Understanding the Early Evolutionary Stages of a Tandem Drosophilamelanogaster-Specific Gene Family: A Structural and Functional Population Study.


Journal

Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455

Informations de publication

Date de publication:
01 09 2020
Historique:
pubmed: 3 5 2020
medline: 17 4 2021
entrez: 3 5 2020
Statut: ppublish

Résumé

Gene 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 ∼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 3' 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.

Identifiants

pubmed: 32359138
pii: 5828227
doi: 10.1093/molbev/msaa109
pmc: PMC7475035
doi:

Substances chimiques

Drosophila Proteins 0
Sdic protein, Drosophila EC 3.6.1.-
Axonemal Dyneins EC 3.6.4.2

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

2584-2600

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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Auteurs

Bryan D Clifton (BD)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

Jamie Jimenez (J)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

Ashlyn Kimura (A)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

Zeinab Chahine (Z)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

Pablo Librado (P)

Laboratoire AMIS CNRS UMR 5288, Faculté de Médicine de Purpan, Université Paul Sabatier, Toulouse, France.

Alejandro Sánchez-Gracia (A)

Departament de Genètica, Microbiologia i Estadistica, Universitat de Barcelona, Barcelona, Spain.
Institut de Recerca de la Biodiversitat, Universitat de Barcelona, Barcelona, Spain.

Mashya Abbassi (M)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

Francisco Carranza (F)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

Carolus Chan (C)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

Marcella Marchetti (M)

Istituto Pasteur Italia, Fondazione Cenci-Bolognetti, Rome, Italy.
Department of Biology and Biotechnology "C. Darwin", Sapienza University of Rome, Rome, Italy.

Wanting Zhang (W)

Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, China.

Mijuan Shi (M)

Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, China.

Christine Vu (C)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

Shudan Yeh (S)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.
Department of Life Sciences, National Central University, Taoyuan City, Zhongli District, Taiwan.

Laura Fanti (L)

Istituto Pasteur Italia, Fondazione Cenci-Bolognetti, Rome, Italy.
Department of Biology and Biotechnology "C. Darwin", Sapienza University of Rome, Rome, Italy.

Xiao-Qin Xia (XQ)

Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, China.

Julio Rozas (J)

Departament de Genètica, Microbiologia i Estadistica, Universitat de Barcelona, Barcelona, Spain.
Institut de Recerca de la Biodiversitat, Universitat de Barcelona, Barcelona, Spain.

José M Ranz (JM)

Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA.

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Classifications MeSH