Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 21 November 2003:
Vol. 302. no. 5649, pp. 1401 - 1404
DOI: 10.1126/science.1089370

Reports

The Origins of Genome Complexity

Michael Lynch1* and John S. Conery2

Complete genomic sequences from diverse phylogenetic lineages reveal notable increases in genome complexity from prokaryotes to multicellular eukaryotes. The changes include gradual increases in gene number, resulting from the retention of duplicate genes, and more abrupt increases in the abundance of spliceosomal introns and mobile genetic elements. We argue that many of these modifications emerged passively in response to the long-term population-size reductions that accompanied increases in organism size. According to this model, much of the restructuring of eukaryotic genomes was initiated by nonadaptive processes, and this in turn provided novel substrates for the secondary evolution of phenotypic complexity by natural selection. The enormous long-term effective population sizes of prokaryotes may impose a substantial barrier to the evolution of complex genomes and morphologies.

1 Department of Biology, Indiana University, Bloomington, IN 47405, USA.
2 Department of Computer and Information Science, University of Oregon, Eugene, OR 97403, USA.

* To whom correspondence should be addressed. E-mail: mlynch{at}bio.indiana.edu

Read the Full Text



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Distinguishing Among Evolutionary Models for the Maintenance of Gene Duplicates.
M. W. Hahn (2009)
J. Hered.
   Abstract »    Full Text »    PDF »
Deletional Bias across the Three Domains of Life.
C.-H. Kuo and H. Ochman (2009)
Gen Biol Evol 2009, 145-152
   Abstract »    Full Text »    PDF »
The genome sizes of megabats (Chiroptera: Pteropodidae) are remarkably constrained.
J. D.L. Smith and T. R. Gregory (2009)
Biol Lett 5, 347-351
   Abstract »    Full Text »    PDF »
Effective population size and the rate and pattern of nucleotide substitutions.
M. Woolfit (2009)
Biol Lett 5, 417-420
   Abstract »    Full Text »    PDF »
Selection for Chaperone-Like Mediated Genetic Robustness at Low Mutation Rate: Impact of Drift, Epistasis and Complexity.
P.-A. Gros and O. Tenaillon (2009)
Genetics 182, 555-564
   Abstract »    Full Text »    PDF »
Deletion Rate Evolution and Its Effect on Genome Size and Coding Density.
M. E. Pettersson, C. G. Kurland, and O. G. Berg (2009)
Mol. Biol. Evol. 26, 1421-1430
   Abstract »    Full Text »    PDF »
Simultaneous Bayesian gene tree reconstruction and reconciliation analysis.
O. Akerborg, B. Sennblad, L. Arvestad, and J. Lagergren (2009)
PNAS 106, 5714-5719
   Abstract »    Full Text »    PDF »
Congruent Evolution of Genetic and Environmental Robustness in Micro-RNA.
G. J. Szollosi and I. Derenyi (2009)
Mol. Biol. Evol. 26, 867-874
   Abstract »    Full Text »    PDF »
Darwinian evolution in the light of genomics.
E. V. Koonin (2009)
Nucleic Acids Res. 37, 1011-1034
   Abstract »    Full Text »    PDF »
Molecular Evolution, Functional Variation, and Proposed Nomenclature of the Gene Family That Includes Sphingomyelinase D in Sicariid Spider Venoms.
G. J. Binford, M. R. Bodner, M. H.J. Cordes, K. L. Baldwin, M. R. Rynerson, S. N. Burns, and P. A. Zobel-Thropp (2009)
Mol. Biol. Evol. 26, 547-566
   Abstract »    Full Text »    PDF »
Genetic Diversity in the Paramecium aurelia Species Complex.
F. Catania, F. Wurmser, A. A. Potekhin, E. Przybos, and M. Lynch (2009)
Mol. Biol. Evol. 26, 421-431
   Abstract »    Full Text »    PDF »
Estimating Translational Selection in Eukaryotic Genomes.
