Complex early genes.

We use the pattern of intron conservation in 684 groups of orthologs from seven fully sequenced eukaryotic genomes to provide maximum likelihood estimates of the number of introns present in the same orthologs in various eukaryotic ancestors. We find: (i) intron density in the plant-animal ancestor was high, perhaps two-thirds that of humans and three times that of Drosophila; and (ii) intron density in the ancestral bilateran was also high, equaling that of humans and four times that of Drosophila. We further find that modern introns are generally very old, with two-thirds of modern bilateran introns dating to the ancestral bilateran and two-fifths of modern plant, animal, and fungus introns dating to the plant-animal ancestor. Intron losses outnumber gains over a large range of eukaryotic lineages. These results show that early eukaryotic gene structures were very complex, and that simplification, not embellishment, has dominated subsequent evolution.

[1]  T. Cavalier-smith Principles of Protein and Lipid Targeting in Secondary Symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan Plastid Origins and the Eukaryote Family Tree 1 , 2 , 1999, The Journal of eukaryotic microbiology.

[2]  Alexei Fedorov,et al.  Large-scale comparison of intron positions among animal, plant, and fungal genes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Eugene V Koonin,et al.  Preferential loss and gain of introns in 3' portions of genes suggests a reverse-transcription mechanism of intron insertion. , 2004, Gene.

[4]  Eugene V Koonin,et al.  Prevalence of intron gain over intron loss in the evolution of paralogous gene families. , 2004, Nucleic acids research.

[5]  Jian Wang,et al.  The Genome Sequence of the Malaria Mosquito Anopheles gambiae , 2002, Science.

[6]  Russell F. Doolittle,et al.  Intron Distribution in Ancient Paralogs Supports Random Insertion and Not Random Loss , 1997, Journal of Molecular Evolution.

[7]  Eugene V Koonin,et al.  A Non-Adaptationist Perspective on Evolution of Genomic Complexity or the Continued Dethroning of Man , 2004, Cell cycle.

[8]  W. Gilbert,et al.  The exon theory of genes. , 1987, Cold Spring Harbor symposia on quantitative biology.

[9]  R. Raff,et al.  Evidence for a clade of nematodes, arthropods and other moulting animals , 1997, Nature.

[10]  R. Ellis,et al.  A phylogeny of caenorhabditis reveals frequent loss of introns during nematode evolution. , 2004, Genome research.

[11]  A. Newman,et al.  Evidence that introns arose at proto‐splice sites. , 1989, The EMBO journal.

[12]  R. Gwilliam,et al.  Sequence of Plasmodium falciparum chromosomes 1, 3–9 and 13 , 2002, Nature.

[13]  A. Newman,et al.  Exon Junction Sequences as Cryptic Splice Sites Implications for Intron Origin , 2004, Current Biology.

[14]  Igor B. Rogozin,et al.  Evidence of Splice Signal Migration from Exon to Intron during Intron Evolution , 2003, Current Biology.

[15]  G. Elgar,et al.  Quality not quantity: the pufferfish genome. , 1996, Human molecular genetics.

[16]  L. Patthy,et al.  Evidence that human genes of modular proteins have retained significantly more ancestral introns than their fly or worm orthologues , 2004, FEBS letters.

[17]  S. J. Souza The Emergence of a Synthetic Theory of Intron Evolution , 2003, Genetica.

[18]  Andrew J. Roger,et al.  U2 and U6 snRNA genes in the microsporidian Nosema locustae: evidence for a functional spliceosome , 1998, Nucleic Acids Res..

[19]  W. Doolittle,et al.  Trichomonas vaginalis possesses a gene encoding the essential spliceosomal component, PRP8. , 1999, Molecular and biochemical parasitology.

[20]  Walter Gilbert,et al.  The triosephosphate isomerase gene from maize introns antedate the plant-animal divergence , 1986, Cell.

[21]  Michael Lynch,et al.  The evolution of spliceosomal introns. , 2002, Current opinion in genetics & development.

[22]  J. Logsdon,et al.  The recent origins of spliceosomal introns revisited. , 1998, Current opinion in genetics & development.

[23]  J D Palmer,et al.  Seven newly discovered intron positions in the triose-phosphate isomerase gene: evidence for the introns-late theory. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Peer Bork,et al.  Comparative Genome and Proteome Analysis of Anopheles gambiae and Drosophila melanogaster , 2002, Science.

[25]  W. Doolittle,et al.  A kingdom-level phylogeny of eukaryotes based on combined protein data. , 2000, Science.

[26]  T. Cavalier-smith,et al.  Intron phylogeny: a new hypothesis. , 1991, Trends in genetics : TIG.

[27]  H. Robertson,et al.  The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving large duplications and deletions and intron gains and losses. , 2000, Genome research.

[28]  W. Gilbert,et al.  Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. Roy Recent evidence for the Exon Theory of Genes , 2003 .

[30]  Tobias Mourier,et al.  Eukaryotic Intron Loss , 2003, Science.

[31]  A. Stoltzfus Molecular Evolution: Introns Fall into Place , 2004, Current Biology.

[32]  M. Lynch,et al.  Messenger RNA surveillance and the evolutionary proliferation of introns. , 2003, Molecular biology and evolution.

[33]  S. Carroll,et al.  Early animal evolution: emerging views from comparative biology and geology. , 1999, Science.

[34]  Albert D. G. de Roos,et al.  Origins of introns based on the definition of exon modules and their conserved interfaces , 2005, Bioinform..

[35]  Arlin Stoltzfus,et al.  The evolutionary gain of spliceosomal introns: sequence and phase preferences. , 2004, Molecular biology and evolution.

[36]  E. Koonin,et al.  Coelomata and not Ecdysozoa: evidence from genome-wide phylogenetic analysis. , 2003, Genome research.

[37]  M. Lynch Intron evolution as a population-genetic process , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[38]  M. Lynch,et al.  The Origins of Genome Complexity , 2003, Science.

[39]  L. Patthy Genome evolution and the evolution of exon-shuffling--a review. , 1999, Gene.

[40]  J. Logsdon Worm genomes hold the smoking guns of intron gain. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  H. Robertson Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. , 1998, Genome research.

[42]  John M. Logsdon,et al.  The recent origins of introns. , 1991 .

[43]  Fabio Piano,et al.  Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  E. Koonin,et al.  Remarkable Interkingdom Conservation of Intron Positions and Massive, Lineage-Specific Intron Loss and Gain in Eukaryotic Evolution , 2003, Current Biology.

[45]  D. Petrov,et al.  Genome size and intron size in Drosophila. , 1998, Molecular biology and evolution.

[46]  Andrew G McArthur,et al.  A spliceosomal intron in Giardia lamblia , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[47]  W. Gilbert Why genes in pieces? , 1978, Nature.

[48]  W. J. Kent,et al.  Conservation, regulation, synteny, and introns in a large-scale C. briggsae-C. elegans genomic alignment. , 2000, Genome research.

[49]  Cristian I. Castillo-Davis,et al.  Accelerated rates of intron gain/loss and protein evolution in duplicate genes in human and mouse malaria parasites. , 2004, Molecular biology and evolution.