The Loom

i-ff7d3f2b6ca35be045e5b9db44885586-eggfly.jpgLike many parasites, a species of bacteria called Wolbachia takes charge of its own fate. Wolbachia can only survive inside the cells of its hosts–invertebrates such as this lovely common eggfly. This way of life limits Wolbachia’s opportunities for long-term survival. If Wolbachia lives inside a female insect, it can infect her eggs. When those eggs hatch and mature into adult insects, they will be infected by Wolbachia as well. But if Wolbachia should find itself in a male, it has reached a dead end. It cannot infect sperm cells, and thus it has no escape from a male host. When a male host dies, Wolbachia dies as well.

Wolbachia’s solution: kill the males before they kill you.

In many species, Wolbachia is lethal to male embryos. As a result, Wolbachia-carrying females only give birth to Wolbachia-infected females. Male killing boosts Wolbachia’s population in two ways. With fewer Wolbachia-free males around, the proportion of eggflies carrying the bacteria goes up. And without males to compete for food, Wolbachia-infected females may be able to increase their odds of surviving until they can reproduce–and produce more Wolbachia.

Male-killing is not the only weapon Wolbachia uses on its hosts. When some strains infect wasps, they alter the females so that their eggs start spontaneously turning into embryos without any need of sperm. All of these sperm-free embryos become females, which can also produce female offspring without the help of males. In other species, Wolbachia allow males to be born but alters their hormones to feminize them and make them produce eggs. And in other cases, Wolbachia decides which males and females may mate with one another. If a healthy female mates with a male carrying Wolbachia, some or all of her fertilized eggs will die. But a female carrying Wolbachia can mate with either infected or uninfected males and produce viable eggs–all of which have Wolbachia in them.

With all these different ways of manipulating their hosts, Wolbachia has become perhaps the most successful species of infectious bacteria on the planet, infecting millions of species of invertebrates.

Scientists have long wondered if the hosts of Wolbachia have any way of defending themselves against the assaults of the bacteria. In a Wolbachia-infected population, a few males get to mate with a lot of females. Any mutation that can allow eggflies to have sons despite the presence of male-killing should be strongly favored by natural selection. While this explanation makes sense on paper, scientists have until now found little evidence of the suppression of male-killing.

There are two possible explanations for this state of affairs. One is that for some reason the suppression of male killers evolves only rarely. The other is that it actually evolves very quickly. It spreads so quickly through populations that there is little outward sign that the hosts have silenced a male-killer.

Today in the journal PLOS Biology, scientists report that the latter is true: male-killer defenses evolve very fast. Over the past few years the scientists have studied eggflies from Southeast Asia and the Pacific. They’ve found that on some Polynesian Islands, male-killing Wolbachia is a common pathogen. But in other parts of its range, the eggfly is infected by the same strain of Wolbachia, but it produces a normal fifty-fifty split of males and females.

To compare these populations, the scientists bred eggflies from the island of Moorea, where Wolbachia is a male-killer, with eggflies from Thailand and the Philippines, where it is not. They found that female Moorea eggflies produced a normal fraction of males if they could mate with male eggflies from Thailand and the Philippines. But if the hybrid females then mated with eggflies from Moorea, they produced fewer and fewer males over the generations. Experiments such as these demonstrated that eggflies from Thailand and the Philippines have a hereditary ability to stop Wolbachia from killing their sons. They may use only one gene to shut the parasite down.

The authors conclude from their experiments that Wolbachia jumped into the eggflies some time in the past and began killing males as it spread through much of the eggfly’s range. The eggflies then evolved a defense against the bacteria. Females that could produce more males were favored by natural selection, until the ratio of the sexes evened out again at fifty-fifty. They continued to carry the bacteria, but Wolbachia was rendered impotent. The dramatic changes the scientists saw in their breeding experiments, suggest that the gene for suppressing male-killing could have spread very quickly through an eggfly population–perhaps in less than 100 generations (about 25 years). Historical records agree. Scientists in the 1960s found all-female populations of eggflies in Borneo, but they’re gone now, 160 generations later.

The scientists predict that as eggflies flit about the Pacific, females carrying the suppressor gene will outcompete the females vulnerable to male-killing. Soon male-killing will become a thing of the past–at least until some strain of Wolbachia hits on a new way to take control of its eggfly hosts. If the scientists are right, then the history of Wolbachia is even more turbulent than once thought. It is infecting a vast number of invertebrates despite their rapid evolution of defenses against them. As it is muzzled in one population, it finds new ways to manipulate another.