M. dos Reis and L. Wernisch (2009)
Mol. Biol. Evol. 26, 451-461
   Abstract »    Full Text »    PDF »
Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world.
E. V. Koonin and Y. I. Wolf (2008)
Nucleic Acids Res. 36, 6688-6719
   Abstract »    Full Text »    PDF »
Estimation of Phylogenetic Inconsistencies in the Three Domains of Life.
V. Soria-Carrasco and J. Castresana (2008)
Mol. Biol. Evol. 25, 2319-2329
   Abstract »    Full Text »    PDF »
Integrating the determinants of suction feeding performance in centrarchid fishes.
R. Holzman, S. W. Day, R. S. Mehta, and P. C. Wainwright (2008)
J. Exp. Biol. 211, 3296-3305
   Abstract »    Full Text »    PDF »
Synonymous and Nonsynonymous Polymorphisms versus Divergences in Bacterial Genomes.
A. L. Hughes, R. Friedman, P. Rivailler, and J. O. French (2008)
Mol. Biol. Evol. 25, 2199-2209
   Abstract »    Full Text »    PDF »
Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata.
S. Lockton, J. Ross-Ibarra, and B. S. Gaut (2008)
PNAS 105, 13965-13970
   Abstract »    Full Text »    PDF »
Evidence of Adaptive Evolution of Accessory Gland Proteins in Closely Related Species of the Drosophila repleta Group.
F. C. Almeida and R. DeSalle (2008)
Mol. Biol. Evol. 25, 2043-2053
   Abstract »    Full Text »    PDF »
Intron Loss Is Associated with Gain of Function in the Evolution of the Gloverin Family of Antibacterial Genes in Bombyx mori.
N. Mrinal and J. Nagaraju (2008)
J. Biol. Chem. 283, 23376-23387
   Abstract »    Full Text »    PDF »
Understanding Randomness and its Impact on Student Learning: Lessons Learned from Building the Biology Concept Inventory (BCI).
K. Garvin-Doxas and M. W. Klymkowsky (2008)
CBE Life Sci Educ 7, 227-233
   Abstract »    Full Text »    PDF »
Near Intron Positions Are Reliable Phylogenetic Markers: An Application to Holometabolous Insects.
V. Krauss, C. Thummler, F. Georgi, J. Lehmann, P. F. Stadler, and C. Eisenhardt (2008)
Mol. Biol. Evol. 25, 821-830
   Abstract »    Full Text »    PDF »
Extremely Intron-Rich Genes in the Alveolate Ancestors Inferred with a Flexible Maximum-Likelihood Approach.
M. Csuros, I. B. Rogozin, and E. V. Koonin (2008)
Mol. Biol. Evol. 25, 903-911
   Abstract »    Full Text »    PDF »
Selection on Major Components of Angiosperm Genomes.
B. S. Gaut and J. Ross-Ibarra (2008)
Science 320, 484-486
   Abstract »    Full Text »    PDF »
Patterns of Molecular Evolution in Caenorhabditis Preclude Ancient Origins of Selfing.
A. D. Cutter, J. D. Wasmuth, and N. L. Washington (2008)
Genetics 178, 2093-2104
   Abstract »    Full Text »    PDF »
Nearly Neutrality and the Evolution of Codon Usage Bias in Eukaryotic Genomes.
S. Subramanian (2008)
Genetics 178, 2429-2432
   Abstract »    Full Text »    PDF »
Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle.
I. J. Tsai, D. Bensasson, A. Burt, and V. Koufopanou (2008)
PNAS 105, 4957-4962
   Abstract »    Full Text »    PDF »
Mammalian non-LTR retrotransposons: For better or worse, in sickness and in health.
V. P. Belancio, D. J. Hedges, and P. Deininger (2008)
Genome Res. 18, 343-358
   Abstract »    Full Text »    PDF »
Extensive Proliferation of Transposable Elements in Heritable Bacterial Symbionts.
