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

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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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C. F. Baer, F. Shaw, C. Steding, M. Baumgartner, A. Hawkins, A. Houppert, N. Mason, M. Reed, K. Simonelic, W. Woodard, et al. (2005)
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   Abstract »    Full Text »    PDF »
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L. Collins and D. Penny (2005)
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   Abstract »    Full Text »    PDF »
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M. Lynch, D. G. Scofield, and X. Hong (2005)
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   Abstract »    Full Text »    PDF »
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S. W. Roy and W. Gilbert (2005)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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I. Hiratani, A. Leskovar, and D. M. Gilbert (2004)
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   Abstract »    Full Text »    PDF »
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   Full Text »    PDF »
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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »