Syed Zeeshan A, Gomez R Antonio, Borziak Kirill, Asif Amaar, Cong Abelard S, O'Grady Patrick M, Kim Bernard Y, Suvorov Anton, Petrov Dmitri A, Lüpold Stefan, Wengert Peter, McDonough-Goldstein Caitlin, Ahmed-Braimah Yasir H, Dorus Steve, Pitnick Scott
Center for Reproductive Evolution, Department of Biology, Syracuse University, Syracuse, NY, USA.
Department of Entomology, Cornell University, Ithaca, NY, USA.
Nat Ecol Evol. 2025 Feb;9(2):336-348. doi: 10.1038/s41559-024-02587-2. Epub 2024 Nov 22.
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.
我们对动物装饰以及驱动其夸张化的交配偏好的理解受到其遗传学知识的限制。交配后的性选择被认为是导致不同分类群中雌性精子储存器官形态以及相应精子质量性状快速进化的原因。在果蝇中，较长鞭毛在精子争夺雌性体内有限储存空间的竞争中传递优势的机制，以及雌性精子储存器官形态使受精偏向于较长精子的机制已经得到了解决。然而，这种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种果蝇的比较分析、黑腹果蝇的全基因组关联研究以及对约9400个基因的分子进化分析，以阐明精子和雌性精子储存器官长度是如何共同进化为自然界中最极端的装饰和偏好之一的。我们的结果揭示了一系列多效性基因，这些基因将精子长度和受精囊长度的表达与中枢神经系统发育和感觉生物学联系起来。精子长度的发育似乎依赖于条件，并受保守的激素（胰岛素/胰岛素样生长因子）和发育（包括Notch和无果基因）途径的控制。包括Notch在内的中枢发育途径基因，也构成了导致精子长度种内和种间变异的一组受限基因的大部分。我们的发现支持了雌性偏好进化的“优质基因”模型。
