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 D. 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.

中文翻译：

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了解串联果蝇特定基因家族的早期进化阶段：结构和功能人口研究。

基因家族是遗传创新和表型多样化的基础。然而，我们对串联排列的基因家族的早期基因组和功能进化的理解仍然不完整，因为旁系同源序列相似性阻碍了它们的准确表征。D. melanogaster特异的基因家族Sdic串联重复并影响精子竞争。我们使用参考质量基因组组装，深度读取方法和qPCR对20个地理上不同的种群中的Sdic进行了检查，发现约90％的个体具有3-7个拷贝以及种群分化的证据。在具有可靠基因注释的菌株中，每个菌株的拷贝数变异（CNV）和差异转座元件插入可区分Sdic区域的一种结构不同的版本。所有31个带注释的副本均具有蛋白质编码潜能，并且根据编码的蛋白质变异体，将其3'末端不同的13个亚型分类为3-5种共存的亚型。尽管广泛地进行了基因转换，但是在阳性选择下，所有菌株中存在的唯一拷贝在编码和调节水平上均在功能上有所不同。与导致雄性表达增加的Sdic区域的人工串联重复相反，世界性菌株中的CNV与表达水平不相关，这可能是由于基因组修饰子组成不同所致。复制该区域并不能提高精子的竞争能力，这表明高表达水平的健身成本或高原效应。除了促进最低限度的最佳表达水平外，