our health, influencing the risk of obesity and chronic diseases. They affect our digestion, by breaking down chemicals in our food that we wouldn’t normally be able to process. And, at least in flies, they can alter sexual preferences, perhaps even contributing to the rise of new species.

Sharon was inspired by experiments by Diane Dodd, who raised two strains of fruit flies on different diets, and found that after 25 generations, their menus had affected their sex lives. Those reared on a menu of starch preferred to mate with other ‘starch flies’, while those reared on maltose had a bias towards ‘maltose flies’. These results were odd. Dodd had set up an artificial evolutionary pressure for diet but somehow, the flies’ mating habits had changed as well.

To work out why, Sharon repeated Dodd’s experiment with the fly Drosophila melanogaster, and raised two strains on either molasses or starch. After just two generations, she found the same effect that Dodd did: the flies were more attracted to individuals reared on the same diets. Something in their food was changing their behaviour.

Bacteria in our guts change according to the food that we eat, so Sharon suspected that something similar was happening in the flies. This idea was dramatically confirmed when he gave the insects a dose of antibiotics. Immediately, their sexual bias disappeared and they were just as likely to mate with flies from either group.

As further evidence, Sharon isolated bacteria from the food that the flies had eaten and added them to vials of sterile food. When the antibiotic-treated flies ate this food, laced with a drizzle of bacteria, they regained their sexual preferences after a single generation. Those that ate food containing ‘starch bacteria’ preferred to mate with starch flies, and those that ate food containing ‘molasses bacteria’ preferred to mate with molasses flies.

Many bacteria are probably responsible for this effect but Sharon singled out Lactobacillus plantarum for special attention. It’s particularly common in starch-based food and while every molasses fly harbours around 2,600 of these bugs, starch flies contain around 23,000 apiece. After a dose of antibiotics, flies that are infected with this bacterium alone take a fancy to starch flies over molasses flies.

It’s possible that the bacteria influence the levels of sex pheromones that affect the fly’s attractiveness, either by producing those chemicals themselves or stimulating the fly to do the same. That’s not too far-fetched: bacteria can alter the smells given off by many animals, and smell certainly affects sexual behaviour. Indeed, Sharon found five different chemicals that are present at different amounts on the outer shells of starch and molasses flies. Antibiotics brought the levels of these chemicals down to similar levels. For a fruit fly, these seem to be the smells that make the differences between striking lucky and getting rejected.

These experiments could have important implications for the origin of new species. Imagine that two wild populations of the same species mate with each other less and less often, because they start to harbour different bacteria (just as the starch and molasses flies did). The stronger these preferences, the greater the odds that these populations will diverge into separate species.

Diet, of course, is just one thing that affects the membership of the bacterial club in our bodies, so it’s unlikely that a species would split in two just because two groups started eating different foods. However, Sharon speculates that diverse diets could intensify the effects of other barriers that restrict the flow of genes, such as physical obstacles.

In any case, the study suggests that you can’t understand an animal’s evolution simply by considering the evolutionary pressures that act on its genome. You also have to consider the genes of the bacteria and other passengers that live inside it, which also create variations in its behaviour and affect is chances of survival. Sharon calls this the hologenome – the combined genes of a host and all the microbes it contains.

Reference: PNAS http://dx.doi.org/10.1073/pnas.1009906107

More on the microbiome

  • An introduction to the microbiome
  • You are what you eat – how your diet defines you in trillions of ways
  • Gut bacteria in Japanese people borrowed sushi-digesting genes from ocean bacteria
  • The bacterial zoo in your bowel
  • Gut bacteria – fat or thin, family or friends, shared or unique
  • Human gut bacteria linked to obesity

