How important is lateral gene transfer?

Recent molecular work has revealed a spate of cases in which genes move between unrelated (often very unrelated) species.  One of the most striking examples, which I wrote about last May, was an aphid’s capture of genes from a fungus, a capture that led to an adaptive polymorphism in the aphid’s body color.

The growing list of such cases has led to realization that adaptive genetic variation needn’t just arise via mutation.  This doesn’t really overturn modern evolutionary theory, since lateral gene transfer (“LGT;” also called “horizontal” gene transfer) simply introduces into a species new genetic variation from a different species; that genetic variation still must be subject to the well known processes of natural selection and genetic drift.  But many critics of evolution do cite LGT as invalidating one of the tenets of modern evolutionary theory: the “tree of life.”  If genes can move widely between species, and do so frequently, you don’t get a tree of life so much as a network of life.

How often does LGT occur?  I’d recommend reading the nice five-page primer on horizontal gene transfer by Olga Zhaxybayeva  and W. Ford Doolittle in the latest issue of Current Biology (access is free; download pdf at link). It’s a pretty even-handed summary of the state of the art.  The authors discuss the history of work on the problem and how one detects LGT, how it occurs, and how important it’s been in evolution.  They give some cute examples, too, and highlight the many unknowns, like how LGT occurs in multicellular organisms.

Another mystery is how “adaptive” LGT is.  There are many cases, of course, in which genes captured by LGT have formed the basis of new adaptations (the colors of aphids described above is one example, antibiotic resistance in bacteria another).  But is the mechanism of LGT adaptive—that is, have organisms evolved mechanisms specifically for capturing genes from other species?  After reading the piece, I’d say the answer is is “it’s possible” for prokaryotes (bacteria), and “probably not” for eukaryotes.  Instances of adaptive LGT in the latter are rare (though of course more will be found), which makes it unlikely that we’d evolve mechanisms to capture genes from other species, especially when most such capture would be maladaptive.  Further, the fact that sperm and eggs are sequestered from the rest of the body in multicellular eukaryotes suggests that those species are largely impervious to infection by foreign genes.  Indeed that may be one reason why sperm and eggs are set off from the rest of the body.

You can also look as LGT as “adaptive” in another sense:  it’s adaptive for the genes themselves to spread between species.  Genes that did so would be represented in more groups, and so we’d expect some “selfish” transfer, even if it wasn’t adaptive but purely “neutral” in the recipient species.

Does LGT invalidate the tree of life?  Since the phenomenon is far more common in bacteria than in eukaryotes, we face more serious problems in reconstructing evolutionary “histories” in the former groups.  LGT makes the evolutionary history of species diverge somewhat from the evolutionary histories of their genes.

In eukaryotes, though, it’s unlikely that LGT is common enough to pose problems for making phylogenies.  In Drosophila, the group I work on, gene-based phylogenies are largely concurrent when one uses different genes, suggesting virtually no lateral transfer of genes from unrelated species.  And those gene histories are concordant with independent histories derived from chromosome banding patterns, so to a large extent gene histories do represent species histories. (There are of course exceptions based on long-standing polymorphisms:  some blood-group genes in humans, for instance, are more closely related to similar blood-group genes in chimps than to other blood-group genes in humans.)

The authors seem to agree that LGT isn’t much of a problem for eukaryotic “trees,” but can be so for prokaryotes. But they add this:

Keeling and Palmer (2008) suggest that, in spite of the growing list of eukaryotic LGT examples, “there is no reason to think that [LGT] is so prevalent as to undermine efforts to reconstruct a dichotomously branching tree of eukaryote phylogeny, much less call for the replacement of the tree metaphor with a ‘web of life’ metaphor, as some have controversially suggested for prokaryotes”. Indeed, but if, as most would agree, Life’s history is predominantly prokaryotic, what then of the combined ‘universal’ tree?

They also emphasize that LGT doesn’t overturn modern evolutionary theory by constituting some sort of brand-new evolutionary process:

LGT can introduce radically new phenotypes that mutation and selection might never achieve. Quantitative estimates of its frequency, even if accurate, may underestimate its importance in adaptation and speciation. Opponents of evolution have cheered its challenge to the ‘Tree of Life’, as if the literal truth of that simile (as Darwin called it) were essential for the modern theory of evolution. We, however, take this theory to be simply that understandable ecological and genetic processes, operating over evolutionary time, are adequate to explain existing biological adaptation and diversity. In fact, the ability of LGT to speed complex and radical adaptation makes it even easier to imagine how “from so simple a beginning, endless forms most beautiful and most wonderful have been, and are being, evolved”.

