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Evolutionary Dynamics of Recently Duplicated Genes: Selective Constraints on Diverging Paralogs in the Drosophila pseudoobscura Genome

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Abstract

Duplicated genes produce genetic variation that can influence the evolution of genomes and phenotypes. In most cases, for a duplicated gene to contribute to evolutionary novelty it must survive the early stages of divergence from its paralog without becoming a pseudogene. I examined the evolutionary dynamics of recently duplicated genes in the Drosophila pseudoobscura genome to understand the factors affecting these early stages of evolution. Paralogs located in closer proximity have higher sequence identity. This suggests that gene conversion occurs more often between duplications in close proximity or that there is more genetic independence between distant paralogs. Partially duplicated genes have a higher likelihood of pseudogenization than completely duplicated genes, but no single factor significantly contributes to the selective constraints on a completely duplicated gene. However, DNA-based duplications and duplications within chromosome arms tend to produce longer duplication tracts than retroposed and inter-arm duplications, and longer duplication tracts are more likely to contain a completely duplicated gene. Therefore, the relative position of paralogs and the mechanism of duplication indirectly affect whether a duplicated gene is retained or pseudogenized.

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Acknowledgements

N. Hasan, B. B. Hilldorfer, R. LeGros, and R. L. Zindren helped with sorting the BLAST hits, and N. Hasan and B. B. Hilldorfer assisted in testing the recently duplicated genes for CNP. S. W. Schaeffer and J. R. Arguello provided useful discussion and comments on the manuscript. V. Gotea and W. Makalowski provided assistance with RepeatMasker and MegaBLAST, and V. Gotea also commented on the manuscript. This material is partially based on work supported by the National Science Foundation under Grant No. 0608186, awarded to RPM. Any opinions, findings and conclusions or recommendations expressed in this material are those of the author and do not necessarily reflect the views of the National Science Foundation.

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  1. Intercollege Graduate Program in Genetics and Department of Biology, The Pennsylvania State University, University Park, PA, 16802, USA

    Richard P. Meisel

  2. Department of Molecular Biology and Genetics, Cornell University, 227 Biotechnology Bldg., Ithaca, NY, 14853, USA

    Richard P. Meisel

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Correspondence to Richard P. Meisel.

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Supplementary Figure S1

Relative rates of amino acid evolution for ancestral and derived paralogs. Estimated amino acid substitutions along the ancestral (dark gray) and derived (white) lineages are graphed for each duplicated gene in the dataset; each pair of bars represents the ancestral and derived copy of a duplicated gene, respectively. Paralogs for which the ancestral and derived copy cannot be distinguished are indicated by two gray bars. Paralogs for which the derived copy contains (A) a partial coding sequence and (B) a complete coding sequence are shown, and the status of the open reading frame of the derived copy is indicated below the X-axis. A relative rate test based on a chi-square test was used to determine if the difference in amino acid substitutions in the ancestral and derived copy of each duplicated gene is significant (Tajima 1993). Paralogs for which the test could not be performed (because of too few substitutions between the paralogs) are indicated by the black bars labeled “N/A”. Paralogs for which the test is significant at P < 0.05 are indicated by a single asterisk and paralogs for which the test is significant at P < 0.005 are indicated by two asterisks. Two completely duplicated genes in which the derived copy is evolving significantly faster than the ancestral copy are labeled. Supplementary material 1 (PDF 304 kb)

Supplementary Figure S2

Tissue expression of D. melanogaster orthologs of completely duplicated genes. Tissue expression data were retrieved for the D. melanogaster orthologs of each completely duplicated gene in the D. pseudoobscura genome (Chintapalli et al. 2007). For each tissue, the number of non-degenerated and degenerated genes expressed and not expressed in that tissue is graphed. A single asterisk indicates a significant departure from independence between degeneration and expression using a G test with P < 0.05. Supplementary material 2 (PDF 272 kb)

Supplementary material 3 (PDF 27 kb)

Supplementary Table S1

Copy number polymorphism primers. Supplementary material 4 (XLS 17 kb)

Supplementary Table S2

Data on each duplicated gene. Supplementary material 5 (XLS 67 kb)

239_2009_9254_MOESM6_ESM.zip

Supplementary Data-Annotated alignments of duplicated genes. Alignments are in the MEGA format, with coding and non-coding sequences annotated. Ancestral copies are indicated by “anc” in the sequence name, and derived copies are indicated by “dup” in the sequence name. For duplicated genes where the ancestral and derived copies could not be determined, the two copies are named “copyA” and “copyB”. Coding sequences were reverse complemented in some alignments (relative to the rest of the aligned sequence) containing multiple genes to keep open reading frames in proper orientation; this was done if the coding sequences were in opposite orientations. The following genes were reverse complemented relative to the rest of the aligned sequence: CG15287, CG14860,CG8016, CG8589, CG13190, CG13063, CG11070, CG16734, CG16983. Supplementary material 6 (ZIP 198 kb)

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Meisel, R.P. Evolutionary Dynamics of Recently Duplicated Genes: Selective Constraints on Diverging Paralogs in the Drosophila pseudoobscura Genome. J Mol Evol 69, 81–93 (2009). https://doi.org/10.1007/s00239-009-9254-1

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