G. R. Plague, H. E. Dunbar, P. L. Tran, and N. A. Moran (2008)
J. Bacteriol. 190, 777-779
   Abstract »    Full Text »    PDF »
The Gypsy Database (GyDB) of mobile genetic elements.
C. Llorens, R. Futami, D. Bezemer, and A. Moya (2008)
Nucleic Acids Res. 36, D38-D46
   Abstract »    Full Text »    PDF »
EPGD: a comprehensive web resource for integrating and displaying eukaryotic paralog/paralogon information.
G. Ding, Y. Sun, H. Li, Z. Wang, H. Fan, C. Wang, D. Yang, and Y. Li (2008)
Nucleic Acids Res. 36, D255-D262
   Abstract »    Full Text »    PDF »
Evolutionary Dynamics of Introns in Plastid-Derived Genes in Plants: Saturation Nearly Reached but Slow Intron Gain Continues.
M. K. Basu, I. B. Rogozin, O. Deusch, T. Dagan, W. Martin, and E. V. Koonin (2008)
Mol. Biol. Evol. 25, 111-119
   Abstract »    Full Text »    PDF »
Effects of metabolic rate on protein evolution.
J. F Gillooly, M. W McCoy, and A. P Allen (2007)
Biol Lett 3, 655-660
   Abstract »    Full Text »    PDF »
Long-term evolution of transposable elements.
A. Le Rouzic, T. S. Boutin, and P. Capy (2007)
PNAS 104, 19375-19380
   Abstract »    Full Text »    PDF »
An Unusually Low Microsatellite Mutation Rate in Dictyostelium discoideum, an Organism With Unusually Abundant Microsatellites.
R. McConnell, S. Middlemist, C. Scala, J. E. Strassmann, and D. C. Queller (2007)
Genetics 177, 1499-1507
   Abstract »    Full Text »    PDF »
Ohno's dilemma: Evolution of new genes under continuous selection.
U. Bergthorsson, D. I. Andersson, and J. R. Roth (2007)
PNAS 104, 17004-17009
   Abstract »    Full Text »    PDF »
Rate variation between mitochondrial domains and adaptive evolution in humans.
M. Ingman and U. Gyllensten (2007)
Hum. Mol. Genet. 16, 2281-2287
   Abstract »    Full Text »    PDF »
A Long-Term Evolutionary Pressure on the Amount of Noncoding DNA.
C. Knibbe, A. Coulon, O. Mazet, J.-M. Fayard, and G. Beslon (2007)
Mol. Biol. Evol. 24, 2344-2353
   Abstract »    Full Text »    PDF »
The Origins of Genome Architecture.
H. Abdel-Haleem (2007)
J. Hered. 98, 633-634
   Full Text »    PDF »
Evolution of the vertebrate twist family and synfunctionalization: a mechanism for differential gene loss through merging of expression domains.
I. Gitelman (2007)
Mol. Biol. Evol. 24, 1912-1925
   Abstract »    Full Text »    PDF »
Evolutionarily conserved genes preferentially accumulate introns.
L. Carmel, I. B. Rogozin, Y. I. Wolf, and E. V. Koonin (2007)
Genome Res. 17, 1045-1050
   Abstract »    Full Text »    PDF »
Three distinct modes of intron dynamics in the evolution of eukaryotes.
L. Carmel, Y. I. Wolf, I. B. Rogozin, and E. V. Koonin (2007)
Genome Res. 17, 1034-1044
   Abstract »    Full Text »    PDF »
Centromeres were derived from telomeres during the evolution of the eukaryotic chromosome.
A. Villasante, J. P. Abad, and M. Mendez-Lago (2007)
PNAS 104, 10542-10547
   Abstract »    Full Text »    PDF »
Exceptionally High Density of NUMTs in the Honeybee Genome.
P. Pamilo, L. Viljakainen, and A. Vihavainen (2007)
Mol. Biol. Evol. 24, 1340-1346
   Abstract »    Full Text »    PDF »
Colloquium Papers: The frailty of adaptive hypotheses for the origins of organismal complexity.
