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Title: Understanding the Early Evolutionary Stages of a Tandem Drosophilamelanogaster-Specific Gene Family: A Structural and Functional Population Study
Author: Clifton, Bryan D.
Jimenez, Jamie
Kimura, Ashlyn
Chahine, Zeinab
Librado, Pablo
Sánchez-Gracia, Alejandro
Abbassi, Mashya
Carranza, Francisco
Chan, Carolus
Marchetti, Marcella
Zhang, Wanting
Shi, Mijuan
Vu, Christine
Yeh, Shudan
Fanti, Laura
Xia, Xiao Qin
Rozas Liras, Julio A.
Ranz, José M.
Keywords: Genòmica
Issue Date: 1-Sep-2020
Publisher: Oxford University Press
Abstract: 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.
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It is part of: Molecular Biology and Evolution, 2020, vol. 37, num. 9, p. 2584-2600
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ISSN: 0737-4038
Appears in Collections:Articles publicats en revistes (Institut de Recerca de la Biodiversitat (IRBio))
Articles publicats en revistes (Genètica, Microbiologia i Estadística)

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