Rapid functional and sequence differentiation of a tandemly repeated species-specific multigene family in Drosophila

TY - JOUR

T1 - Rapid functional and sequence differentiation of a tandemly repeated species-specific multigene family in Drosophila

AU - Clifton, Bryan D.

AU - Sanz, Pablo Librado

AU - Yeh, Shu-Dan

AU - Solares, Edwin S.

AU - Real, Daphne A.

AU - Jayasekera, Suvini U.

AU - Zhang, Wanting

AU - Shi, Mijuan

AU - Park, Ronni V.

AU - Magie, Robert D.

AU - Ma, Hsiu Ching

AU - Xia, Xiao Qin

AU - Marco, Antonio

AU - Rozas, Julio

AU - Ranz, José M.

PY - 2017/1/1

Y1 - 2017/1/1

N2 - Gene clusters of recently duplicated genes are hotbeds for evolutionary change. However, our understanding of how mutational mechanisms and evolutionary forces shape the structural and functional evolution of these clusters is hindered by the high sequence identity among the copies, which typically results in their inaccurate representation in genome assemblies. The presumed testis-specific, chimeric gene Sdic originated, and tandemly expanded in Drosophila melanogaster, contributing to increased male-male competition. Using various types of massively parallel sequencing data, we studied the organization, sequence evolution, and functional attributes of the different Sdic copies. By leveraging long-read sequencing data, we uncovered both copy number and order differences from the currently accepted annotation for the Sdic region. Despite evidence for pervasive gene conversion affecting the Sdic copies, we also detected signatures of two episodes of diversifying selection, which have contributed to the evolution of a variety of C-termini and miRNA binding site compositions. Expression analyses involving RNA-seq datasets from 59 different biological conditions revealed distinctive expression breadths among the copies, with three copies being transcribed in females, opening the possibility to a sexually antagonistic effect. Phenotypic assays using Sdic knock-out strains indicated that should this antagonistic effect exist, it does not compromise female fertility. Our results strongly suggest that the genome consolidation of the Sdic gene cluster is more the result of a quick exploration of different paths of molecular tinkering by different copies than a mere dosage increase, which could be a recurrent evolutionary outcome in the presence of persistent sexual selection.

AB - Gene clusters of recently duplicated genes are hotbeds for evolutionary change. However, our understanding of how mutational mechanisms and evolutionary forces shape the structural and functional evolution of these clusters is hindered by the high sequence identity among the copies, which typically results in their inaccurate representation in genome assemblies. The presumed testis-specific, chimeric gene Sdic originated, and tandemly expanded in Drosophila melanogaster, contributing to increased male-male competition. Using various types of massively parallel sequencing data, we studied the organization, sequence evolution, and functional attributes of the different Sdic copies. By leveraging long-read sequencing data, we uncovered both copy number and order differences from the currently accepted annotation for the Sdic region. Despite evidence for pervasive gene conversion affecting the Sdic copies, we also detected signatures of two episodes of diversifying selection, which have contributed to the evolution of a variety of C-termini and miRNA binding site compositions. Expression analyses involving RNA-seq datasets from 59 different biological conditions revealed distinctive expression breadths among the copies, with three copies being transcribed in females, opening the possibility to a sexually antagonistic effect. Phenotypic assays using Sdic knock-out strains indicated that should this antagonistic effect exist, it does not compromise female fertility. Our results strongly suggest that the genome consolidation of the Sdic gene cluster is more the result of a quick exploration of different paths of molecular tinkering by different copies than a mere dosage increase, which could be a recurrent evolutionary outcome in the presence of persistent sexual selection.

KW - Drosophila

KW - Functional diversification

KW - Gene amplification

KW - Newly evolved gene

KW - Sdic

U2 - 10.1093/molbev/msw212

DO - 10.1093/molbev/msw212

M3 - Journal article

C2 - 27702774

AN - SCOPUS:85014900175

SN - 0737-4038

VL - 34

SP - 51

EP - 65

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

IS - 1

ER -