M. Lynch (2007)
PNAS 104, 8597-8604
   Abstract »    Full Text »    PDF »
The Orientia tsutsugamushi genome reveals massive proliferation of conjugative type IV secretion system and host cell interaction genes.
N.-H. Cho, H.-R. Kim, J.-H. Lee, S.-Y. Kim, J. Kim, S. Cha, S.-Y. Kim, A. C. Darby, H.-H. Fuxelius, J. Yin, et al. (2007)
PNAS 104, 7981-7986
   Abstract »    Full Text »    PDF »
The mode and tempo of genome size evolution in eukaryotes.
M. J. Oliver, D. Petrov, D. Ackerly, P. Falkowski, and O. M. Schofield (2007)
Genome Res. 17, 594-601
   Abstract »    Full Text »    PDF »
The Evolution of Spliceosomal Introns in Alveolates.
H. D. Nguyen, M. Yoshihama, and N. Kenmochi (2007)
Mol. Biol. Evol. 24, 1093-1096
   Abstract »    Full Text »    PDF »
Position of the Final Intron in Full-Length Transcripts: Determined by NMD?.
D. G. Scofield, X. Hong, and M. Lynch (2007)
Mol. Biol. Evol. 24, 896-899
   Abstract »    Full Text »    PDF »
Scaling of number, size, and metabolic rate of cells with body size in mammals.
V. M. Savage, A. P. Allen, J. H. Brown, J. F. Gillooly, A. B. Herman, W. H. Woodruff, and G. B. West (2007)
PNAS 104, 4718-4723
   Abstract »    Full Text »    PDF »
Accumulation of Deleterious Mutations in Small Abiotic Populations of RNA.
S. J. Soll, C. D. Arenas, and N. Lehman (2007)
Genetics 175, 267-275
   Abstract »    Full Text »    PDF »
Patterns of Intron Loss and Gain in Plants: Intron Loss-Dominated Evolution and Genome-Wide Comparison of O. sativa and A. thaliana.
S. W. Roy and D. Penny (2007)
Mol. Biol. Evol. 24, 171-181
   Abstract »    Full Text »    PDF »
Intron Size, Abundance, and Distribution within Untranslated Regions of Genes.
X. Hong, D. G. Scofield, and M. Lynch (2006)
Mol. Biol. Evol. 23, 2392-2404
   Abstract »    Full Text »    PDF »
Large Global Effective Population Sizes in Paramecium.
M. S. Snoke, T. U. Berendonk, D. Barth, and M. Lynch (2006)
Mol. Biol. Evol. 23, 2474-2479
   Abstract »    Full Text »    PDF »
Allopatric origins of microbial species.
R. J Whitaker (2006)
Phil Trans R Soc B 361, 1975-1984
   Abstract »    Full Text »    PDF »
Sequence diversity of the mucABD locus in Pseudomonas aeruginosa isolates from patients with cystic fibrosis..
A. Bragonzi, L. Wiehlmann, J. Klockgether, N. Cramer, D. Worlitzsch, G. Doring, and B. Tummler (2006)
Microbiology 152, 3261-3269
   Abstract »    Full Text »    PDF »
Evolution of complexity in signaling pathways.
O. S. Soyer and S. Bonhoeffer (2006)
PNAS 103, 16337-16342
   Abstract »    Full Text »    PDF »
Comparative genomics of the lactic acid bacteria.
K. Makarova, A. Slesarev, Y. Wolf, A. Sorokin, B. Mirkin, E. Koonin, A. Pavlov, N. Pavlova, V. Karamychev, N. Polouchine, et al. (2006)
PNAS 103, 15611-15616
   Abstract »    Full Text »    PDF »
Evolution of sensory complexity recorded in a myxobacterial genome.