Wolbachia is not alone in distorting the ratio of the sexes. An organism’s own genes may sometimes tip the balance. Sex-distorting genes sit on the chromosomes that determine an animal or plant’s sex. In humans, two X chromosomes produce a female, and an X and a Y produce a male. If a gene on an X chromosome can raise the odds that its chromosome will be passed down to an offspring, that gene will become more common. And it will increase the number of females in a population.

Sometimes called meiotic drive, this evolutionary force is often countered by another: genes that suppress the tilt towards one sex over the other. Plenty of examples of meiotic drive have been documented in flies and other species. A few clues have emerged from studies on humans, but just a few. If the new study on Wolbachia is right, I wonder if some scientists will look more closely at our own selfish genes. There might be some hidden tugs-of-war waiting for someone to discover.

Update 822 1:20 pm: Josh at Thoughts from Kansas knows about the strange ways of Wolbachia first hand.

Comments

  1. #1 oldhippie
    August 21, 2006

    “Male-killing is not the only weapon Wolbachia uses on its hosts. When some strains infect wasps, they alter the females so that their eggs start spontaneously turning into embryos without any need of sperm. All of these sperm-free embryos become females, which can also produce female offspring without the help of males.”
    Could that not eventually end in a stable situation with the complete elimination of the males? There would presumably be a loss of genetic diversity which would be disadvantgeous in the long term.

  2. #2 e
    August 21, 2006

    Hey oldhippie,

    I’m guessing that the “sperm-free embryos” that become females are clones of the mother. The loss of genetic diversity is catastrophic: any pathogen that would harm the mother would harm the daughters in the same way. It is a good hedge-bet by the Wolbachia, however, as it causes the bacteria to survive for another generation of hosts, as it waits for males to show up and contribute new genes.

    Of course, I am just guessing. =)

  3. #3 sharon
    August 22, 2006

    Wolbachia’s solution: kill the males before they kill you.

    nice post.
    so much for some who mistakingly believe in the “creator God” who has it in for females and personal preference for patriarchal systems over matriarchal.
    good post.

    …always interesting to find species, where the female plays a dominate role as with female worker bees who toss out the drones and keep the stores all for themselves..

    caste of the Honeybees
    Worker bees, which are half the size and weight of the Drones, pick up the larger Drones, carry them to the entrance and toss them to the ground. …

    though in Carl’s example it’s a lose-lose situation for either sex.

    The Brains of Female Hyena Twins
    It appears that in many species of fishes if you remove the dominant male from a social group, the largest female then becomes male. …

    Seems a lot of species naturally change sex, and that some scientists tend to gloss over homosexual behavior in the wild.

    And, Black Widow has got a really bad rap…

    Myth: When black widow spiders mate, the female always kills and eats the male.
    Fact: This myth (which is not totally false, but very far from true) is believed even by scientists, and can be found in many ecology textbooks! It’s depressing; the authors are obviously copying each other and have never actually watched black widows mate in the field. [...] there are many different species worldwide in the black-widow group (the genus Latrodectus) [...] in the past most observations of mating took place in laboratory cages, where males could not escape. [...] Of U.S. species, mate cannibalism occurs sometimes in Latrodectus mactans, the eastern black widow, but most males survive to mate another day. In the other two black species, including the western black widow L. hesperus (only species west of Kansas), mate cannibalism has never been observed in the wild!
    Source: Black Widow Myth

    And, a lot more could be said on these issues. . .

  4. #4 Peter Ellis
    August 22, 2006

    There’s some fairly solid hints that there’s a buried X-Y conflict in the mouse genome – sex ratio skews associated with Y chromosome partial deletion, along with an upregulation of X-linked genes in testes of the Y-deleted mice. It’s not strictly meiotic drive, since it appears to affect the fertilisation efficiency of sperm rather than actual chromosome segregation. There’s also a suggestion that this is the reason sex chromosomes get silenced during (and after) meiosis – to prevent them getting hijacked by sex ratio distorters.

    Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS. Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids.

    Toure A, Clemente EJ, Ellis P, Mahadevaiah SK, Ojarikre OA, Ball PA, Reynard L, Loveland KL, Burgoyne PS, Affara NA. Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol. 2005;6(12):R102. Epub 2005 Dec 2.

