The study of the evolution of novel genes generally focuses on the formation of new coding sequences. However, equally important in the evolution of novel functional genes are the formation of regulatory regions that allow the expression of the genes and the effects of the new genes in the organism as well. Herein, we discuss the current knowledge on the evolution of novel functional genes, and we examine in more detail the youngest genes discovered. We examine the existing data on a very recent and rapidly evolving cluster of duplicated genes, the Sdic gene cluster. This cluster of genes is an excellent model for the evolution of novel genes, as it is very recent and may still be in the process of evolving. 1. Introduction The availability of complete genome sequences allows the comparison of genomes, thus revealing the differences in gene complement and demonstrating the nature of the changes that occur in the evolution of genomes. In particular, genomic analysis showed that more than one-third of the eukaryotic genome is composed of gene duplications and gene families (e.g., [1–4]), highlighting the prominence of duplications in the evolution of genomes. The study of whole genomes also allows an analysis of the rates and dynamics of duplications as well as the divergence and silencing of duplicates (e.g., [5–7]). Moreover, evidence indicates that the rates of duplication are extremely high and of the same order of magnitude as the rate of mutation per nucleotide; for example, the frequency of duplication for coding genes was found to be 0.01 per gene per million years [8] and for internal duplications of gene segments, 0.001–0.013 duplications/gene per million years [9]. The fates of gene duplicates can be very different according to the mutations they undergo and the selective pressures they are under. After a gene is duplicated, the most common fate seems to be the loss of function of one copy by the acquisition of degenerative mutations, while the other copy retains the original function. The originally identical copies can also both be maintained in the genome, allowing a higher production of the corresponding RNA or protein. Subsequent mutation by retrotransposon insertion into one of the copies can affect adaptive evolution because the effect on the phenotype can in some cases be beneficial to the organism [10]. Partial gene duplications can also occur, and if the duplicated part involves a structural or functional domain the new gene can increase the functional complexity of the encoded protein. It has also been proposed that if two copies of
References
[1]
S. Kaul, H. L. Koo, J. Jenkins et al., “Analysis of the genome sequence of the flowering plant Arabidopsis thaliana,” Nature, vol. 408, no. 6814, pp. 796–815, 2000.
[2]
G. M. Rubin, M. D. Yandell, J. R. Wortman et al., “Comparative genomics of the eukaryotes,” Science, vol. 287, no. 5461, pp. 2204–2215, 2000.
[3]
J. C. . Venter, M. D. Adams, E. W. Myers, P. W. Li, R. J. Mural, G. G. Sutton, et al., “The sequence of the human genome,” Science, vol. 291, pp. 1304–1351, 2001.
[4]
R. D. Morin, E. Chang, A. Petrescu et al., “Sequencing and analysis of 10,967 full-length cDNA clones from Xenopus laevis and Xenopus tropicalis reveals post-tetraploidization transcriptome remodeling,” Genome Research, vol. 16, no. 7, pp. 947–803, 2006.
[5]
Z. Gu, D. Nicolae, H. H. S. Lu, and W. H. Li, “Rapid divergence in expression between duplicate genes inferred from microarray data,” Trends in Genetics, vol. 18, no. 12, pp. 609–613, 2002.
[6]
P. Zhang, Z. Gu, and W. H. Li, “Different evolutionary patterns between young duplicate genes in the human genome,” Genome Biology, vol. 4, no. 9, article R56, 2003.
[7]
L. Bu, U. Bergthorsson, and V. Katju, “Local synteny and codon usage contribute to asymmetric sequence divergence of Saccharomyces cerevisiae gene duplicates,” BMC Evolutionary Biology, vol. 11, article 279, 2011.
[8]
M. Lynch and J. S. Conery, “The evolutionary fate and consequences of duplicate genes,” Science, vol. 290, no. 5494, pp. 1151–1155, 2000.
[9]
X. Gao and M. Lynch, “Ubiquitous internal gene duplication and intron creation in eukaryotes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 49, pp. 20818–20823, 2009.
[10]
A. Kanazawa, B. Liu, F. Kong, S. Arase, and J. Abe, “Adaptive evolution involving gene duplication and insertion of a novel Ty1/copia-like retrotransposon in soybean,” Journal of Molecular Evolution, vol. 69, no. 2, pp. 164–175, 2009.
[11]
A. Force, M. Lynch, F. B. Pickett, A. Amores, Y. L. Yan, and J. Postlethwait, “Preservation of duplicate genes by complementary, degenerative mutations,” Genetics, vol. 151, no. 4, pp. 1531–1545, 1999.