38 Comments

  1. Sajanas
    Posted April 13, 2011 at 7:10 am | Permalink

    I’m glad you posted about this, I’m still trying to think of ways that Eukaryotes with separated sex cells could pick up genes that weren’t carried by a virus (though I suppose it is also possible that a virus carried those genes). Even viral transmission seems slightly problematic… it would have to get into germline cells, or hit a fetus at a very young age.

  2. Ken Pidcock
    Posted April 13, 2011 at 7:13 am | Permalink

    That was an excellent summary of a topic that is typically either ignored or overhyped.

    I hate to be a pest, but could people pause before using the word prokaryote?

    • mswzebo
      Posted April 13, 2011 at 1:58 pm | Permalink

      and replace it with ‘microorganism’? But that doesn’t exclude euk’s. ‘Bacteria’ doesn’t include Archaea…but I guess that’s really the fundamental point, right? We shouldn’t be lumping Bacteria and Archaea together anyway…the fact that microbiologists study the two is kind of like the old tradition of having mycologists in botany departments…hence we don’t need a new term to replace the misguided old term, we need to simply stop using the unjustifiable term in the first place.

      • Michael Syvanen
        Posted April 13, 2011 at 3:18 pm | Permalink

        Prokaryote is a perfectly respectable term. It distinguishes, well prokaryotes from eukaryotes. And what are eukaryotes. Well they are chimeras of Archaea, of alpha-proteobacter, of gram positive bacteria, of cyanobacteria plus a collection of 500 or so genes that have no identifiable relationship to any other prokaryote, either archaea or bacteria.

        See horizontal gene transfer is so pervasive in the evolution of the eukaryotic cell, that it becomes almost absurd to try to insist on a taxonomy that assumes pure tree like patterns of descent. That is why the word prokaryote continues to have scientific value.

        The problem that is being revealed in this debate happens to be an insistence of the modern rules of taxonomy to force categories to obey pure tree like patterns of descent. Horizontal gene transfer is the new fact of life that makes those rules obsolete.

    • Sven DiMilo
      Posted April 13, 2011 at 2:56 pm | Permalink

      bah.
      ‘Prokaryotes’ is a para- (possibly poly-) -phyletic group, but so what? So is ‘algae’, ‘monkeys’, ‘crustaceans’, etc. Keep formal taxonomy monophyletic, but don’t expect vernacular English to follow suit.
      ‘Prokaryotes’ is a perfectly cromulent word for organisms that share a certain basic cell-type.

      • Ken Pidcock
        Posted April 13, 2011 at 4:43 pm | Permalink

        The point is that the word has no phylogenetic meaning, and that our use of it implies that it does, that cellular life is somehow divided between prokaryotes and eukaryotes and, worse, that eukaryotes are descended from prokaryotes. All of this, as you know, is wrong. Quoting Norman Pace,

        Because it has long been used by all texts of biology, it is hard to stop using the word, prokaryote. But the next time you
        are inclined to do so, think what you teach your students: a wrong idea.

        And if Pace doesn’t convince you, perhaps it would help to remind you that defending prokaryote as a biologically meaningful term allies you with Lynn Margulis. (And New Scientist?) 🙂

        • Posted April 13, 2011 at 7:14 pm | Permalink

          Ken–is that paper you linked above available anywhere else (not behind a pay wall)? Or–just, you guys keep talking! This is just *fascinating*!

          • Ken Pidcock
            Posted April 14, 2011 at 6:49 am | Permalink

            I’ve been unable to find it outside of Nature. Which is stupid, stupid, stupid. A one page essay from 2006 ought to be available to the public.

            Pace does have a slide show on his own page that includes the argument.

  3. Posted April 13, 2011 at 7:23 am | Permalink

    I always saw the “tree” of life to be more like a snowflake of life, where time passes as you move outward from the core.

    Whether it’s a tree, a snowflake, or a sausage is really quite irrelevant is it not?

  4. Posted April 13, 2011 at 7:59 am | Permalink

    The last paragraph, yeah.

    It’s messed up that evolution is the only theory where every proclamation of “Well, it turns out it’s even weirder than we thought” results in a chorus of “See? The theory is wrong and everybody who believes in it is smelly!” Imagine if, every time some new principle in quantum mechanics were verified, there was a New Scientist headline “Einstein was wrong!”

    Cool stuff, though.

    • Buzz
      Posted April 13, 2011 at 8:41 am | Permalink

      I’m afraid that does happen in physics too. “Einstein was wrong!” headlines are common enough, actually (but not over articles related to quantum mechanics, since everybody already knows he was wrong about that). When it comes to quantum mechanics, there is no real disagreement about what the end result of any given experiment should be, but people scream and shout all the time about how a particular way of interpreting the math upends all sorts of basic principles.

      • Torbjörn Larsson, OM
        Posted April 13, 2011 at 8:47 am | Permalink

        Yeah, but that is the point isn’t it? It is the basic principles that get blasted, not the theory (math) that leads to said blast.

        Creationists need to have the cake and eat it too. And it _is_ messed up that they can get to bloviate in such a manner.

    • Ken Pidcock
      Posted April 13, 2011 at 9:13 am | Permalink

      Imagine if, every time some new principle in quantum mechanics were verified, there was a New Scientist headline “Einstein was wrong!”

      Yeah, then imagine if a group of self-righteous blokes warned NS that it was giving aid and comfort to the enemy. That’d be funny, no? (Sorry, just my personal opinion.)

      • Kevin
        Posted April 13, 2011 at 12:57 pm | Permalink

        Your analogy fails, because there are no priests, ministers, imams or other religious authority figures claiming that because Einstein was wrong, therefore god is responsible for the position and velocity of the electron.

        The aid and comfort given was to those who would deny settled science in favor of superstitious nonsense. Claiming Einstein’s wrongness only pits one scientist against another.

        Sorry, just my personal opinion, but you’re way off base.

        • Ken Pidcock
          Posted April 13, 2011 at 7:02 pm | Permalink

          Look, the trolls are already wide awake and vigorously searching for bits of information with which to deceive the public. When, in 2004, Carl Woese proposed that there may not be one universal common progenitor, Stephen Meyer couldn’t contain his joy, as if a serious contribution to our understanding of biogenesis was proof that it didn’t happen. That’s just the way these folks interface with science; I’ve no doubt that people who think the moon is made of green cheese are avid students of lunar geology. But the DI fellows’ interest in finding things to distort shouldn’t mean that scientists and science journalists have to filter everything they say or write to ensure that it cannot possibly be distorted. Constantly asking ourselves What Would Jerry Do? is no way to enjoy biology nor to convey that joy to our students and the public. I say of the ID crowd, let them enforce their orthodoxy. We have none to enforce.

  5. Matt G
    Posted April 13, 2011 at 8:08 am | Permalink

    How about when populations separate, evolve, and then hybridize before the speciation event is complete? Would this be considered horizontal gene transfer? This is thought to have happened between us and H. neandertalensis.

    • Torbjörn Larsson, OM
      Posted April 13, 2011 at 8:51 am | Permalink

      You have to ask the participants. I tend to think, re Auel, that the missionary position wasn’t the preferred one in such events.

      [Especially since there _were_ no missionaries. Really, who comes up with these ideas anyway!?]

      • Diane G.
        Posted April 13, 2011 at 2:36 pm | Permalink

        In doggy style, the important parts of the participants could still be considered horizontal.

        😀

  6. Torbjörn Larsson, OM
    Posted April 13, 2011 at 8:44 am | Permalink

    Thanks for the alert! I am trying to understand the case study of Earth life as applied to astrobiology, and the pattern of evolution is a vital part of that even if you are no biologist.

    It is heartening to see Doolittle et al acknowledge that there are two equally predictive theories here. Constructing trees with state changes from both kind of transfers. (Say, by minimizing or, better, maximizing, gene sets used.) Or constructing nets with state changes from both kind of transfers. (Say, by maximizing or, better, minimizing, state changes used.)

    In the best of worlds they should converge on more or less the same outcome, branching topology being the arbiter. That is, locally a binary branching tree is the simplest model, but it isn’t likely to fit all cases depending on resolution. And in parts the global tree will look like a net.

    But arguing for the later is still the case of trying to use, or worse insert, complexity where there is no obvious need. It is obvious too in the otherwise very well done part where the paper notes the often arguable issue of time frame. After promoting this issue they turn around and imply that the known existence of a LUCA means vertical branching order is not a valid simplest default!

    If the case really comes down to “will there be any Nobel prizes awarded for horizontal transfer”, I guess the case is no outside of mechanisms. (Or has it already happened?) But that is the analysis of an outsider, biologists could be privy to better information.

    Then you can retire the question all the way down to the pro- to protobiotic transition and the pathway to a LUCA or the domain splits if outside of Bacteria. Which, if you are adamant about dominant horizontal transfer I understand is then not a done deal; the rooting evidence used instead of outliers is still assuming vertical descent I believe.

