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  4. Manyuan Long

Manyuan Long

Professor
mlong@uchicago.edu
Research Summary
//// Since my doctoral study in California in the early 1990s, I have been focusing on the study of a new and major scientific problem: How does a gene originate and evolve? The approaches I have developed and are being used to investigate the new gene problem include theoretical, computational, and molecular experimental approaches. We are currently exploring following scientific issues: #Phenotypic effects and functions of new genes; #Evolution of gene essentiality in development; #Evolutionary analysis of gene interactions with new genes; #Sex selection and sexual conflict on new genes: #De novo gene origination. //// Our scientific works have been recorded in ~200 publications of research reports, commentaries, reviews, interviews and popular science articles with numerous reports of news media. 110 research articles are selected below. Most of their pdf files can be found in the lab website. Besides, five books and monographs were also published: 2021. How Do New Genes Originate and Evolve? Genes. With E. Beltran 2020. Walter Gilbert: Selected Works. 614 pages. World Scientific, Singapore. With W. Gilbert. 2019. Evolution of Genes and Genomes. 174 pages. Science China Life Science. With B. Shen 2010. Darwin’s Heritage Today. 385 pages. Higher Education Press. With H. Gu and Z. Zhou 2003. Origin and Evolution of New Gene Functions. Volume 10, Contemporary Issues in Genetics and Evolution. 202 pages. Kluwer Academic Publishers. The Netherlands. //// Our works have generated scientific and societal impacts: ## Scientific impacts: #The American Association for the Advancement of Science (AAAS) summarized my contribution when conferring me with a fellow honor (2014 AAAS Fellow) as “You are being honored: For distinguished contributions to the fields of molecular evolution and genetics, particularly for starting and leading the area of new gene evolution using experimental and computational genomics and molecular biology”. #Our discovers have helped shape the new chapters and sections about new gene evolution in major textbooks pf evolutionary biology (e.g. Douglas Futuyma, 2009 and 2005, Evolution, Sinauer, Massachusetts; Michael Lynch, 2007, The Origins of Genome Architecture, Sinauer, Massachesetts; Wen-Hsiung Li, 1997, Molecular Evolution, Sinauer, Massachusetts; Roderic Page and Edward Holmes, 1998, Molecular Evolution. Blackwell Science London). Nature published a News Feature to highlight our discovery of a large number of de novo genes in Oryza (Levy, 2019. Genes from the Junkyard. Nature 574: 314-316). ## Societal impacts: #New York Times, Washington Times, Chicago Tribune, Sacramento Bee, The Huffington Post, La Vanguardia, the New Scientist, the Scientist, Discover, La Recherche, Wen Hui Bao, and other news media in US, Europe, East Asia reported in various languages his scientific discovers and commentaries. #Our research results summarized in a Nature Rev Genet article (Manyuan Long et al, 2003) were cited as major evidence for a successful defense of Amendment I to the United States Constitution in the nationally concerned case of Kitzmiller et al. vs. Dover Area School District in Pennsylvania in 2005. #American Scientist published a feature popular science article by us to discuss de novo gene origination (Mortola and Long, 2021. New Genes Born to Junk. May-June Issue.) Quanta magazine published two interviews with me to discuss de novo gene origination and evolution of gene essentiality (Callier, 2020. Where do new genes come from. April 9. Callier, 2020. Scientists Find Vital Genes Evolving in Genome’s Junkyard. November 16.)
Keywords
molecular evolution, evolutionary genetics, evolutionary novelties, sexual selection, adaptation, bioinformatics, new gene functions
Education
  • Sichuan Agricultural University , Sichuan, B.A. and M.S. Crop Plants and Genetics 01/2015
  • University of California at Davis, California, M.S. and Ph.D. Genetics and Evolution 12/1992
  • Harvard University, Cambridge Massachusetts, Postdoctoral Fellow Gene evolution and molecular biology 10/1997
Biosciences Graduate Program Association
Awards & Honors
  • 1993 - Allen Marr Prize The University of California at Davis
  • 1999 - David & Lucile Packard Fellow for Science & Engineering Davis & Lucile Packard Foundation
  • 2003 - CAREER Award National Science Foundation
  • 2011 - Inaugural Edna K Papazian Distinguished Service Professor The University of Chicago
  • 2014 - AAAS Fellow the American Association for the Advancement of Science
  • 2019 - 15 Studies That Challenged Medical Dogma in 2019 Medscape
  • 2020 - Distinguished Investigator Award, Senior Award The University of Chicago, Division of Biological Sciences
  • 2022 - John Simon Guggenheim Memorial Fellowship for Biology John Simon Guggenheim Memorial Foundation
  • 2022 - Ray Wu Award Ray Wu Society / Chinese Biological Investigator Society, Ithaca
Publications