[12]
H. Innan and F. Kondrashov, “The evolution of gene duplications: classifying and distinguishing between models,” Nature Reviews Genetics, vol. 11, no. 2, pp. 97–108, 2010.
[13]
J. B. S. Haldane, The Causes of Evolution, Princeton University Press, 1990.
[14]
C. B. Bridges, “The Bar “gene” a duplication,” Science, vol. 83, no. 2148, pp. 210–211, 1936.
[15]
H. J. Muller, “Bar duplication,” Science, vol. 83, no. 2161, pp. 528–530, 1936.
[16]
S. Ohno, Evolution by Gene Duplication, Springer, 1970.
[17]
V. F. Irish and A. Litt, “Flower development and evolution: gene duplication, diversification and redeployment,” Current Opinion in Genetics and Development, vol. 15, no. 4, pp. 454–460, 2005.
[18]
T. Ohta, “Role of gene duplication in evolution,” Genome, vol. 31, no. 1, pp. 304–310, 1989.
[19]
J. S. Taylor and J. Raes, “Duplication and divergence: the evolution of new genes and old ideas,” Annual Review of Genetics, vol. 38, pp. 615–643, 2004.
[20]
J. Zhang, “Evolution by gene duplication: an update,” Trends in Ecology and Evolution, vol. 18, no. 6, pp. 292–298, 2003.
[21]
M. Long, E. Betrán, K. Thornton, and W. Wang, “The origin of new genes: glimpses from the young and old,” Nature Reviews Genetics, vol. 4, no. 11, pp. 865–875, 2003.
[22]
C. D. Jones, A. W. Custer, and D. J. Begun, “Origin and evolution of a chimeric fusion gene in Drosophila subobscura D. madeirensis and D. guanche,” Genetics, vol. 170, no. 1, pp. 207–219, 2005.
[23]
W. Wang, H. Yu, and M. Long, “Duplication-degeneration as a mechanism of gene fission and the origin of new genes in Drosophila species,” Nature Genetics, vol. 36, no. 5, pp. 523–527, 2004.
[24]
H. Kaessmann, “Origins, evolution, and phenotypic impact of new genes,” Genome Research, vol. 20, no. 10, pp. 1313–1326, 2010.
[25]
G. A. Wray, “The evolutionary significance of cis-regulatory mutations,” Nature Reviews Genetics, vol. 8, no. 3, pp. 206–216, 2007.
[26]
P. J. Wittkopp, “Evolution of cis-regulatory sequence and function in Diptera,” Heredity, vol. 97, no. 3, pp. 139–147, 2006.
[27]
S. B. Carroll, “Evolution at two levels: on genes and form,” PLoS Bology, vol. 3, no. 7, p. e245, 2005.
[28]
F. Rodriguez-Trelles, R. Tarríol, and F. J. Ayala, “Evolution of cis-regulatory regions versus codifying regions,” International Journal of Developmental Biology, vol. 47, no. 7-8, pp. 665–673, 2003.
[29]
R. L. Rogers, T. Bedford, and D. L. Hart, “Formation and longevity of chimeric and duplicate genes in Drosophila melanogaster,” Genetics, vol. 181, no. 1, pp. 313–322, 2009.
[30]
Q. Zhou, G. Zhang, Y. Zhang et al., “On the origin of new genes in Drosophila,” Genome Research, vol. 18, no. 9, pp. 1446–1455, 2008.
[31]
R. L. Rogers and D. L. Hartl, “Chimeric genes as a source of rapid evolution in Drosophila melanogaster,” Molecular Biology and Evolution, vol. 29, no. 2, pp. 517–529, 2012.
[32]
S. Yang, J. R. Arguello, X. Li et al., “Repetitive element-mediated recombination as a mechanism for new gene origination in Drosophila,” PLoS Genetics, vol. 4, no. 1, article e3, 2008.
[33]
D. A. Petrov and D. L. Hartl, “High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups,” Molecular Biology and Evolution, vol. 15, no. 3, pp. 293–302, 1998.
[34]
D. A. Petrov, E. R. Lozovskaya, and D. L. Harti, “High intrinsic rate of DNA loss in Drosophila,” Nature, vol. 384, no. 6607, pp. 346–349, 1996.
[35]
D. A. Petrov and D. L. Hartl, “Trash DNA is what gets thrown away: high rate of DNA loss in Drosophila,” Gene, vol. 205, no. 1-2, pp. 279–289, 1997.
[36]
M. E. Johnson, L. Viggiano, J. A. Bailey et al., “Positive selection of a gene family during the emergence of humans and African apes,” Nature, vol. 413, no. 6855, pp. 514–519, 2001.
