Convergent evolution between shrunken animals and bloated protists

Our invertebrate zoology textbook, being a good couple decades behind schedule as any textbook ought to, felt rather heavily biased against molecular phylogenetic analysis, and rather conservative in sticking to traditional taxonomy in spite of contradicting molecular data. In fact, towards the end somewhere the authors rather explicitly pointed out that molecular phylogenies are not to be trusted, especially when in disagreement with embryological data.

Here we run into the age-old problem in evolutionary biology: how do you reconstruct the past is the models of evolution you use are based on your...reconstructions of the past? Hah, as with any other interesting problem in life, you have to do both simultaneously, devoid of simple algorithms. Dismissing molecular phylogenies because they disagree with your pet theories on morphological evolution is just stupid. The non-photosynthetic stramenopiles(=heterokonts), for example, include things that were once, based on morphology, considered as: yeast, filamentous fungi, 'heliozoa' (group now completely defunct) and ciliates. Molecular phylogenies, while definitely full of their own flaws, eventually resolved that mess.

Curiously, it seems there may be a bit of a problem with bacterial phylogenies being overrated in spite of the organisms and their biology. So while traditional taxonomy fails there as well, it's as if the field got a little carried away with sequences. Part of the reason may be that there seems to be very little communication between cell and evolutionary bacteriologists, emphasised by the stark absense of organism in evolutionary discussions and evolution in organismal ones. Which is another thing that makes protistology a pretty awesome field - there appears to be at least some semblance of balance and sanity between organismal and evolutionary protistologists, perhaps because there's so few of them to begin with.

Anyway, back to our invert zool text, one major drawback of clumping things together by morphology is that smaller things tend to go together that way. Obviously, sharing size does not imply any phylogenetic closeness; nor does the level of structural complexity. Plagued by past notions of a progression towards increased complexity, many taxonomists lumped the 'simpler' incertae sedis taxa together.

One such example was the acoelomate/pseudocoelomate/coelomate concept, where the inner body cavity (coelom) became progressively more complex as proto-bilaterians evolved into acoelomate flatworms, then pseudocoelomate nematode-like intermediates and finally acheived the true coelom of arthropods and vertebrates. From the morphological perspective, that makes sense. However, along came molecular data and cast this neat little story into the rubbish pile, revealing that many of the acoelomates and pseudocoelomates have secondarily reduced coeloms, derived from a true coelom. Thus, Acoelomata and Pseudocoelomata kind of exploded all over the tree. Much like 'yeasts' and 'heliozoans' and 'rhizopods' (amoebae, forams, etc).

Structural complexity is very dangerous, as evolution wanders about rather aimlessly and has little against losing complexity if it can. In fact, selective pressures tend to favour simplicity, and to put it crudely, reduction of complexity tends to be adaptive more often than bloating. I've rambled on about this before, but this is to emphasise that this concept is actually kind of important and useful, and not just idle philosophising. It is actually dangerous to assume some sort of adaptive search for complexity as shown in cases like those of Acoelomata and Archaezoa.

This leads us to the next taxonomic 'clump' - small metazoans, or 'meiofauna'. Meiofauna include Loriciferans, Rotifers, Gastrotrichs and the rather adorable Tardigrades. Many of them weren't clumped together seriously as much as simply due to lack of any information about them, considering they sadly don't fare well in the charismatic megafauna beauty contest. Turns out that meiofauna tend to be secondarily miniaturised. There is only so many ways an organism can be shrunk and still viable, thus convergence becomes a rampant feature in miniaturisation, the central theme of Rundell & Leander 2010 BioEssays:

Latest sketch of the metazoan phylogeny with representative meiofauna depicted in the images, where applicable. Very nice of them to put metazoa into the broader eukaryotic perspective in the top left corner! As meiofauna are quite widespread over the metazoan phyla, it is emphasised that a better understanding of these groups is crucial to properly reconstruct metazoan evolution and diversity. Microorganisms being important...another issue in need of reminders every five years or so? (Rundell & Leander 2010 BioEssays)

Rundell & Leander focus on interstitial organisms (those of the intertidal zone) and note the prevalence and importance of convergent evolution between various independently reduced animals, such as adult loriciferans and larval priapulids; and adult vs. larval ostracods and barnacles, respectively:

a) adult loriciferan b) larval priapulid c) adult ostracod d) barnacle larva (Cypris stage) Scalebars: a - 30um; b-d - 100um. (Rundell & Leander 2010 BioEssays)

Of course the comparisons at this stage are superficial, but still a good lesson in the prominence of convergent evolution and the dangers of morphological lumping. Furthermore, they proceed to point out convergent features shared with some protistan representatives from the same environment: ciliates. Meiofaunal taxonomy is plagued by cases of well-trained zoologists failing to distinguish ciliates from rotifers and cryptic small metazoa (there was one cryptic species mentioned in the textbook that was obviously a ciliate based on the description, especially the 'dispersal by transverse fragmentation' part... can't find it at the moment, perhaps someone might know what I'm talking about? Name starts with a C or an S...), and there may be good reasons for that:

a) A gastrotrich b) A [hypotrich] ciliate. Note the dorsal spines and dense ventral cilia on both. Incidentally, both are benthic, so this is rather unsurprising, but still cool considering the former is a case of size reduction whereas the latter is a case of a size increase. c-d) stalked rotiferConochilus e) stalked ciliate Epistylis. They are both capable of rapid contractions in a very similar manner. Again, only so many ways one can be a stalked colonial organism of this size and ecological niche. Scalebars - 10um. (Rundell & Leander 2010 BioEssays)

As shown above, the examples of convergence are quite striking, and also not too surprising - there are only so many ways one can survive under given conditions, especially when the conditions are extreme as in the intertidal case (or in case of parasitism as well). Extreme conditions generally imply stronger selective pressures which lead to greater streamlining and a reduced 'design space', to steal a term Dennett often uses in Darwin's Dangerous Idea (1995). What is quite intriguing is that parts of this design space are accessible to both unicellular and multicellular organisms, leading to striking convergence as in the stalked rotifer and ciliate examples above. While the 'function' (I use this word with fear...) is similar, the mechanisms underlying it are as different as can get, striking down the phylogenetically-limited argument that all convergent features are ultimately homologous in some way (see Leander 2008 JEM and an informative reply in 2008 TrEE here(both free access)).

Of course, the crux of all this is that microscopic organisms of all phylogenetic affiliations are infinitely awesome and desperately in need of research attention. If you insist on multicellularity, then metazoan 'meiofauna' are for you. If we can still find amitochondriate anaerobic animals in 2010, there must be plenty of other amazing stuff hidden within neglected, obscure and underexplored phyla.

And with that, I shall migrate back towards my protists - feels like I'm cheating on them. My past two 'meatier' posts have been about...metazoa. That's just...wrong =P

Gonna stop there as someone holds freakishly early lab meetings (9.30am! the cruelty...!) so someone else must be up early... yes, before noon is early, ok?

[completely off topic: someone besides TC-S agrees people have become a little too obsessed with the role of endosymbiosis in eukaryogenesis - essay by Poole & Penny 2007 Nature]

Reference:
Rundell, R., & Leander, B. (2010). Masters of miniaturization: Convergent evolution among interstitial eukaryotes BioEssays, 32 (5), 430-437 DOI: 10.1002/bies.200900116