Eukaryotes: more than just animals

Aug 16 2010 Published by under [Biology&Environment]

If there is one thing that bothers the ever-loving-shit out of YHN, it is when people make broad claims about "the evolution of eukaryotes", when they really mean "the evolution of animals", one of the least interesting branches of the Tree of Life from an evolutionary standpoint. Every time I hear someone say "And we looked at this phenomenon across all eukaryotes, from humans all the way to flies!" I want to stand up in their presentation and whip my fucking laptop at them. Maybe when I need to upgrade...

In presentations it just show the stupidity of the lab and the animocentrism that most people use to view the world. In print, however, it had to get through reviewers and the editor. So, when I got the feed from the most recent issue of Trends in Ecology and Evolution and clicked on the link for the paper by Schaack et al., I expected some interesting stuff. The title of the paper is, afterall, "Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution".  Sounds pretty cool, right? I like interesting eukaryote-wide phenomena that may have an impact of evolution of organisms. Isn't that what everyone reads to their kids at night?

But by the time I got through the first section, I knew this horse had blinders on and has galloping full speed to metazoatown. Ironically, the second paper they cite is a solid review by Keeling & Palmer on eukaryotic gene transfer which brings up several cases of movement of transposable elements among non-animal organisms (in fact they dedicate Box 4 to this very issue), but Sclaack et al only use this reference to state that gene transfer between eukeryotes "has remained more obscure" than that between prokaryotes. Um, true, but there is a shit-ton of data on the topic, much of it covered well in the Keeling and Palmer paper. It is usually a good idea to read more than the abstract when citing a paper.

In fact we know a LOT about the transfer of both genes and, to a lesser extent, non-coding DNA between eukaryotes. It happens often and if you search for the terms HGT or LGT and eukaryotes you get over 450 hits. Considering our understanding of this phenomenon has really emerged only as genome sequencing has expanded relatively recently, that's a decent number of papers.

But wait, PLS, you might say. The paper is about transposable elements, not all gene transfer! True, but not only has there been a significant amount of non-animal work done in this realm as well, the sheer number of genomes that have been sequenced from non-animal organisms in the last 5 years has yielded more than enough data to examine this question across eukaryotes.  And no, throwing in one or two references from the land plant lit does not get one of the hook.

So why does such a small portion of an entire group continually serve in the eyes of many as a proxy for the whole? It is, IMO, just pure blind ignorance and unwillingness to think beyond the obvious. If I wrote an article claiming to have discovered a critical force for the evolution of vegetables and then only discussed a couple of examples from squash, do you think that would get reviewed well? How fast would I get reviews back blasting me for over-stating my evidence? Would it even get past the editor's desk?

If you haven't opened a biology textbook since the 1970's, consider this a head's up that the whole 3 kingdom 'animals, plants, fungi' (in that order of importance) classification is long dead and things are much more complicated these days. In fact, we know a tremendous amount about the world around us and how insignificant a contribution animals make to the diversity of organisms on the planet. Perhaps it is time to stop learning about biodiversity from the Discovery Channel and introduce yourself to the other 95% of eukaryotes.

References:

Schaack, S., Gilbert, C., & Feschotte, C. (2010) Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol. Evol. (25) 537-546.

Keeling, P., Palmer, J. (2008) Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. (9) 605-618.

19 responses so far

  • Dan Gaston says:

    Great post. I experience this frustration continuously myself. I work in a lab whose main focus is on deep eukaryotic evolution, eukaryotic phylogenetics, and the evolution of Mitochondrion-Like Organelles. Most people have no idea how tiny the groups they think are important (metazoa, plants, fungi) actually are in terms of eukaryotic diversity.

  • Isabel says:

    "and the evolution of Mitochondrion-Like Organelles. " Which are these? I am very curious. Can you point me to some literature?

    Great post PLS. Thank you! Animals generally have uncharacteristically simple sex lives and life cycles as well. Boring!

    It's egocentric, and maybe because so much funding is ultimately expected to benefit human health (NIH funding is 10x NSF).

