Deepening the Clues

I have already provided a couple of clues that suggest introns played some important role in the emergence of multicellular life.  Let me now add a little depth to those clues.

We saw that the general rule was that complex multicellular genomes tend to be intron-rich, while the genomes of single-celled organisms tend to have very few introns.

But there is a glaring exception.  Recall the choanoflagellates – the single-celled organisms thought to be most closely related to metazoans.  When their genome was sequenced, it provided a big boost to the hypothesis of front-loading, as it contained a whole toolkit of genes needed for metazoan existence, including the information to make cell adhesion domains, extracellular-matrix-associated protein domains, and an elaborate phosphotyrosine signalling machinery (all of these once believed to be specific to metazoans).

So do the choanoflagellates have introns?

Oh yeah.

Choanoflagellates are the closest known relatives of metazoans. To discover potential molecular mechanisms underlying the evolution of metazoan multicellularity, we sequenced and analysed the genome of the unicellular choanoflagellate Monosiga brevicollis. The genome contains approximately 9,200 intron-rich genes, including a number that encode cell adhesion and signalling protein domains that are otherwise restricted to metazoans.

[….]

Whereas the M. brevicollis genome is compact, its genes are almost as intron-rich as human genes (6.6 introns perM. Brevicollis gene versus 7.7 introns per human gene). M. brevicollis introns are short (averaging 174 bp) relative to metazoan introns, and with few exceptions do not include the extremely long introns found in some metazoan genes.

From Nicole King et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature Vol 45

So while introns are usually sparse in protozoan genomes, in the case of this protozoan genome, they exist at a density that is analogous to the human genome.  So it is reasonable to propose that an intron-rich genome did precede the appearance of metazoan.  Such a genome might have constituted a preadaptation that would facilitate the emergence of metazoans.

In fact, feast your eyes on the abstract from Sullivan, J. C., Reitzel, A. M. & Finnerty, J. R. 2006. A high percentage of introns in human genes were present early in animal evolution: evidence from the basal metazoan Nematostella vectensis. Genome Inform. 17, 219–229.

Intronic sequences represent a large fraction of most eukaryotic genomes, and they are known to play a critical role in genome evolution. Based on the conserved location of introns, conserved sequence within introns, and direct experimental evidence, it is becoming increasingly clear that introns perform important functions such as modulating gene expression. Here, we demonstrate that the positions of 69% (862/1246) of human introns in 343 orthologous genes are conserved in the starlet sea anemone Nematostella vectensis, a phylogenetically basal animal (phylum Cnidaria; class Anthozoa). This degree of intron concordance greatly exceeds that between humans and three more closely related animals: fruitfly (14%), mosquito (13%) and nematode worm (19%). Surprisingly, the fruitfly and mosquito, two members of the order Diptera, share only 43% of intron locations, fewer than the percentage of cumulative introns shared between human and sea anemone (47%), despite sharing a much more recent common ancestor. Our analysis indicates (1) that early animal genomes were intron-rich, (2) that a large fraction of introns present within the human genome likely originated early in evolution, before the cnidarian-bilaterian split, at least 600 million years ago, and (3) that there has been a high degree of intron loss during the evolution of the protostome lineage leading to the fruitfly, mosquito, and nematode. These data also reinforce the conclusion that there are functional constraints on the placement of introns in eukaryotic genes. (emphasis added)

Having laid out the clues to support my hypothesis that introns facilitated the evolution of metazoan life, we should start speculating how introns facilitated the evolution of metazoan life.  But before going there, we need to unpack this hypothesis a bit.

In essence, there are two possible ways to interpret this hypothesis.

1. Introns facilitated the emergence of metazoan life.

2. Introns facilitated the evolutionary spread of metazoan life forms.

The first version would have us focus on how introns helped evolution transition from a single-celled existence to a multicellular existence. The second version would have us focus on how introns helped multicellular organisms expand into their various phyla.

Both possibilities are in play, although the second version entails a front-loading event that attempts to reach much further into the future.