Our understanding of animal ornaments and the mating preferences driving their exaggeration is limited by knowledge of their genetics. Post-copulatory sexual selection is credited with the rapid evolution of female sperm-storage organ morphology and corresponding sperm quality traits across diverse taxa. In Drosophila, the mechanisms by which longer flagella convey an advantage in the competition among sperm for limited storage space in the female, and by which female sperm-storage organ morphology biases fertilization in favour of longer sperm have been resolved. However, the evolutionary genetics underlying this model post-copulatory ornament and preference system have remained elusive. Here we combined comparative analyses of 149 Drosophila species, a genome-wide association study in Drosophila melanogaster and molecular evolutionary analysis of ~9,400 genes to elucidate how sperm and female sperm-storage organ length co-evolved into one of nature’s most extreme ornaments and preferences. Our results reveal a diverse repertoire of pleiotropic genes linking sperm length and seminal receptacle length expression to central nervous system development and sensory biology. Sperm length development appears condition-dependent and is governed by conserved hormonal (insulin/insulin-like growth factor) and developmental (including Notch and Fruitless) pathways. Central developmental pathway genes, including Notch, also comprised the majority of a restricted set of genes contributing to both intraspecific and interspecific variation in sperm length. Our findings support ‘good genes’ models of female preference evolution.

我们对动物装饰品的理解和导致它们夸大其词的交配偏好受到其遗传学知识的限制。交配后性选择被认为是雌性精子储存器官形态的快速进化和不同分类群中相应的精子质量特征的原因。在果蝇中，较长的鞭毛在精子之间争夺雌性有限储存空间的机制中传递优势，以及雌性精子储存器官形态偏向于受精而有利于较长精子的机制已经得到解决。然而，该模型交配后装饰和偏好系统背后的进化遗传学仍然难以捉摸。在这里，我们结合了对 149 种果蝇物种的比较分析、对果蝇黑腹果蝇的全基因组关联研究和对 ~9,400 个基因的分子进化分析，以阐明精子和女性精子储存器官长度如何共同进化成自然界最极端的装饰品和偏好之一。我们的结果揭示了多种多效性基因库，这些基因将精子长度和容器长度表达与中枢神经系统发育和感觉生物学联系起来。精子长度发育似乎与条件有关，并受保守激素（胰岛素/胰岛素样生长因子）和发育（包括 Notch 和 Fruitless）途径控制。包括 Notch 在内的中央发育途径基因也包含导致精子长度种内和种间变异的受限基因集的大部分。我们的研究结果支持女性偏好进化的“好基因”模型。