  • proflikesubstance says:

    Isabel, I believe that Dan is referring to mitosomes and other relic mitochondria. Check a 2006 Nature review by Embley and Martin (doi:10.1038/nature04546) for more on the topic.

  • Patchi says:

    I cringed when I walk into Natural History museums in NYC and saw the evolutionary trees they have posted!

    My graduate background was in plants and a lot of reviews come back saying "this has already been shown in plants". For a postdoc I spent some time in a mammalian cell culture lab and was amazed that people have no problem publishing data from different cell lines, even if they are "this also works in these cells". Animocentric bias is very unfortunate.

  • Casey says:

    Got any nice reviews on protist evolution? Last I heard, there were something like 8 general groups of eukaryotes, with protozoans, animals, and fungi all in one group, and algae and plants in another. The other 6 are really weird stuff most people never think about. I'd be curious to know what the thinking is these days.

  • Isabel says:

    Thanks for the reference.

    "I cringed when I walk into Natural History museums in NYC and saw the evolutionary trees they have posted! "

    Can you be more specific Patchi? I was there last year and many of the evolutionary diagrams were recently updated, I must have missed what you experienced - hope they didn't screw up.

  • gnuma says:

    Jeez, they should have just said 'higher eukaryotes'! jk

    Did you know there are no TEs in bdelloid rotifers? One of the few genomes analyzed that lack them.

  • proflikesubstance says:

    Got any nice reviews on protist evolution?

    There have been a few changes since this, but it isn't a bad place for an update.

    The other 6 are really weird stuff most people never think about.

    Ouch, dude.

  • Isabel says:

    "The other 6 are really weird stuff most people never think about.

    Ouch, dude."

    Well the brown kelps aren't THAT weird, and 'people' do think about them from time to time!

  • Dan Gaston says:

    Isabel:

    Yes Mitosomes and Hydrogenosomes being the two most common MLOs other than Mitochondria and Anaerobic Mitochondria. There are also a host of organelles that fill in the spectrum. The MLO of Blastocystis seems to fall somewhere between an Anaerobic Mitochondria and a Hydrogenosome for instance.

  • Nothing ticks of botanists more than the human-biomedical tail wagging the biological dog. A truly unbiased exo-biologists describing Earth's biota for the Galactic Guide to Life would say simply "mostly unicellular".

  • Patchi says:

    Isabel, I was there a year and a half ago, so maybe they did update the stuff between our visits. What bothers me is the variety and detail given to the animal kingdom in comparison to the abbreviated counterparts in the other kingdoms. As my background is in plants I always notice the difference in emphasis and detail between animals and plants.

  • proflikesubstance says:

    Patchi X 3.4 bazilion for anything not animal plant or fungus

  • As a fly person, I am constantly frustrated by the importance placed on vertebrates. The amount of stuff we have learned from C. Elegans is amazing. Yet the C.Elegans are rarely cited, which is sad. Nevermind the importance prokaryotes have been in helping us understand Eurkaryotes.

  • Cedric Feschotte says:

    As the corresponding author on the TREE paper you are referring to, I am feeling obligated to rectify several inaccuracies in your post.

    First, I have to say I am quite offended, not to say shocked, by your post. Because my group is actually one of the very few, along with my wife's Ellen Pritham, to work on transposable elements in several 'protist' genomes, including apicomplexans, trichomonads, Entamoeba rhizarians...etc. We are collaborating with a number of eminent protist biologists and hence we are well aware that the diversity of eukaryotes is far from limited to metazoans.

    Unlike most others in the TE field, we always try to be very careful in our wording to avoid generalizing some of our findings in metazoans to other eukaryotic groups. Granted, it is not often easy to do, it is a fine line between oversimplification and overspecialization - especially in journals that have tight constraints in title, abstract, references and overall text length. For simplicity and brevity, we have to use general terms such as 'eukaryotes' in titles and abstract, to make it clear that prokaryotes will not be covered and also, in this particular piece, to emphasize the differences with what is known on HT of mobile elements in prokaryotes. I guess we could have used 'multicellular eukaryotes', although I suspect the editor would have demanded to delete 'multicellular'!!