[37]
M. T. Levine, C. D. Jones, A. D. Kern, H. A. Lindfors, and D. J. Begun, “Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 26, pp. 9935–9939, 2006.
[38]
T. J. A. J. Heinen, F. Staubach, D. H？ming, and D. Tautz, “Emergence of a New Gene from an Intergenic Region,” Current Biology, vol. 19, no. 18, pp. 1527–1531, 2009.
[39]
M. Toll-Riera, N. Bosch, N. Bellora et al., “Origin of primate orphan genes: a comparative genomics approach,” Molecular Biology and Evolution, vol. 26, no. 3, pp. 603–612, 2009.
[40]
R. L. Rogers, T. Bedford, A. M. Lyons, and D. L. Hartl, “Adaptive impact of the chimeric gene Quetzalcoatl in Drosophila melanogaster,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 24, pp. 10943–10948, 2010.
[41]
C. Fan and M. Long, “A new retroposed gene in Drosophila heterochromatin detected by microarray-based comparative genomic hybridization,” Journal of Molecular Evolution, vol. 64, no. 2, pp. 272–283, 2007.
[42]
J. R. Arguello, Y. Chen, S. Yang, W. Wang, and M. Long, “Origination of an X-linked testes chimeric gene by illegitimate recombination in Drosophila,” PLoS Genetics, vol. 2, no. 5, article e77, 2006.
[43]
W. Wang, J. Zhang, C. Alvarez, A. Llopart, and M. Long, “The origin of the jingwei gene and the complex modular structure of its parental gene, yellow emperor, in Drosophila melanogaster,” Molecular Biology and Evolution, vol. 17, no. 9, pp. 1294–1301, 2000.
[44]
W. Wang, F. G. Brunet, E. Nevo, and M. Long, “Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 7, pp. 4448–4453, 2002.
[45]
M. Long, M. Deutsch, W. Wang, E. Betrán, F. G. Brunet, and J. Zhang, “Origin of new genes: evidence from experimental and computational analyses,” Genetica, vol. 118, no. 2-3, pp. 171–182, 2003.
[46]
C. D. Jones and D. J. Begun, “Parallel evolution of chimeric fusion genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 32, pp. 11373–11378, 2005.
[47]
D. I. Nurminsky, M. V. Nurminskaya, D. De Aguiar, and D. L. Hartl, “Selective sweep of a newly evolved sperm-specific gene in Drosophila,” Nature, vol. 396, no. 6711, pp. 572–575, 1998.
[48]
R. Ponce, “The use of a non-LTR element to date the formation of the Sdic gene cluster,” Genetica, vol. 131, no. 3, pp. 315–324, 2007.
[49]
S.-D. Yeh, T. Do, C. Chan et al., “Functional evidence that a recently evolved Drosophila sperm-specific gene boosts sperm competition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 6, pp. 2043–2048, 2012.
[50]
E. Betrán and M. Long, “Dntf-2r, a young Drosophila retroposed gene with specific male expression under positive Darwinian selection,” Genetics, vol. 164, no. 3, pp. 977–988, 2003.
[51]
Y. Ding, L. Zhao, S. Yang et al., “A young Drosophila duplicate gene plays essential roles in spermatogenesis by regulating several Y-linked male fertility genes,” PLoS Genetics, vol. 6, no. 12, article e1001255, 2010.
[52]
S. Chen, H. Yang, B. H. Krinsky, A. Zhang, and M. Long, “Roles of young serine-endopeptidase genes in survival and reproduction revealed rapid evolution of phenotypic effects at adult stages,” Fly, vol. 5, pp. 345–351, 2011.
[53]
S. T. Chen, H. C. Cheng, D. A. Barbash, and H. P. Yang, “Evolution of hydra, a recently evolved testis-expressed gene with nine alternative first exons in Drosophila melanogaster,” PLoS Genetics, vol. 3, no. 7, article e107, 2007.
[54]
D. V. Babushok, K. Ohshima, E. M. Ostertag et al., “A novel testis ubiquitin-binding protein gene arose by exon shuffling in hominoids,” Genome Research, vol. 17, no. 8, pp. 1129–1138, 2007.
[55]
D. T. Sullivan, W. T. Starmer, S. W. Curtiss, M. Menotti-Raymond, and J. Yum, “Unusual molecular evolution of an Adh pseudogene in Drosophila,” Molecular Biology and Evolution, vol. 11, no. 3, pp. 443–458, 1994.
