A recent paper adds more support to this hypothesis:
Origin and evolution of spliceosomal introns.
Rogozin IB, Carmel L, Csuros M, Koonin EV.
Biol Direct. 2012 Apr 16;7(1):11.
Let’s go through the abstract.
Evolution of exon-intron structure of eukaryotic genes has been a matter of long-standing, intensive debate. The introns-early concept, later rebranded ‘introns first’ held that protein-coding genes were interrupted by numerous introns even at the earliest stages of life’s evolution and that introns played a major role in the origin of proteins by facilitating recombination of sequences coding for small protein/peptide modules. The introns-late concept held that introns emerged only in eukaryotes and new introns have been accumulating continuously throughout eukaryotic evolution. Analysis of orthologous genes from completely sequenced eukaryotic genomes revealed numerous shared intron positions in orthologous genes from animals and plants and even between animals, plants and protists, suggesting that many ancestral introns have persisted since the last eukaryotic common ancestor (LECA). Reconstructions of intron gain and loss using the growing collection of genomes of diverse eukaryotes and increasingly advanced probabilistic models convincingly show that the LECA and the ancestors of each eukaryotic supergroup had intron-rich genes, with intron densities comparable to those in the most intron-rich modern genomes such as those of vertebrates.
This is not news here. In fact, we have seen that LECA was remarkably modern-like in terms of its complexity. But given that LECA “had intron-rich genes, with intron densities comparable to those in the most intron-rich modern genomes such as those of vertebrates,” it is not unreasonable to propose that these organisms were poised to evolve into a metazoan state. In other words, the basic type of genomic architecture that was needed to evolve vertebrates came into existence with the emergence of the eukarytotic cell itself.
The subsequent evolution in most lineages of eukaryotes involved primarily loss of introns, with only a few episodes of substantial intron gain that might have accompanied major evolutionary innovations such as the origin of metazoa.
This further supports my hypothesis, as we can see that introns were superfluous to unicellular life. It was the metazoan lineage that found them necessary and expanded upon them.
The original invasion of self-splicing Group II introns, presumably originating from the mitochondrial endosymbiont, into the genome of the emerging eukaryote might have been a key factor of eukaryogenesis that in particular triggered the origin of endomembranes and the nucleus.
So once again, the various complex features that we associate with the eukaryotic cell and genome a) came into existence in parallel such that LECA would possess them all and b) most likely originate from a symbiotic union that was front-loaded to occur. That’s the hypothesis.
Conversely, splicing errors gave rise to alternative splicing, a major contribution to the biological complexity of multicellular eukaryotes.
As I have argued.
There is no indication that any prokaryote has ever possessed a spliceosome or introns in protein-coding genes, other than relatively rare mobile self-splicing introns.
This is because introns, a forward-looking feature, came into existence as a consequence of a front-loaded symbiotic union. The design potential of self-splicing Group II introns needed more than the right abiotic environment to be tapped. It needed the correct biotic context. Once again, the cell’s design helps to guide evolution.
So in conclusion:
Thus, the introns-first scenario is not supported by any evidence but exon-intron structure of protein-coding genes appears to have evolved concomitantly with the eukaryotic cell, and introns were a major factor of evolution throughout the history of eukaryotes.
Which is one reason why there are no prokaryotic mice. Evolution is not simply about the right mutation in the right environment. Without the eukaryotic cell plan, there is no right mutation or right environment that can unlock the emergence of metazoan-type complexity. Evolution is rightly seen as a biological process.