    Secondly, and perhaps more importantly, before accusing us to cite papers (Keeling and Palmer) after only reading their abstract, you should be reading more carefully the ones you are writing about in your blog. In the Introduction of our paper, which you are paraphrasing partially and inaccurately in your post, we were careful to say that we are placing emphasis in this review on transfer of genetic material between the NUCLEUS of MULTICELLULAR eukaryotes. Indeed we state in the very first sentence of the paper:

    "Horizontal transfer has long been recognized as a crucial
    mechanism driving bacterial evolution [1]. In contrast, the
    evolutionary significance of horizontal transfer between
    the nuclear genomes of multicellular eukaryotes has
    remained more obscure [2]."

    We are perfectly aware of the growing number of HGT events reported in unicellular eukaryotes, a topic well covered in the Keeling and Palmer review. But note that almost all of these are transfers from bacteria or plastids to nucleus. There are still very few clear instances of HGT reported between the nuclear genomes of eukaryotes, even for unicellular organisms (but see the remarkable case of bdelloid rotifers). As for plants, until last month or so, there had been not a single report of nucleus-to-nucleus HGT between plants. All the cases of HGT reported by Palmer and others involved organelle genes.

    In terms of TEs, the focus of our review, we still no very little on unicellular eukaryotes (aside from a handful of yeasts). Most of the protist genomes sequenced so far are from species with very small genomes (e.g. apicomplexans) which seem to harbor very few, if any TEs.

    Out of the >200 solid cases of HT of TEs reported to date, to the best of our knowledge, none involve a unicellular or protist species. It means we know virtually nothing about the phenomenon of HTT in these organisms. So I don't see what else we could have possibly said about these organisms in our review. Clearly a lot of work remains to be done in this area. As I mentioned above, we are actively working on characterizing TEs in several, deeply diverged protist lineages.

    In several places in our paper, we warn against the temptation to generalize the patterns inferred in this review based on a very limited sample of (mostly multicellular) eukaryotic species. For example, page 540, we wrote:

    " Currently, the taxonomic sampling bias of whole-genome sequencing projects
    among eukaryotes leans strongly towards animals
    and fungi, making it difficult to infer patterns among
    under-represented groups, for example unicellular eukaryotes
    and plants. Thus, it is important to be cautious when
    making generalizations about patterns of HTT based on
    1.5 million extant eukaryotes become
    available."

    I think we couldn't be more explicit and more cautious. Don't you think?

    For all these reasons, I found your post completely unfair and misleading. I am very sensitive to the issue of ignorance of the general public and lack of attention given to the wonderful diversity of unicellular eukaryotes, and I found myself regularly advocating and educating my students and colleagues about it.

    In my opinion, it was poor judgment from your part to use our paper to illustrate a real and serious issue. It is not serving the cause eloquently. I hope you'll realize this when you read it again, this time more carefully. And I hope people reading your blog will do the same.

  • palmd says:

    In my opinion, it was poor judgment from your part to use our paper to illustrate a real and serious issue.

    No, it's friggin awesome! And it's even more awesome that you responded, bringing this issue to other people who are interested, rather than keeping it locked up in some academic dungeon where alterkakers can sit around and have a big circle jerk.

  • proflikesubstance says:

    Cedric, I am away at the moment and don't have the ability to write a full response, which I will do next week. Nevertheless, hold the shock and horror. Despite the few sentences here and there where caveats are scattered, it is hard to reconcile the title and abstract with the subject of the paper, which is entirely focused on animals. Yes, there is a fine line when writing for such a journal, but substituting animals for eukaryotes is not a subtle distinction.

    Thanks for coming by to add your thoughts, however. It's always appreciated when authors take the time to engage in discussion about their work.

    More when I get back.

  • [...] Eukaryotes: more than just animals [...]

  • proflikesubstance says:

    I've added my response to Cedrichere.

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