[56]
C. T. Ting, S. C. Tsaur, M. L. Wu, and C. I. Wu, “A rapidly evolving homeobox at the site of a hybrid sterility gene,” Science, vol. 282, no. 5393, pp. 1501–1504, 1998.
[57]
C. T. Ting, S. C. Tsaur, S. Sun et al., “Gene duplication and speciation in Drosophila: evidence from the Odysseus locus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 33, pp. 12232–12235, 2004.
[58]
B. Loppin, D. Lepetit, S. Dorus, P. Couble, and T. L. Karr, “Origin and neofunctionalization of a Drosophila paternal effect gene essential for zygote viability,” Current Biology, vol. 15, no. 2, pp. 87–93, 2005.
[59]
R. Dubruille, G. A. Orsi, L. Delabaere et al., “Specialization of a drosophila capping protein essential for the protection of sperm telomeres,” Current Biology, vol. 20, no. 23, pp. 2090–2099, 2010.
[60]
T. Matsuo, “Rapid evolution of two odorant-binding protein genes, Obp57d and Obp57e, in the Drosophila melanogaster species group,” Genetics, vol. 178, no. 2, pp. 1061–1072, 2008.
[61]
E. Harada, J. Nakagawa, T. Asano et al., “Functional evolution of duplicated odorant-binding protein genes, Obp57d and Obp57e, in Drosophila,” PLoS ONE, vol. 7, no. 1, article e29710, 2012.
[62]
E. Betrán, W. Wang, L. Jin, and M. Long, “Evolution of the Phosphoglycerate mutase processed gene in human and chimpanzee revealing the origin of a new primate gene,” Molecular Biology and Evolution, vol. 19, no. 5, pp. 654–663, 2002.
[63]
R. J. Kulathinal, S. A. Sawyer, C. D. Bustamante, D. Nurminsky, R. Ponce, and J. M. Ranz, “Selective sweep in the evolution of a new sperm-specific gene in Drosophila,” in Selective Sweep, D. Nurminsky, Ed., pp. 22–33, Springer, Boston, Mass, USA, 2005.
[64]
R. Nielsen, C. Bustamante, A. G. Clark et al., “A scan for positively selected genes in the genomes of humans and chimpanzees,” PLoS Bology, vol. 3, no. 6, article e170, 2005.
[65]
E. Betrán, K. Thornton, and M. Long, “Retroposed new genes out of the X in Drosophila,” Genome Research, vol. 12, no. 12, pp. 1854–1859, 2002.
[66]
J. B. S. Haldane, The Causes of Evolution, Princeton University Press, 1990.
[67]
M. J. Madison-Villar and P. Michalak, “Misexpression of testicular microRNA in sterile Xenopus hybrids points to tetrapod-specific microRNAs associated with male fertility,” Journal of Molecular Evolution, vol. 73, pp. 316–324, 2011.
[68]
D. I. Nurminsky, M. V. Nurminskaya, E. V. Benevolenskaya, Y. Y. Shevelyov, D. L. Hartl, and V. A. Gvozdev, “Cytoplasmic dynein intermediate-chain isoforms with different targeting properties created by tissue-specific alternative splicing,” Molecular and Cellular Biology, vol. 18, no. 11, pp. 6816–6825, 1998.
[69]
J. M. Ranz, A. R. Ponce, D. L. Hartl, and D. Nurminsky, “Origin and evolution of a new gene expressed in the Drosophila sperm axoneme,” Genetica, vol. 118, no. 2-3, pp. 233–244, 2003.
[70]
R. Ponce and D. L. Hartl, “The evolution of the novel Sdic gene cluster in Drosophila melanogaster,” Gene, vol. 376, no. 2, pp. 174–183, 2006.
[71]
R. Ponce, “The recent origin of the Sdic gene cluster in the melanogaster subgroup,” Genetica, vol. 135, no. 3, pp. 415–418, 2009.
[72]
B. R. Graveley, A. N. Brooks, J. W. Carlson et al., “The developmental transcriptome of Drosophila melanogaster,” Nature, vol. 471, no. 7339, pp. 473–479, 2011.
[73]
M. Long and C. H. Langley, “Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila,” Science, vol. 259, no. 5104, pp. 91–95, 1993.
[74]
D. Nurminsky, D. De Aguiar, C. D. Bustamante, and D. L. Hartl, “Chromosomal effects of rapid gene evolution in drosophila melanogaster,” Science, vol. 291, no. 5501, pp. 128–130, 2001.
[75]
M. Touchon, C. Hoede, O. Tenaillon et al., “Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths,” PLoS Genetics, vol. 5, no. 1, article e1000344, 2009.