B. S. Goldman, W. C. Nierman, D. Kaiser, S. C. Slater, A. S. Durkin, J. A. Eisen, C. M. Ronning, W. B. Barbazuk, M. Blanchard, C. Field, et al. (2006)
PNAS 103, 15200-15205
   Abstract »    Full Text »    PDF »
Evolution of the Cichlid Visual Palette through Ontogenetic Subfunctionalization of the Opsin Gene Arrays.
T. C. Spady, J. W. L. Parry, P. R. Robinson, D. M. Hunt, J. K. Bowmaker, and K. L. Carleton (2006)
Mol. Biol. Evol. 23, 1538-1547
   Abstract »    Full Text »    PDF »
Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity.
M. Freeling and B. C. Thomas (2006)
Genome Res. 16, 805-814
   Abstract »    Full Text »    PDF »
Very little intron loss/gain in Plasmodium: Intron loss/gain mutation rates and intron number.
S. W. Roy and D. L. Hartl (2006)
Genome Res. 16, 750-756
   Abstract »    Full Text »    PDF »
Complexity, simplicity, and epidemiology.
N. Pearce and F. Merletti (2006)
Int. J. Epidemiol. 35, 515-519
   Full Text »    PDF »
Mutation Rate and the Cost of Complexity.
R. Haygood (2006)
Mol. Biol. Evol. 23, 957-963
   Abstract »    Full Text »    PDF »
Population size does not influence mitochondrial genetic diversity in animals..
E. Bazin, S. Glemin, and N. Galtier (2006)
Science 312, 570-572
   Abstract »    Full Text »    PDF »
Objects that make objects: the population dynamics of structural complexity.
J. P Crutchfield and O. Gornerup (2006)
J R Soc Interface 3, 345-349
   Abstract »    Full Text »    PDF »
Evolution of Programmed DNA Rearrangements in a Scrambled Gene.
L. C. Wong and L. F. Landweber (2006)
Mol. Biol. Evol. 23, 756-763
   Abstract »    Full Text »    PDF »
Mutation pressure and the evolution of organelle genomic architecture..
M. Lynch, B. Koskella, and S. Schaack (2006)
Science 311, 1727-1730
   Abstract »    Full Text »    PDF »
Cryptic Genetic Variation Is Enriched for Potential Adaptations.
J. Masel (2006)
Genetics 172, 1985-1991
   Abstract »    Full Text »    PDF »
Patterns of Protein Evolution in Tetrahymena thermophila: Implications for Estimates of Effective Population Size.
L. A. Katz, O. Snoeyenbos-West, and F. P. Doerder (2006)
Mol. Biol. Evol. 23, 608-614
   Abstract »    Full Text »    PDF »
Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication.
B. A. Chapman, J. E. Bowers, F. A. Feltus, and A. H. Paterson (2006)
PNAS 103, 2730-2735
   Abstract »    Full Text »    PDF »
Role of positive selection in the retention of duplicate genes in mammalian genomes.
S.-H. Shiu, J. K. Byrnes, R. Pan, P. Zhang, and W.-H. Li (2006)
PNAS 103, 2232-2236
   Abstract »    Full Text »    PDF »
The Origins of Eukaryotic Gene Structure.
M. Lynch (2006)
Mol. Biol. Evol. 23, 450-468
   Abstract »    Full Text »    PDF »
Pleiotropic functions of a conserved insect-specific Hox peptide motif.
C. T. Hittinger, D. L. Stern, and S. B. Carroll (2005)
Development 132, 5261-5270
   Abstract »    Full Text »    PDF »
Comparative genomics of Gossypium and Arabidopsis: Unraveling the consequences of both ancient and recent polyploidy.
J. Rong, J. E. Bowers, S. R. Schulze, V. N. Waghmare, C. J. Rogers, G. J. Pierce, H. Zhang, J. C. Estill, and A. H. Paterson (2005)
Genome Res. 15, 1198-1210
   Abstract »    Full Text »    PDF »
Unexpected Diversity and Differential Success of DNA Transposons in Four Species of Entamoeba Protozoans.