  1. Evolution and maintenance of phenotypic plasticity. Biosystems. 2022 Dec; 222:104791. View in: PubMed

  2. Evolutionary New Genes in a Growing Paradigm. Genes (Basel). 2022 09 08; 13(9). View in: PubMed

  3. Retrogene Duplication and Expression Patterns Shaped by the Evolution of Sex Chromosomes in Malaria Mosquitoes. Genes (Basel). 2022 05 28; 13(6). View in: PubMed

  4. Gene fusion as an important mechanism to generate new genes in the genus Oryza. Genome Biol. 2022 06 15; 23(1):130. View in: PubMed

  5. Rapid Cis-Trans Coevolution Driven by a Novel Gene Retroposed from a Eukaryotic Conserved CCR4-NOT Component in Drosophila. Genes (Basel). 2021 12 26; 13(1). View in: PubMed

  6. Species-specific partial gene duplication in Arabidopsis thaliana evolved novel phenotypic effects on morphological traits under strong positive selection. Plant Cell. 2022 02 03; 34(2):802-817. View in: PubMed

  7. Rapid Gene Evolution in an Ancient Post-transcriptional and Translational Regulatory System Compensates for Meiotic X Chromosomal Inactivation. Mol Biol Evol. 2022 01 07; 39(1). View in: PubMed

  8. New Genes Interacted With Recent Whole-Genome Duplicates in the Fast Stem Growth of Bamboos. Mol Biol Evol. 2021 12 09; 38(12):5752-5768. View in: PubMed

  9. Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development. PLoS Genet. 2021 07; 17(7):e1009654. View in: PubMed

  10. A zebrafish-specific chimeric gene evolved essential developmental functions: discussion of conceptual significance. Sci China Life Sci. 2021 May; 64(5):840-842. View in: PubMed

  11. Evolutionary Dynamics of Abundant 7-bp Satellites in the Genome of Drosophila virilis. Mol Biol Evol. 2020 05 01; 37(5):1362-1375. View in: PubMed

  12. Rapid Evolution of Gained Essential Developmental Functions of a Young Gene via Interactions with Other Essential Genes. Mol Biol Evol. 2019 10 01; 36(10):2212-2226. View in: PubMed

  13. Evolution of genes and genomes: an emerging paradigm in life science. Sci China Life Sci. 2019 04; 62(4):435-436. View in: PubMed

  14. Origination and evolution of orphan genes and de novo genes in the genome of Caenorhabditis elegans. Sci China Life Sci. 2019 Apr; 62(4):579-593. View in: PubMed

  15. Topological evolution of coexpression networks by new gene integration maintains the hierarchical and modular structures in human ancestors. Sci China Life Sci. 2019 Apr; 62(4):594-608. View in: PubMed

  16. GenTree, an integrated resource for analyzing the evolution and function of primate-specific coding genes. Genome Res. 2019 04; 29(4):682-696. View in: PubMed

  17. Rapid evolution of protein diversity by de novo origination in Oryza. Nat Ecol Evol. 2019 04; 3(4):679-690. View in: PubMed

