Center for Neural Development and Disease, Department of Biomedical Genetics, and Department of Biology, University of Rochester, School of Medicine and Dentistry, Rochester, New York 14642.
J Neurosci. 2014 Jan 29;34(5):1579-91. doi: 10.1523/JNEUROSCI.4352-13.2014.
Sex differences in shared behaviors (for example, locomotion and feeding) are a nearly universal feature of animal biology. Though these behaviors may share underlying neural programs, their kinematics can exhibit robust differences between males and females. The neural underpinnings of these differences are poorly understood because of the often-untested assumption that they are determined by sex-specific body morphology. Here, we address this issue in the nematode Caenorhabditis elegans, which features two sexes with distinct body morphologies but similar locomotor circuitry and body muscle. Quantitative behavioral analysis shows that C. elegans and related nematodes exhibit significant sex differences in the dynamics and geometry of locomotor body waves, such that the male is generally faster. Using a recently proposed model of locomotor wave propagation, we show that sex differences in both body mechanics and the intrinsic dynamics of the motor system can contribute to kinematic differences in distinct mechanical contexts. By genetically sex-reversing the properties of specific tissues and cells, however, we find that sex-specific locomotor frequency in C. elegans is determined primarily by the functional modification of shared sensory neurons. Further, we find that sexual modification of body wall muscle together with the nervous system is required to alter body wave speed. Thus, rather than relying on a single focus of modification, sex differences in motor dynamics require independent modifications to multiple tissue types. Our results suggest shared motor behaviors may be sex-specifically optimized though distributed modifications to several aspects of morphology and physiology.
动物生物学中几乎普遍存在共享行为（例如，运动和摄食）的性别差异。尽管这些行为可能具有潜在的神经程序，但它们的运动学在雄性和雌性之间可能存在明显差异。由于通常未经测试的假设，即它们由性别特异性的身体形态决定，这些差异的神经基础理解甚少。在这里，我们在具有不同身体形态但相似运动电路和身体肌肉的线虫秀丽隐杆线虫中解决了这个问题。定量行为分析表明，秀丽隐杆线虫和相关线虫在运动身体波的动力学和几何形状上表现出显著的性别差异，使得雄性通常更快。使用最近提出的运动波传播模型，我们表明，身体力学和运动系统的内在动力学中的性别差异都可以导致在不同机械环境中的运动学差异。然而，通过遗传上反转特定组织和细胞的性别特征，我们发现秀丽隐杆线虫中特定的性别运动频率主要取决于共享感觉神经元的功能修饰。此外，我们发现改变身体波速需要对体壁肌肉和神经系统进行性修饰。因此，运动动力学的性别差异不需要依赖单一的修饰焦点，而是需要对多个组织类型进行独立修饰。我们的结果表明，共享运动行为可能通过对形态和生理学的几个方面进行分布式修饰而具有性别特异性优化。