An introduction to the microbiome

<p>You could be sitting alone and still be completely outnumbered for your body is home to trillions upon trillions of tiny passengers – bacteria. Your body is made up of around ten trillion cells, but you harbour <em>a hundred </em>trillion bacteria. For every gene in your genome, there are 100 bacterial ones. This is your ‘microbiome’ and it has a huge impact on your health, your ability to digest food and more. We, in turn, affect them. Everything from the food we eat to the way we’re born influences the species of bacteria that take up residence in our bodies.</p>
<p>This slideshow is a tour through this “<a href="http://www.nytimes.com/2010/07/20/opinion/20tue4.html?_r=1">universe of us</a>”. Every slide has links to previous pieces that I’ve written on the subject if you want to delve deeper. Or download a podcast of <a href="blogs.discovermagazine.com/notrocketscience/2011/10/19/i-microbes-my-radio-4-talk-on-the-hordes-of-microbes-inside-us/">my Radio 4 programme on these hidden partners</a>.</p>
<p>Image by David Gregory &amp; Debbie Marshall, Wellcome Images</p><p>To our microbiome, the human body must seem like an entire planet, full of different ecosystems. This is especially true for those that <a title="Permanent Link to The bacterial zoo living on your skin" href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/06/23/2009/05/28/the-bacterial-zoo-living-on-your-skin/">live on our skin</a>. At the microscopic scale, the hairy, moist surface of your armpits is as different from the smooth, dry skin of your forearms as a rainforest is to a desert.</p>
<p>In a thorough survey of our skin microbiome, Elizabeth Grice identified species from at least 205 different genera. Your forearm has the richest community with an average of 44 species, while your nostril, ears and inguinal crease (between leg and groin) are the most stable habitats. Grice also found at bacteria from a specific body part have more in common than those from a specific person. Your butt microbes have more in common with mine than they do with your elbow microbes.</p><p>Despite its diversity, the skin microbiome is a tiny country village compared to the <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/06/23/2010/03/03/the-bacterial-zoo-in-your-bowel/">bustling metropolis inside your bowels</a>. The dark corridors of your intestine house more bacteria than any other part of your body. A team of international scientists led by Junjie Qin and Ruiqiang Li discovered that each of our bowels carries at least 160 bacterial species. Together, our collective guts have just under 3.3 million bacterial genes, more than 150 times as many as reside in our own genomes. They also showed that the gut microbiome of a healthy person looks very different to that of someone with a bowel condition like Crohn’s disease or ulcerative colitis.</p>
<p>Despite this diversity, Peer Bork has shown that the gut bacteria of people from Europe, North American and Japan collapse <a href="http://blogs.discovermagazine.com/notrocketscience/2011/04/20/divided-by-language-united-by-gut-bacteria-%e2%80%93-people-have-three-common-gut-types/">into three enterotypes, or gut types</a>. These clusters cut across age, gender, body weight and nationality. Each produces energy in a slightly different way, manufactures a different vitamin and may affect our susceptibility to different diseases.</p>
<p>The quest to understand gut microbes may seem like an arcane niche of science, but it’s actually very important for public health. We rely on these microscopic passengers more than we realise. They harvest energy from our food, provide us with nutrients that would otherwise be denied to us, prevent the growth of harmful bacteria, and more. In many ways, they’re like a forgotten organ. They can also go rogue, changing their community in ways that are linked to obesity or bowel diseases.</p>
<p> </p>
<p>Image by Med. Mic. Sciences Cardiff Uni, Wellcome Images</p><p><a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/06/23/baby%e2%80%99s-first-bacteria-depend-on-route-of-delivery/">We inherit our microbiomes from our mother</a>, picking up billions of them as we slide from her largely bacteria-free womb through her microbe-laden vagina. Being slathered in vaginal microbes might not seem like much of a treat but it’s vital for a newborn.</p>
<p>Babies end up with a very different portfolio of skin and gut bacteria depending on how they are delivered. Those who are born naturally harbour a more diverse array of bacteria, which resemble those in their mother’s vagina, including several species that are important for digestion. Those who are delivered by C-section are colonised by a less diverse array of bacteria, including some like <em>Staphylococcus</em> that are picked up from the hospital environment.</p>
<p>These early differences could directly affect a baby’s health for these first colonisers determine which the species that will follow. The bacterial heirlooms that babies inherit from their mothers might act as a shield, preventing more dangerous microbes like from setting up shop. By changing baby’s first bacteria, C-sections could alter the make-up of their later communities, leading to long-term effects on health and nutrition.</p><p><a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/08/03/you-are-what-you-eat-%e2%80%93-how-your-diet-defines-you-in-trillions-of-ways/">Our microbiome is like a hidden organ</a>, helping us to break down foodstuffs that our own cells cannot cope with. And in turn, our food affects our microbiome. Our first set is laden with genes for digesting milk proteins, allowing us to make full use of our only source of nourishment as babies. Breast milk might even have evolved to nourish the most beneficial bacteria with special sugars.</p>
<p>Just before we move onto solid foods, our microbiome starts activating genes that break down the complex sugars and starches in plants, preparing us for the menu to come. As our diet diversifies, so do our bacteria. They activate genes that use carbohydrates effectively, produce vitamins, and break down unusual and diverse chemicals. As adults, our microbiome becomes relatively stable, but its membership roster depends on the food we eat. The guts of African villagers who eat high-fibre diets are dominated by plant-digesting specialists, which are much rarer in the guts of Europeans who eat high-fat diets.</p><p>Before the age of better food hygiene, our meals used to provide a rich source of foreign bacteria that our microbiome could plunder for genetic tools. Bacteria trade genes as easily as humans trade gifts. For example, the gut bacteria of Japanese people have borrowed genes from a marine species, which now <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/04/07/gut-bacteria-in-japanese-people-borrowed-sushi-digesting-genes-from-ocean-bacteria/">allows them to digest the special carbohydrates in seaweed</a>. The marine bacterium eats seaweed, including the types that are used to make nori, a common sushi ingredient.  In the past, when diners wolfed down morsels of nori, some also swallowed seaweed-eating bacteria, which traded genes with those in their own guts.</p>
<p>This wouldn’t happen nowadays because nori is roasted before being eaten. In fact, processing food presents a blockade to bacteria from the outside world and as a result, Western gut communities have become gentrified. They lack genetic diversity, and they have few ways of increasing it.</p>
<p>Images by Alice Wiegand, Alex Kovach, Tristan Barbeyron and Mirjam Czjzek</p><p>The microbiome is more than just our partners-in-digestion – they affect our health too. They have been linked to a variety of medical conditions, including allergies, immune diseases, and even obesity. For example, the balance of the two major groups – the Bacteroidetes and Firmicutes – <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/06/23/2008/10/06/human-gut-bacteria-linked-to-obesity/">could influence our body weight</a>.</p>
<p>Fat mice and humans have a less diverse milieu of gut bacteria, with a <a href="http://blogs.discovermagazine.com/notrocketscience//notrocketscience/2008/12/01/gut-bacteria-fat-or-thin-family-or-friends-shared-or-unique/">greater proportion of Firmicutes to Bacteroidetes in their bowels</a>. This ratio increases if we eat high-fat diets and falls if we eat low-fat diets. And if the gut bacteria from fat mice are transplanted into mice with no gut bacteria of their own, they can make the new hosts overeat and pile on the pounds. This research suggests that gut bacteria could be manipulating us for their own ends. Some species send out signals that make us hungrier, encourage us to eat more, and affect the way we store fat. And some of our immune genes help to moderate these signals.</p>
<p>As we learn more about our bacterial partners, we might eventually find ways of influencing them to improve our health. This is already happening. In 2008, Alexander Khoruts from the University of Minnesota managed to cure a woman with a “vicious gut infection” by giving her <a href="http://www.nytimes.com/2010/07/13/science/13micro.html?_r=2&amp;pagewanted=1">a transplant of her husband’s gut bacteria</a>.</p><p>What happens in the gut doesn’t stay in the gut – it sometimes affects the brain. Animal studies have started to show that the microbiome, from its staging ground in the bowel, can influence the development of its host’s brain.</p>
<p>Rochellys Diaz Heijtz found that <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2011/01/31/gut-bacteria-steer-the-development-of-the-young-brain/">germ-free mice, without any microbiome</a>, were more active, less anxious and less risk-averse than usual. Their brains differed in the activity of over a hundred genes that provide cells with energy, influence chemical communications in the brain and strengthen the connection between nerve cells. Heijtz could even shift her germ-free mice towards “normal” behaviour and genetic activity by giving them a microbiome transplant, but this only worked early in their lives.</p>
<p>But later,  Javier Bravo  at University College Cork managed to<a href="http://blogs.discovermagazine.com/notrocketscience/2011/08/29/from-guts-to-brains-%e2%80%93-eating-probiotic-bacteria-changes-behaviour-in-mice/"> change the behaviour of normal adult mice</a> by feeding them with a probiotic bacterium  called <span id="apture_prvw1" class="aptureLink"><span class="aptureLinkIcon" style="background-position: right -1348px;"> </span><span class="aptureLink snap_noshots"><em>Lactobacillus rhamnosus</em></span></span>,  often found in yoghurts and dairy products. The bacterial menu changed  the levels of signalling chemicals in the rodents’ brains, and reduced  behaviours associated with stress, anxiety and depression.</p>
<p>Meanwhile, Gil Sharon found that <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/11/01/gut-bacteria-change-the-sexual-preferences-of-fruit-flies/">gut bacteria can shape the sexual choices of flies</a>. Flies that are raised on diets of starch prefer to mate with other “starch flies” while those raised on maltose prefer “maltose flies”. When Sharon dosed the flies with antibiotics, she killed both their gut bacteria <em>and </em>their sexual preferences. If she inoculated the sterile flies with the microbiome of their peers, their preferences reappeared instantly. It’s possible that the bacteria influence the levels of sex pheromones that affect the fly’s attractiveness.</p>
<p>These studies show that you can’t understand an animal’s evolution simply by considering the evolutionary pressures that act on its genome. You also have to consider the genes of the bacteria and other passengers that live inside it. We’re each like a superorganism – a unified alliance between the genes of several different species, only one of which is human.</p>The teeming masses of the microbiome also contain a record of our evolutionary past. Howard Ochman found that the <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/11/16/gut-bacteria-recap-the-evolution-of-apes/">evolution of the gut microbes in great apes</a> perfectly recaps that of their host. The bacteria from the two species of gorilla are more closely related to each other than they are to human gut bacteria. Geography, diet and disease aside, the main thing that influences the members of these bacterial cities is the species of the host. You could reconstruct the evolution of the apes, simply by comparing the bacteria in their bowels.<p>The bacteria of our microbiome are mostly our allies. <a href="http://blogs.discovermagazine.com/notrocketscience/2011/10/13/beneficial-gut-bacteria-can-become-virus-collaborators/">But they can also they can be turned against us.</a> Two new studies in mice have found  that viruses - including one that causes polio, and another that causes cancer - can exploit gut bacteria to infect our bodies.</p>
<p>They use molecules on the bacteria's surfaces as reins, to ride towards host cells, or backstage passes to sneak past the immune system. Our microscopic allies can turn into  unwitting collaborators for dangerous infections.</p>
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November 1st, 2010 Tags: Bacteria, fruit fly, mating, microbiome, Speciation
by Ed Yong in Animal behaviour, Animals, Bacteria, Evolution, Insects, Invertebrates, Microbiome, Predators and prey, Speciation | 12 comments | RSS feed | Trackback >

12 Responses to “Gut bacteria change the sexual preferences of fruit flies”

  1. 1.   Walter S. Andriuzzi Says:
    November 1st, 2010 at 5:17 pm

    Another great omg! (and slightly wtf?!) article :)
    The good thing is that we have even more evidence for evolution. The bad– no, actually even better thing is that we have even more evidence that evolution is more complicated than was previously thought. But no matter how many new, unexpected evolutionary factors we find, the core of the darwinian (sensu lato) theory not only does not falter, indeed grows even stronger – you gotta love this theory!

  2. 2.   Mike Lisieski Says:
    November 1st, 2010 at 5:27 pm

    My quick armchair theory is that flies use their own smell as a basis for comparison when identifying another animal as a conspecific. Therefore, flies that smell different smell more like another species, and so the fly is less likely to treat them as a possible mate.

    But, I don’t know anything about fruit flies. Neat post!

  3. 3.   "Shecky R." Says:
    November 1st, 2010 at 5:53 pm

    the complexity, intricacy, wonder of biology never ends (even at the level of fruit flies)… fascinating stuff! (I predict more awards coming your way in 2011 :-) )

  4. 4.   JanedeLartigue Says:
    November 1st, 2010 at 6:39 pm

    Really fantastic study, as always written up beautifully by you.
    @Mike I was actually going to ask in my comment why they might be driven to mate with flies that smell the same. Great explanation!

  5. 5.   chezjake Says:
    November 1st, 2010 at 11:08 pm

    “Gut bacteria change the sexual preferences of fruit flies”, but it appears that science writer changes sex/gender of researcher. ;)

    Correct me if I’m wrong, Ed, but in paragraph 4 I see, “After just two generations, she found the same effect that Dodd did: the flies were more attracted to individuals reared on the same diets.” And in paragraph 5 there is, “This idea was dramatically confirmed when he gave the insects a dose of antibiotics.” In both sentences the antecedent of the personal pronoun seems to be researcher Sharon.

    It’s still a fascinating piece of research that is, as usual, well reported.

  6. 6.   Quinn O'Neill Says:
    November 1st, 2010 at 11:41 pm

    Maybe the way to a man’s heart really is through his stomach …

  7. 7.   Shade Says:
    November 2nd, 2010 at 4:27 am

    A question for every one:
    Am I misunderstanding evolutionary theory?
    You see I personally understand evolution says that small mutations cause the changes we see over time, but i don’t think that that works, due to the fact that biological systems try to stamp out mutations. Incest would make the most evolutonaryly advanced humans otherwise no?

    Sorry for this not relating directly to the post, but walter’s comment made me remember this question I had. Nobody thus far has been able to properly elucidate this for me :/

  8. 8.   Lab Rat Says:
    November 2nd, 2010 at 6:40 am

    Wow, fascinating. Loved this post, and so did my undergrad student :p My vote for the reason for the preferences would be smell as well, different bacteria will have very distinct ones, in particular thinking of poo-smell here.

    Shade: I’m kinda wary of going into this but basically some mutations are harmful, and some can be useful. Most organisms try to err on the side of having few mutations as possible, but some will occur despite various mechanisms being in place to stop them. And some of those will have useful effects and thus be retained within the organism.

    The reason incest is a bad idea is not because it increases mutations but because every human has two copies of each gene. In some cases negative mutations will happen on one gene copy but not the other. If you procreate with a relative it increases the changes that your child will get two copies of the negative mutation and thus will be a lot less healthy.

    Also sometimes in evolution you can get big mutations, like whole chunks of genome being moved, duplicated, or deleated. These often lead to severe negative outcomes, but can also lead to positive ones, such as creating two copies of a protein, which can then specialise in different tasks.

    [Ed - feel free to delete that if it's derailing the conversation]

  9. 9.   lucas Says:
    November 2nd, 2010 at 11:42 am

    Wow, I had never expected besides temporal, sexual, and spatial differences, now culinary habits can drive species apart! Biology’s beautiful.
    While I agree with Sharon’s comment that we should consider the hologenome to understand an organism’s evolution, I think we should take it one step further and consider all these other factors that exert pressures (ecosystems, behaviour etc.). It’s holobiology, so to speak.

  10. 10.   Ed Yong Says:
    November 2nd, 2010 at 7:14 pm

    Re: incest. I wrote about a paper a while back suggesting that third-cousin couples have more children/grandchildren than couples who were more/less related. Will repost it at some point.

  11. 11.   Shade Says:
    November 3rd, 2010 at 4:06 am

    Thanks for tha answers, incest was just an example of something that has a very high rate of mutation is all.
    could have been toxic waste for all it matters.

    p.s. as lab rat said, sorry for derailing.

  12. 12.   Jenny Morber Says:
    November 4th, 2010 at 10:17 pm

    I thought that you might pick this one up. Pretty cool, eh? Makes one wonder how much the microbiome influences human mate choices. I can see headlines in 5 years: “Women who want to attract doctors from Sweden should eat sushi” etc.

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