  18. Publisher Correction: Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet. 2018 11; 50(11):1618. View in: PubMed

  19. Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions. Nat Ecol Evol. 2018 04; 2(4):705-712. View in: PubMed

  20. Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet. 2018 02; 50(2):285-296. View in: PubMed

  21. Meiotic Sex Chromosome Inactivation: Compensation by Gene Traffic. Curr Biol. 2017 07 10; 27(13):R659-R661. View in: PubMed

  22. Genetic Architecture of Natural Variation Underlying Adult Foraging Behavior That Is Essential for Survival of Drosophila melanogaster. Genome Biol Evol. 2017 05 01; 9(5):1357-1369. View in: PubMed

  23. Expressed Structurally Stable Inverted Duplicates in Mammalian Genomes as Functional Noncoding Elements. Genome Biol Evol. 2017 Apr 01; 9(4):981-992. View in: PubMed

  24. LTR-mediated retroposition as a mechanism of RNA-based duplication in metazoans. Genome Res. 2016 12; 26(12):1663-1675. View in: PubMed

  25. New genes drive the evolution of gene interaction networks in the human and mouse genomes. Genome Biol. 2015 Oct 01; 16:202. View in: PubMed

  26. New genes contribute to genetic and phenotypic novelties in human evolution. Curr Opin Genet Dev. 2014 Dec; 29:90-6. View in: PubMed

  27. The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nat Genet. 2014 Sep; 46(9):982-8. View in: PubMed

  28. New genes important for development. EMBO Rep. 2014 May; 15(5):460-1. View in: PubMed

  29. Evolution of gene structural complexity: an alternative-splicing-based model accounts for intron-containing retrogenes. Plant Physiol. 2014 May; 165(1):412-23. View in: PubMed

  30. A long-term demasculinization of X-linked intergenic noncoding RNAs in Drosophila melanogaster. Genome Res. 2014 04; 24(4):629-38. View in: PubMed

  31. New gene evolution: little did we know. Annu Rev Genet. 2013; 47:307-33. View in: PubMed

  32. New genes as drivers of phenotypic evolution. Nat Rev Genet. 2013 Sep; 14(9):645-60. View in: PubMed

  33. High occurrence of functional new chimeric genes in survey of rice chromosome 3 short arm genome sequences. Genome Biol Evol. 2013; 5(5):1038-48. View in: PubMed

  34. gKaKs: the pipeline for genome-level Ka/Ks calculation. Bioinformatics. 2013 Mar 01; 29(5):645-6. View in: PubMed

  35. Why rodent pseudogenes refuse to retire. Genome Biol. 2012 Nov 20; 13(11):178. View in: PubMed

  36. Adaptive evolution and the birth of CTCF binding sites in the Drosophila genome. PLoS Biol. 2012; 10(11):e1001420. View in: PubMed

  37. New genes expressed in human brains: implications for annotating evolving genomes. Bioessays. 2012 Nov; 34(11):982-91. View in: PubMed

  38. Segmental dataset and whole body expression data do not support the hypothesis that non-random movement is an intrinsic property of Drosophila retrogenes. BMC Evol Biol. 2012 Sep 05; 12:169. View in: PubMed

  39. Frequent recent origination of brain genes shaped the evolution of foraging behavior in Drosophila. Cell Rep. 2012 Feb 23; 1(2):118-32. View in: PubMed

  40. Re-analysis of the larval testis data on meiotic sex chromosome inactivation revealed evidence for tissue-specific gene expression related to the drosophila X chromosome. BMC Biol. 2012 Jun 12; 10:49; author reply 50. View in: PubMed

  41. Reshaping of global gene expression networks and sex-biased gene expression by integration of a young gene. EMBO J. 2012 Jun 13; 31(12):2798-809. View in: PubMed

  42. Retrogenes moved out of the z chromosome in the silkworm. J Mol Evol. 2012 Apr; 74(3-4):113-26. View in: PubMed

  43. The origin and evolution of new genes. Methods Mol Biol. 2012; 856:161-86. View in: PubMed

  44. Drosophila duplication hotspots are associated with late-replicating regions of the genome. PLoS Genet. 2011 Nov; 7(11):e1002340. View in: PubMed

  45. Accelerated recruitment of new brain development genes into the human genome. PLoS Biol. 2011 Oct; 9(10):e1001179. View in: PubMed

  46. Roles of young serine-endopeptidase genes in survival and reproduction revealed rapid evolution of phenotypic effects at adult stages. Fly (Austin). 2011 Oct-Dec; 5(4):345-51. View in: PubMed

  47. Evolutionary patterns of RNA-based duplication in non-mammalian chordates. PLoS One. 2011; 6(7):e21466. View in: PubMed

  48. A cautionary note for retrocopy identification: DNA-based duplication of intron-containing genes significantly contributes to the origination of single exon genes. Bioinformatics. 2011 Jul 01; 27(13):1749-53. View in: PubMed

  49. Deficiency of X-linked inverted duplicates with male-biased expression and the underlying evolutionary mechanisms in the Drosophila genome. Mol Biol Evol. 2011 Oct; 28(10):2823-32. View in: PubMed

  50. Highly tissue specific expression of Sphinx supports its male courtship related role in Drosophila melanogaster. PLoS One. 2011 Apr 26; 6(4):e18853. View in: PubMed

  51. Dynamic programming procedure for searching optimal models to estimate substitution rates based on the maximum-likelihood method. Proc Natl Acad Sci U S A. 2011 May 10; 108(19):7860-5. View in: PubMed

  52. New genes in Drosophila quickly become essential. Science. 2010 Dec 17; 330(6011):1682-5. View in: PubMed

  53. The rapid generation of chimerical genes expanding protein diversity in zebrafish. BMC Genomics. 2010 Nov 24; 11:657. View in: PubMed

  54. Chromosomal redistribution of male-biased genes in mammalian evolution with two bursts of gene gain on the X chromosome. PLoS Biol. 2010 Oct 05; 8(10). View in: PubMed

  55. Evolution of enzymatic activities of testis-specific short-chain dehydrogenase/reductase in Drosophila. J Mol Evol. 2010 Oct; 71(4):241-9. View in: PubMed

  56. Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Res. 2010 Nov; 20(11):1526-33. View in: PubMed

  57. Direct evidence for postmeiotic transcription during Drosophila melanogaster spermatogenesis. Genetics. 2010 Sep; 186(1):431-3. View in: PubMed

  58. Mutational bias shaping fly copy number variation: implications for genome evolution. Trends Genet. 2010 Jun; 26(6):243-7. View in: PubMed

  59. Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell. 2010 Apr 01; 21(7):1200-13. View in: PubMed

  60. Recombination yet inefficient selection along the Drosophila melanogaster subgroup's fourth chromosome. Mol Biol Evol. 2010 Apr; 27(4):848-61. View in: PubMed

  61. Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet. 2009 Nov; 5(11):e1000731. View in: PubMed

  62. Positive selection for the male functionality of a co-retroposed gene in the hominoids. BMC Evol Biol. 2009 Oct 15; 9:252. View in: PubMed

  63. The subtelomere of Oryza sativa chromosome 3 short arm as a hot bed of new gene origination in rice. Mol Plant. 2008 Sep; 1(5):839-50. View in: PubMed

  64. Extensive structural renovation of retrogenes in the evolution of the Populus genome. Plant Physiol. 2009 Dec; 151(4):1943-51. View in: PubMed

  65. Detection of intergenic non-coding RNAs expressed in the main developmental stages in Drosophila melanogaster. Nucleic Acids Res. 2009 Jul; 37(13):4308-14. View in: PubMed

  66. General gene movement off the X chromosome in the Drosophila genus. Genome Res. 2009 May; 19(5):897-903. View in: PubMed

  67. A rice gene of de novo origin negatively regulates pathogen-induced defense response. PLoS One. 2009; 4(2):e4603. View in: PubMed