E. J. Pritham, C. Feschotte, and S. R. Wessler (2005)
Mol. Biol. Evol. 22, 1751-1763
   Abstract »    Full Text »    PDF »
Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell.
K. S. Makarova, Y. I. Wolf, S. L. Mekhedov, B. G. Mirkin, and E. V. Koonin (2005)
Nucleic Acids Res. 33, 4626-4638
   Abstract »    Full Text »    PDF »
Parallel evolution of chimeric fusion genes.
C. D. Jones and D. J. Begun (2005)
PNAS 102, 11373-11378
   Abstract »    Full Text »    PDF »
Epistasis and the Adaptability of an RNA Virus.
R. Sanjuan, J. M. Cuevas, A. Moya, and S. F. Elena (2005)
Genetics 170, 1001-1008
   Abstract »    Full Text »    PDF »
Evolutionary Capacitance May Be Favored by Natural Selection.
J. Masel (2005)
Genetics 170, 1359-1371
   Abstract »    Full Text »    PDF »
Pyoverdine Receptor: a Case of Positive Darwinian Selection in Pseudomonas aeruginosa.
B. Tummler and P. Cornelis (2005)
J. Bacteriol. 187, 3289-3292
   Full Text »    PDF »
Origin and Evolution of a Chimeric Fusion Gene in Drosophila subobscura, D. madeirensis and D. guanche.
C. D. Jones, A. W. Custer, and D. J. Begun (2005)
Genetics 170, 207-219
   Abstract »    Full Text »    PDF »
The Origin of Subfunctions and Modular Gene Regulation.
A. Force, W. A. Cresko, F. B. Pickett, S. R. Proulx, C. Amemiya, and M. Lynch (2005)
Genetics 170, 433-446
   Abstract »    Full Text »    PDF »
Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes.
C. F. Baer, F. Shaw, C. Steding, M. Baumgartner, A. Hawkins, A. Houppert, N. Mason, M. Reed, K. Simonelic, W. Woodard, et al. (2005)
PNAS 102, 5785-5790
   Abstract »    Full Text »    PDF »
Complex Spliceosomal Organization Ancestral to Extant Eukaryotes.
L. Collins and D. Penny (2005)
Mol. Biol. Evol. 22, 1053-1066
   Abstract »    Full Text »    PDF »
The Evolution of Transcription-Initiation Sites.
M. Lynch, D. G. Scofield, and X. Hong (2005)
Mol. Biol. Evol. 22, 1137-1146
   Abstract »    Full Text »    PDF »
Complex early genes.
S. W. Roy and W. Gilbert (2005)
PNAS 102, 1986-1991
   Abstract »    Full Text »    PDF »
Evidence for Abundant Slightly Deleterious Polymorphisms in Bacterial Populations.
A. L. Hughes (2005)
Genetics 169, 533-538
   Abstract »    Full Text »    PDF »
Rapid Subfunctionalization Accompanied by Prolonged and Substantial Neofunctionalization in Duplicate Gene Evolution.
X. He and J. Zhang (2005)
Genetics 169, 1157-1164
   Abstract »    Full Text »    PDF »
Population Dynamics Through the Lens of Extreme Environments.
R. J. Whitaker and J. F. Banfield (2005)
Reviews in Mineralogy and Geochemistry 59, 259-277
   Full Text »    PDF »
Polymorphix: a sequence polymorphism database.
E. Bazin, L. Duret, S. Penel, and N. Galtier (2005)
Nucleic Acids Res. 33, D481-D484
   Abstract »    Full Text »    PDF »
On the Evolution of Codon Volatility.
J. Zhang (2005)
Genetics 169, 495-501
   Abstract »    Full Text »    PDF »
Simplicity and Complexity of Microsporidian Genomes.
P. J. Keeling and C. H. Slamovits (2004)
Eukaryot. Cell 3, 1363-1369
   Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)