title: Rapid Functional and Sequence Differentiation of a Tandemly Repeated Species-Specific Multigene Family in Drosophila.
abstract: 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.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.
authors.forename: Bryan D
authors.initials: BD
authors.lastname: Clifton
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
authors.forename: Pablo
authors.initials: P
authors.lastname: Librado
authors.affiliation: Department of Life Sciences, National Central University, Taoyuan City, Zhongli District, Taiwan.
authors.forename: Shu-Dan
authors.initials: SD
authors.lastname: Yeh
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.
authors.forename: Edwin S
authors.initials: ES
authors.lastname: Solares
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.
authors.forename: Daphne A
authors.initials: DA
authors.lastname: Real
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.
authors.forename: Suvini U
authors.initials: SU
authors.lastname: Jayasekera
authors.affiliation: Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, China.
authors.forename: Wanting
authors.initials: W
authors.lastname: Zhang
authors.affiliation: Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, China.
authors.forename: Mijuan
authors.initials: M
authors.lastname: Shi
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.
authors.forename: Ronni V
authors.initials: RV
authors.lastname: Park
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.
authors.forename: Robert D
authors.initials: RD
authors.lastname: Magie
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.
authors.forename: Hsiu-Ching
authors.initials: HC
authors.lastname: Ma
authors.affiliation: Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, China.
authors.forename: Xiao-Qin
authors.initials: XQ
authors.lastname: Xia
authors.affiliation: School of Biological Sciences, University of Essex, Colchester, United Kingdom.
authors.forename: Antonio
authors.initials: A
authors.lastname: Marco
authors.affiliation: Departament de Genètica, Microbiologia i Estadistica, and Institut de Recerca de la Biodiversitat, Universitat de Barcelona, Barcelona, Spain.
authors.forename: Julio
authors.initials: J
authors.lastname: Rozas
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA jranz@uci.edu.
authors.forename: José M
authors.initials: JM
authors.lastname: Ranz
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D056444:Axonemal Dyneins / Q000235:genetics; D005075:Biological Evolution; D029721:Drosophila Proteins / Q000235:genetics; D004331:Drosophila melanogaster / Q000235:genetics*; D019143:Evolution, Molecular; D005260:Female; D005785:Gene Conversion; D020440:Gene Duplication; D017344:Genes, Insect; D014644:Genetic Variation; D008297:Male; D005810:Multigene Family; D010802:Phylogeny; D017422:Sequence Analysis, DNA / Q000379:methods; D013045:Species Specificity; D020080:Tandem Repeat Sequences
chemical_list: D029721:Drosophila Proteins; C116304:Sdic protein, Drosophila; D056444:Axonemal Dyneins
keywords: Drosophila; Sdic; functional diversification; gene amplification; newly evolved gene