    I am not sure “a gene meld” is a necessary mechanism for the transition to a stable hereditary system. I just read about the wondrous increasing and decreasing genome of the classic Amoeba. Besides it large size the author hypothesized that gene scuffling in incessant multiplication and random purge of genes could make up for absence of sexuality.

    Applying that to Shostak’s protocells (to ease modeling) one can hypothesize that this, if true, could replace the equally unsupported hypothesis of rampant horizontal transfer.

    Now I’m not sure if these protocells wouldn’t spontaneously merge, with content, now and then instead of competing for membrane components. But I think the later is the observed mode of putative evolution. The amount of “phylogenetic signal” vs time frame as Doolittle put it could be testable (in the model system)!

    • Torbjörn Larsson, OM
      Posted April 13, 2011 at 9:15 am | Permalink

      [It is OT, but as I touched on rooting of LUCA and is curious: does anyone know _why_ we shouldn’t use an outlaying root such as it is even in this case? As an example we could use a weathering rock, or better some form of hydrothermal vent chemistry.

      Then stuff like minimal amount of genes, or presumed early natural availability of molecules and chemical pathways, would be naturally promoted in the phylogenetic analysis (genes and/or traits). It wouldn’t be a hereditary analysis as such, more like an external constraint, but anyway.

      I don’t know if it is enough, and todays preferred method may be better, but I can’t help wonder if it couldn’t contribute some information. Has anyone tried it?]

  7. Insightful Ape
    Posted April 13, 2011 at 8:58 am | Permalink

    I think this should be of particular interest to Michael Behe, who “discovered” that bacteria isolated from all kinds of gene transfer (including through phages) would not have many beneficial mutations…

  8. AT
    Posted April 13, 2011 at 10:00 am | Permalink

    Thanks to Jerry for keeping readership informed of all important developments in the field

    i think anyone who values understanding of reality would appreciate these pointers

    i enjoyed reading the article a lot

    and I commend Jerry’s picl of quotes – it conveys most important ideas of the authors in their own words – this is science journalism at its best!

    thank you again!

  9. Posted April 13, 2011 at 10:12 am | Permalink

    The article concludes:

    We, however, take this theory to be simply that understandable ecological and genetic processes, operating over evolutionary time, are adequate to explain existing biological adaptation and diversity.

    I think the “Central” idea here is “understandable”. It seems that “Understandable” as oppose to “Divine Magic” is key to finding any sort of consistency in the evolving “theory of evolution”.

    Heck what if something outside of “genetic” gets into the picture. The point is, we still expect it to be “understandable”. But no metaphor “tree” or “gene” or others should be held as sacred or central as we struggle and constantly readjust our lastest approximation of reality.

    Thanx, fantastic post and article.
    Is LTG a term from American football or European rugby? 🙂

  10. Chris
    Posted April 13, 2011 at 10:47 am | Permalink

    HGT is just another molecular mechanism for developing a genome. There is an industry that sells plasmid vectors for biotech. Swapping plasmids is the microbial answer to sex.

    Swapping genes does not necessarily imply anything about an organism’s survivability. That is still governed by natural selection.

    One would think that if there is a particularly useful plasmid in a bacterial population (for say, antibiotic resistance), that plasmid would survive, duplicate, and be much more likely to be passed around.

  11. Curtis
    Posted April 13, 2011 at 11:19 am | Permalink

    This seems to support Lynn Margulis’s ideas on speciation. I bring this up because Coyne recently said Margulis “has been off the deep end for a while. She wrote a book on speciation that maintained, contrary to all evidence, that it was completely due to endosymbiosis.”

    http://scienceblogs.com/aetiology/2011/04/margulis_does_it_again.php#comments
    (Comment 8)

    Am I missing something? Or is Coyne just saying Margulis has taken a reasonable idea and taken it past its reasonable limits?

    • Chris
      Posted April 13, 2011 at 11:35 am | Permalink

      What I understand from others in the field is that she has done some good work in the past. She did early work on symbiosis and now “systems biology” is one of the major grant friendly buzzwords.

      Lately, she’s been going way over the top.

    • Insightful Ape
      Posted April 13, 2011 at 12:31 pm | Permalink

      And this bakcs Margulis’ view-how? Did you miss the part that said it is negligible in eukaryokes?

    • Ken Pidcock
      Posted April 13, 2011 at 4:49 pm | Permalink

      Am I missing something? Or is Coyne just saying Margulis has taken a reasonable idea and taken it past its reasonable limits?

      If that’s your understanding, you’re not missing anything.