    Ward MA, Burgoyne PS. The effects of deletions of the mouse Y chromosome long arm on sperm function–intracytoplasmic sperm injection (ICSI)-based analysis. Biol Reprod. 2006 Apr;74(4):652-8. Epub 2005 Dec 14.

    Ellis PJ, Clemente EJ, Ball P, Toure A, Ferguson L, Turner JM, Loveland KL, Affara NA, Burgoyne PS. Deletions on mouse Yq lead to upregulation of multiple X- and Y-linked transcripts in spermatids. Hum Mol Genet. 2005 Sep 15;14(18):2705-15. Epub 2005 Aug 8.

  5. #5 david maas
    August 22, 2006

    Is there a possibility that this reproduction-jacking could give rise to a= new species combining parasite and host? Sounds like a step away, at least in my sci-fi infected brain…

  6. #6 oldhippie
    August 22, 2006

    “The loss of genetic diversity is catastrophic: any pathogen that would harm the mother would harm the daughters in the same way.”
    Yes, but that is long term, I am not sure how, other than genetically, Wolbachia gets passed along, but it presumably infects enough hosts to have considerable genetic diversity at least at the outset. If the pathogen then turns females into clone producers that do not go near males, and presuming their offspring are not more unsuccessful than uninfected females, and if Wolbachia also have another mode of infection so that they continue colonization, I could see a possibilty males could be eliminated, and the new female/bacteria clone models could be around for a very long time. The day of the body snatchers did come to mind. As David Maas said rather sci-fi. But then what is wierder than something getting into a rat, manipulating its brain and driving up to a cat?

  7. #7 RPM
    August 22, 2006

    “Is there a possibility that this reproduction-jacking could give rise to a= new species combining parasite and host?”

    Wolbachia mediated speciation has been proposed, but I’m not sure if there is much evidence to support this hypothesis. I follow the wolbachia literature enough to have heard of it, but not enough to know whether anyone has conclusive evidence of it occurring in the wild.

    “I’m guessing that the “sperm-free embryos” that become females are clones of the mother.”

    Are they clones or are the they product of selfing? Both processes will decrease the genetic variation in the population, but they are different. Aren’t sperm-free diploid progeny due to the fusion of a polar body with the oocyte?

  8. #8 Garrett
    August 22, 2006

    We’d better not let women read this post or they might get some ideas from it :P

  9. #9 speedwell
    August 22, 2006

    Bite your tongue, Garrett. It’s a lady’s prerogative to enjoy the attentions of gentlemen. Some women exercise the right not to exercise the prerogative, but don’t paint us all with the same brush! :)

  10. #10 sharon
    August 22, 2006

    Garrett: better not let women read this post or they might get some ideas

    ohhhh, you mean what the male has been doing over the past eon?

  11. #11 Garrett
    August 23, 2006

    I know. I was just being facetious, raise a little ire and all that. Nothing serious meant to be implied.

    Sharon: I was thinking along that lines that the ideas might be revenge for what your link says. Really, society would probably be better off without men doing their testosterone induced thing. My train of thought was that if women see that it was possible to get rid of us and still survive as a species then they might want to implement that.

    Yeah, I get myself in trouble sometimes. It’s standard stand up comedy routine fare, though.

  12. #12 sharon
    August 23, 2006

    Garrett: My train of thought was that if women see that it was possible to get rid of us and still survive as a species then they might want to implement that.

    Well, honestly I had thought about it…

    A REVIEW of all the world’s cloned animals suggests that every one of them is genetically and physically defective. The study coincides with claims by researchers trying to create the first cloned human. In Italy, Dr Severino Antinori has claimed that three women are pregnant with cloned babies; in America, Dr Panayiotis Zavos has said he will achieve such a pregnancy within two years. Wilmut said his latest research suggested that a cloned human would also be at huge risk of genetic defects. This was a clear warning that “nobody should be attempting to clone a child”.
    She [Dolly] was born with chromosomes that have shortened telomeres the DNA tips that protect the end of chromosomes.

    decades of extensive laboratory experimentation and millions on research, turns out you men are useful for something afterall.

    What will science discover next?

  13. #13 Miguel
    August 24, 2006

    What a sick twisted critter. Amazing. Darwin whould have loved it.

  14. #14 Lynn
    April 14, 2007

    “Wolbachia has become perhaps the most successful species of infectious bacteria on the planet, infecting millions of species of invertebrates.”

    Has Wolbachia been documented to infect “millions” of invertebrates?