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 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 increasedmale 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 tandemmultigene families can follow toward long-term consolidation in eukaryotic genomes.

Understanding the early evolutionary stages of a tandem drosophila melanogaster-specific gene family: A structural and functional population study / Clifton, B. D.; Jimenez, J.; Kimura, A.; Chahine, Z.; Librado, P.; Sanchez-Gracia, A.; Abbassi, M.; Carranza, F.; Chan, C.; Marchetti, M.; Zhang, W.; Shi, M.; Vu, C.; Yeh, S.; Fanti, L.; Xia, X. -Q.; Rozas, J.; Ranz, J. M.. - In: MOLECULAR BIOLOGY AND EVOLUTION. - ISSN 0737-4038. - 37:9(2020), pp. 2584-2600. [10.1093/molbev/msaa109]

Understanding the early evolutionary stages of a tandem drosophila melanogaster-specific gene family: A structural and functional population study

Marchetti M.
Membro del Collaboration Group
;
Fanti L.
Membro del Collaboration Group
;
2020

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 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 increasedmale 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 tandemmultigene families can follow toward long-term consolidation in eukaryotic genomes.
2020
CNV; Complex genomic regions; Expression variation; Gene conversion; Sexual selection; Tandem multigene families
01 Pubblicazione su rivista::01a Articolo in rivista
Understanding the early evolutionary stages of a tandem drosophila melanogaster-specific gene family: A structural and functional population study / Clifton, B. D.; Jimenez, J.; Kimura, A.; Chahine, Z.; Librado, P.; Sanchez-Gracia, A.; Abbassi, M.; Carranza, F.; Chan, C.; Marchetti, M.; Zhang, W.; Shi, M.; Vu, C.; Yeh, S.; Fanti, L.; Xia, X. -Q.; Rozas, J.; Ranz, J. M.. - In: MOLECULAR BIOLOGY AND EVOLUTION. - ISSN 0737-4038. - 37:9(2020), pp. 2584-2600. [10.1093/molbev/msaa109]
File allegati a questo prodotto
File Dimensione Formato  
Clifton_Understanding_2020.pdf

accesso aperto

Tipologia: Versione editoriale (versione pubblicata con il layout dell'editore)
Licenza: Creative commons
Dimensione 833.25 kB
Formato Adobe PDF
833.25 kB Adobe PDF
Clifton_Understanding_2020_supplementarydata.pdf

accesso aperto

Tipologia: Versione editoriale (versione pubblicata con il layout dell'editore)
Licenza: Tutti i diritti riservati (All rights reserved)
Dimensione 1.43 MB
Formato Adobe PDF
1.43 MB Adobe PDF

I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.

Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/11573/1471095
Citazioni
  • ???jsp.display-item.citation.pmc??? 3
  • Scopus 11
  • ???jsp.display-item.citation.isi??? 8
social impact