  12. Thanny
    Posted April 13, 2011 at 11:31 am | Permalink

    The tree is entirely intact, all the way down, provided you look at the issue correctly.

    In the primary sense, the branches aren’t organisms, but genes. They spend a lot of their time bundled together with other genes in an organismal gene pool, and occasionally (more frequently in prokaryotes) shoot over to join another gene pool.

    With whole organisms, the tree is still really intact, though our ability to discern the branch points is compromised. There’s still a real chain of cell division leading back from current progeny to distant ancestor, but, as Jerry puts it, the mutations along the way can come from gene imports as well as various types of replication errors.

    Deficits in our practical ability to acquire knowledge of facts do not impinge on saids facts existence.

  13. Jim Thomerson
    Posted April 13, 2011 at 11:39 am | Permalink

    The first comment reflects a moderately common confusion of terms. Eukaryote is not a synonym of animal. Eukaryote includes all organisms which have membrane enclosed nuclei. Not the least of these are the higher plants. Flowering plants do not have early segregation of germ cells, in contrast to most familiar animals. Flower buds arise more or less de novo, and new germ cells are formed. So somatic mutations, including viral gene transfer, can end up in germ cells. This is what you are seeing if a stem of a plant has different appearing flowers, which produce germ cells with the different appearing genes. (No, it wasn’t grafted!) This is one of the horticultural sources for new varieties of flowering plants. (I’m neglecting other plants, because I don’t remember exactly what they do.)

    • Diane G.
      Posted April 13, 2011 at 3:05 pm | Permalink

      Thank you. Always glad to get the botanical POV.

    • Posted April 13, 2011 at 7:11 pm | Permalink

      Really! That might explain an eggplant I had with the usual purple flowers on all branches, and a single branch with thorns(!) and white flowers….hmmm…. (With Diane–thanks for the botanical POV:-))

  14. Sigmund
    Posted April 13, 2011 at 12:06 pm | Permalink

    If you allow retroviral derived sequences to be included in the definition of ‘lateral gene transfer’ then you see a very different picture. In fact our genome and the genomes of other animals contain far more ‘lateral’ derived sequence than coding sequence.

    • Michael Syvanen
      Posted April 13, 2011 at 3:29 pm | Permalink

      Sigmund, that is a very good point. Retroviral and other transposable elements definitely are included in the examples of HGT.

      And these are not just junk DNAs either. All placental mammals share a specific ERV (endogenous retrovirus)that seems to play a role in preventing maternal immune rejection of embryos.

  15. sponge bob
    Posted April 13, 2011 at 1:58 pm | Permalink

    Would be interesting if LGT was a factor in mimicry. Seems to me that some mimicry is so good that mutation with selection doesn’t seem like enough to me to do the job without a little “informational” help from the environment. But I’m no expert of course.

  16. miko
    Posted April 13, 2011 at 4:26 pm | Permalink

    I’ve seen lots of trees that have branches that go around something and then refuse. Very common in many parts of the world. Only a colonial, Eurocentric concept of “tree” suggests that HGT violates the tree-ness of evolution. So there.

    • Diane G.
      Posted April 13, 2011 at 4:30 pm | Permalink

      Perhaps we should consider the “strangler fig” of evolution…

      😀

  17. VP SEGERS
    Posted February 19, 2014 at 2:38 pm | Permalink

    Don’t forget that your mitochondrial DNA can be infected by bacteriophages, and that DNA can make its way from your mitochondria into your nuclear DNA. In this way genes can move nearly directly from prokaryotes into eukaryotes.


5 Trackbacks/Pingbacks

  1. […] How important is lateral gene transfer? « Why Evolution Is True One of the most striking examples which I wrote about last May, was an aphid's capture of genes from a fungus, a capture that led to an adaptive polymorphism in the aphid's body color. new genetic variation from a different species; that genetic variation still must be subject to the well known processes of natural selection and genetic drift. But many critics of evolution do cite LGT as invalidating one of the tenets of modern evolutionary theory: the “tree of life. […]

  2. […] How important is lateral gene transfer? Posted on April 13, 2011 by marksolock How important is lateral gene transfer? […]

  3. […] Here is a post about an evolutionary mechanism called Lateral Gene Transfer; this mechanism involves one species taking genes directly from another. This doesn’t […]

  4. […] How important is lateral gene transfer? Teaching a seminar-based course on it this semester. Fascinating. […]

  5. […] https://whyevolutionistrue.wordpress.com/2011/04/13/how-important-is-lateral-gene-transfer/ […]

%d bloggers like this: