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Understanding the Early Evolutionary Stages of a Tandem Drosophila melanogaster-Specific Gene Family: A Structural and Functional Population Study
Clifton, Bryan D.1; Jimenez, Jamie1; Kimura, Ashlyn1; Chahine, Zeinab1; Librado, Pablo2; Sanchez-Gracia, Alejandro3,4; Abbassi, Mashya1; Carranza, Francisco1; Chan, Carolus1; Marchetti, Marcella5,6; Zhang, Wanting7; Shi, Mijuan7; Vu, Christine1; Yeh, Shudan1,8; Fanti, Laura5,6; Xia, Xiao-Qin7; Rozas, Julio3,4; Ranz, Jose M.1
Corresponding AuthorRanz, Jose M.(jranz@uci.edu)
2020-09-01
Source PublicationMOLECULAR BIOLOGY AND EVOLUTION
ISSN0737-4038
Volume37Issue:9Pages:2584-2600
AbstractGene families underlie genetic innovation and phenotypic diversification. However, our understanding of the early genomic and functional evolution of tandemly arranged gene families remains incomplete as paralog sequence similarity hinders their accurate characterization. The Drosophila melanogaster-specific gene family Sdic is tandemly repeated and impacts sperm competition. We scrutinized Sdic in 20 geographically diverse populations using reference-quality genome assemblies, read-depth methodologies, and qPCR, finding that similar to 90% of the individuals harbor 3-7 copies as well as evidence of population differentiation. In strains with reliable gene annotations, copy number variation (CNV) and differential transposable element insertions distinguish one structurally distinct version of the Sdic region per strain. All 31 annotated copies featured protein-coding potential and, based on the protein variant encoded, were categorized into 13 paratypes differing in their 30 ends, with 3-5 paratypes coexisting in any strain examined. Despite widespread gene conversion, the only copy present in all strains has functionally diverged at both coding and regulatory levels under positive selection. Contrary to artificial tandem duplications of the Sdic region that resulted in increased male expression, CNV in cosmopolitan strains did not correlate with expression levels, likely as a result of differential genome modifier composition. Duplicating the region did not enhance sperm competitiveness, suggesting a fitness cost at high expression levels or a plateau effect. Beyond facilitating a minimally optimal expression level, Sdic CNV acts as a catalyst of protein and regulatory diversity, showcasing a possible evolutionary path recently formed tandem multigene families can follow toward long-term consolidation in eukaryotic genomes.
Keywordcomplex genomic regions tandem multigene families CNV expression variation gene conversion sexual selection
DOI10.1093/molbev/msaa109
Funding OrganizationNational Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds
Indexed BySCI ; SCI
Language英语
Funding ProjectNational Science Foundation[MCB-1157876] ; University of California, Irvine intramural funds
WOS Research AreaBiochemistry & Molecular Biology ; Evolutionary Biology ; Genetics & Heredity
WOS SubjectBiochemistry & Molecular Biology ; Evolutionary Biology ; Genetics & Heredity
WOS IDWOS:000574386500010
WOS KeywordCOPY NUMBER VARIATION ; SPERM-SPECIFIC GENE ; NATURAL-POPULATIONS ; POSITIVE SELECTION ; CYTOPLASMIC DYNEIN ; INTERMEDIATE CHAIN ; MULTIGENE FAMILY ; DIVERGENCE ; DIVERSITY ; REGIONS
PublisherOXFORD UNIV PRESS
Funding OrganizationNational Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; National Science Foundation ; National Science Foundation ; National Science Foundation ; National Science Foundation ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds ; University of California, Irvine intramural funds
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Document Type期刊论文
Identifierhttp://ir.ihb.ac.cn/handle/342005/38944
Collection水生生物分子与细胞生物学研究中心_期刊论文
Corresponding AuthorRanz, Jose M.
Affiliation1.Univ Calif Irvine, Dept Ecol & Evolutionary Biol, Irvine, CA 92717 USA
2.Univ Paul Sabatier, Fac Med Purpan, Lab AMIS, CNRS,UMR 5288, Toulouse, France
3.Univ Barcelona, Dept Genet Microbiol & Estadist, Barcelona, Spain
4.Univ Barcelona, Inst Recerca Biodiversitat, Barcelona, Spain
5.Fdn Cenci Bolognetti, Ist Pasteur Italia, Rome, Italy
6.Sapienza Univ Rome, Dept Biol & Biotechnol C Darwin, Rome, Italy
7.Chinese Acad Sci, Inst Hydrobiol, Wuhan, Hubei, Peoples R China
8.Natl Cent Univ, Dept Life Sci, Taoyuan, Zhongli Distric, Taiwan
Recommended Citation
GB/T 7714
Clifton, Bryan D.,Jimenez, Jamie,Kimura, Ashlyn,et al. Understanding the Early Evolutionary Stages of a Tandem Drosophila melanogaster-Specific Gene Family: A Structural and Functional Population Study[J]. MOLECULAR BIOLOGY AND EVOLUTION,2020,37(9):2584-2600.
APA Clifton, Bryan D..,Jimenez, Jamie.,Kimura, Ashlyn.,Chahine, Zeinab.,Librado, Pablo.,...&Ranz, Jose M..(2020).Understanding the Early Evolutionary Stages of a Tandem Drosophila melanogaster-Specific Gene Family: A Structural and Functional Population Study.MOLECULAR BIOLOGY AND EVOLUTION,37(9),2584-2600.
MLA Clifton, Bryan D.,et al."Understanding the Early Evolutionary Stages of a Tandem Drosophila melanogaster-Specific Gene Family: A Structural and Functional Population Study".MOLECULAR BIOLOGY AND EVOLUTION 37.9(2020):2584-2600.
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