  68. RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet. 2009 Jan; 10(1):19-31. View in: PubMed

  69. Origination of chimeric genes through DNA-level recombination. Genome Dyn. 2007; 3:131-146. View in: PubMed

  70. Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science. 2008 Jun 20; 320(5883):1629-31. View in: PubMed

  71. The evolution of courtship behaviors through the origination of a new gene in Drosophila. Proc Natl Acad Sci U S A. 2008 May 27; 105(21):7478-83. View in: PubMed

  72. Recurrent tandem gene duplication gave rise to functionally divergent genes in Drosophila. Mol Biol Evol. 2008 Jul; 25(7):1451-8. View in: PubMed

  73. Adaptive evolution of the insulin two-gene system in mouse. Genetics. 2008 Mar; 178(3):1683-91. View in: PubMed

  74. Repetitive element-mediated recombination as a mechanism for new gene origination in Drosophila. PLoS Genet. 2008 Jan; 4(1):e3. View in: PubMed

  75. An intronic signal for alternative splicing in the human genome. PLoS One. 2007 Nov 28; 2(11):e1246. View in: PubMed

  76. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 2007 Nov 08; 450(7167):203-18. View in: PubMed

  77. Origins of new male germ-line functions from X-derived autosomal retrogenes in the mouse. Mol Biol Evol. 2007 Oct; 24(10):2242-53. View in: PubMed

  78. Side effects of Tamiflu: clues from an Asian single nucleotide polymorphism. Cell Res. 2007 Apr; 17(4):309-10. View in: PubMed

  79. A new retroposed gene in Drosophila heterochromatin detected by microarray-based comparative genomic hybridization. J Mol Evol. 2007 Feb; 64(2):272-83. View in: PubMed

  80. Retrogene movement within- and between-chromosomes in the evolution of Drosophila genomes. Gene. 2006 Dec 30; 385:96-102. View in: PubMed

  81. High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell. 2006 Aug; 18(8):1791-802. View in: PubMed

  82. Origination of an X-linked testes chimeric gene by illegitimate recombination in Drosophila. PLoS Genet. 2006 May; 2(5):e77. View in: PubMed

  83. Translational effects of differential codon usage among intragenic domains of new genes in Drosophila. Biochim Biophys Acta. 2005 May 01; 1728(3):135-42. View in: PubMed

  84. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004 Dec 09; 432(7018):695-716. View in: PubMed

  85. Evolving protein functional diversity in new genes of Drosophila. Proc Natl Acad Sci U S A. 2004 Nov 16; 101(46):16246-50. View in: PubMed

  86. Excess of amino acid substitutions relative to polymorphism between X-linked duplications in Drosophila melanogaster. Mol Biol Evol. 2005 Feb; 22(2):273-84. View in: PubMed

  87. Sex chromosomes and male functions: where do new genes go? Cell Cycle. 2004 Jul; 3(7):873-5. View in: PubMed

  88. Nucleotide variation and recombination along the fourth chromosome in Drosophila simulans. Genetics. 2004 Apr; 166(4):1783-94. View in: PubMed

  89. Duplication-degeneration as a mechanism of gene fission and the origin of new genes in Drosophila species. Nat Genet. 2004 May; 36(5):523-7. View in: PubMed

  90. Extensive gene traffic on the mammalian X chromosome. Science. 2004 Jan 23; 303(5657):537-40. View in: PubMed

  91. The origin of new genes: glimpses from the young and old. Nat Rev Genet. 2003 Nov; 4(11):865-75. View in: PubMed

  92. Dntf-2r, a young Drosophila retroposed gene with specific male expression under positive Darwinian selection. Genetics. 2003 Jul; 164(3):977-88. View in: PubMed

  93. Origin of new genes: evidence from experimental and computational analyses. Genetica. 2003 Jul; 118(2-3):171-82. View in: PubMed

