Incurring the Cost

There’s another paper that supports my front-loading hypothesis that envisions introns as part of the mechanism to facilitate the emergence of metazoan-like complexity.  The paper is: Extremely intron-rich genes in the alveolate ancestors inferred with a flexible maximum-likelihood approach, by Csurös M, Rogozin IB, and Koonin EV (Mol Biol Evol. 2008 May;25(5):903-11).

Let’s walk through the abstract.

Chromalveolates are a large, diverse supergroup of unicellular eukaryotes that includes Apicomplexa, dinoflagellates, ciliates (three lineages that form the alveolate branch), heterokonts, haptophytes, and cryptomonads (three lineages comprising the chromist branch). All sequenced genomes of chromalveolates have relatively low intron density in protein-coding genes, and few intron positions are shared between chromalveolate lineages.

Let’s pull out our eukaryotic tree of life to translate this:

The sequenced genomes of the organisms in the lower left pink box have don’t have many introns and when you compare the introns that exist among them, few share the same positions.  This would seem to indicate that introns arose independently, after the various lineages split apart.  But…

In contrast, genes of different chromalveolates share many intron positions with orthologous genes from other eukaryotic supergroups, in particular, the intron-rich orthologs from animals and plants.

When we compare the introns from organisms in the lower left pink panel with introns from organisms in the lower right purple panel and upper left green panel, many of the positions are shared.  This would suggest the ancestors of all the organisms in the pink, green, and purple boxes contained these introns.

Reconstruction of the history of intron gain and loss during the evolution of chromalveolates using a general and flexible maximum-likelihood approach indicates that genes of the ancestors of chromalveolates and, particularly, alveolates had unexpectedly high intron densities. It is estimated that the chromalveolate ancestor had, approximately, two-third of the human intron density, whereas the intron density in the genes of the alveolate ancestor is estimated to be slightly greater than the human intron density.

So as we go deep back into eukaryotic history, into the central zone with the five branches, we find an ancestral unicellular state loaded with introns.  Why is this significant?

Accordingly, it is inferred that the evolution of chromalveolates was dominated by intron loss. (emphasis added)

Which means…

The conclusion that ancestral chromalveolate forms had high intron densities is unexpected because all extant unicellular eukaryotes have relatively few introns and are thought to be unable to maintain numerous introns due to intense purifying selection in their, typically, large populations. (emphasis added)

Recall that one clue supporting my hypothesis was “as a general rule, introns are far more common in multicellular genomes than single-celled genomes.”  This is pattern that suggests introns would have greater utility in a multicellular context than a unicellular context.  And sure enough, this view is supported by the evolution of chromalveolates being dominated by intron loss, while the evolution of metaozoans was not dominated by intron loss.  Use it or lose it.

Now think like a bunny and view eukaryotic evolution from the perspective of a designed process.  The first unicellular eukaryotes are loaded with introns, but again and again and again, various protozoan lineages that emerge from this state shed their introns.  Yet when it comes to the origin of animals and plants, they emerge from an ancestral state that is high in intron density and introns are “locked in” during the subsequent evolution of plants and animals.

If introns are playing important roles in multicellular development and physiology (as seems likely from alternative splicing alone), then we have a distinct echo of foresight.  For this would constitute the classic pattern of incurring a cost in the present for the sake of future profit. Introns in early eukaryotes were costly, as can be seen by their repeated loss across many protozoan lineages.  Yet this cost is more than compensated for when the multicellular state emerged, where introns could finally play a role in the evolvability of organisms.

What’s more, this teleological hypothesis has the added benefit of raising more questions to guide further inquiry.  In addition to the obvious search for intron utility in multicellular states, we should wonder how it was some unicellular lineages were able to retain their introns when other lineages were shedding them.  Is there is some form of biotic process that pushes back against the environmental forces favoring intron loss in the unicellular state, such that a designer could count on some fraction of protists retaining introns long enough for metaozoan-like life to appear?

Here, we can begin to compare the biology of Monosiga and Chlamydomonas.  As you can see from the tree above, they are very distantly related (Monosiga are the choanoflagellates and Chlamydomonas are the green algae).  Yet they share two common themes:

1. They are exceptions in that they are unicellular organisms with genomes that have many introns and

2. Monosiga are closely related to animals, while Chlamydomonas are closely related to plants.

So we would predict other similarities between these two unicellular life forms that are not universal among the protists.  For starters, is it mere coincidence that these two lineages also have the tyrosine kinase circuitry?


6 responses to “Incurring the Cost

  1. still moderated?

  2. Thinking and digging like a bunny.

  3. pretty awesome

  4. No Alan, moderation is not on.

  5. I got that from the test post, thanks. My previous last comment flagged up as awaiting moderation, but must have been a glitch. Feel free to delete this and other comment on moderation.

  6. Pingback: More Incurred Cost «

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