  94. Retroposed new genes out of the X in Drosophila. Genome Res. 2002 Dec; 12(12):1854-9. View in: PubMed

  95. Expansion of genome coding regions by acquisition of new genes. Genetica. 2002 May; 115(1):65-80. View in: PubMed

  96. Intron presence-absence polymorphism in Drosophila driven by positive Darwinian selection. Proc Natl Acad Sci U S A. 2002 Jun 11; 99(12):8121-6. View in: PubMed

  97. Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome. Mol Biol Evol. 2002 Jun; 19(6):918-25. View in: PubMed

  98. Evolution of the phosphoglycerate mutase processed gene in human and chimpanzee revealing the origin of a new primate gene. Mol Biol Evol. 2002 May; 19(5):654-63. View in: PubMed

  99. Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2002 Apr 02; 99(7):4448-53. View in: PubMed

  100. Nucleotide variation along the Drosophila melanogaster fourth chromosome. Science. 2002 Jan 04; 295(5552):134-7. View in: PubMed

  101. Evolution of novel genes. Curr Opin Genet Dev. 2001 Dec; 11(6):673-80. View in: PubMed

  102. Gene duplication and evolution. Science. 2001 Aug 31; 293(5535):1551. View in: PubMed

  103. Testing the "proto-splice sites" model of intron origin: evidence from analysis of intron phase correlations. Mol Biol Evol. 2000 Dec; 17(12):1789-96. View in: PubMed

  104. A new function evolved from gene fusion. Genome Res. 2000 Nov; 10(11):1655-7. View in: PubMed

  105. The origin of the Jingwei gene and the complex modular structure of its parental gene, yellow emperor, in Drosophila melanogaster. Mol Biol Evol. 2000 Sep; 17(9):1294-301. View in: PubMed

  106. Origin of new genes and source for N-terminal domain of the chimerical gene, jingwei, in Drosophila. Gene. 1999 Sep 30; 238(1):135-41. View in: PubMed

  107. Association of intron phases with conservation at splice site sequences and evolution of spliceosomal introns. Mol Biol Evol. 1999 Nov; 16(11):1528-34. View in: PubMed

  108. Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res. 1999 Aug 01; 27(15):3219-28. View in: PubMed

  109. Generation of a widespread Drosophila inversion by a transposable element. Science. 1999 Jul 16; 285(5426):415-8. View in: PubMed

  110. Toward a resolution of the introns early/late debate: only phase zero introns are correlated with the structure of ancient proteins. Proc Natl Acad Sci U S A. 1998 Apr 28; 95(9):5094-9. View in: PubMed

  111. Relationship between "proto-splice sites" and intron phases: evidence from dicodon analysis. Proc Natl Acad Sci U S A. 1998 Jan 06; 95(1):219-23. View in: PubMed

  112. The yeast splice site revisited: new exon consensus from genomic analysis. Cell. 1997 Dec 12; 91(6):739-40. View in: PubMed

  113. Origin of genes. Proc Natl Acad Sci U S A. 1997 Jul 22; 94(15):7698-703. View in: PubMed

  114. Introns and gene evolution. Genes Cells. 1996 Jun; 1(6):493-505. View in: PubMed

  115. Exon shuffling and the origin of the mitochondrial targeting function in plant cytochrome c1 precursor. Proc Natl Acad Sci U S A. 1996 Jul 23; 93(15):7727-31. View in: PubMed

  116. Evolution of the intron-exon structure of eukaryotic genes. Curr Opin Genet Dev. 1995 Dec; 5(6):774-8. View in: PubMed

  117. Intron phase correlations and the evolution of the intron/exon structure of genes. Proc Natl Acad Sci U S A. 1995 Dec 19; 92(26):12495-9. View in: PubMed

  118. Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science. 1993 Apr 02; 260(5104):91-5. View in: PubMed

  119. Codon usage divergence of homologous vertebrate genes and codon usage clock. J Mol Evol. 1991 Jan; 32(1):6-15. View in: PubMed
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