The development and evolution of vertebrate electroreceptors

我们习惯于用五种感官来体验世界：视觉、嗅觉、味觉、触觉和听觉（它能探测到内耳特殊感觉“毛细胞”上微小“毛发”的机械位移）。然而，陆地脊椎动物（爬行动物、鸟类和哺乳动物，包括人类），以及青蛙和大多数现代硬骨鱼，已经失去了最古老的脊椎动物感官之一，即探测水中弱电场的能力。这种“电感受”的感觉用于寻找猎物和确定方向。陆地脊椎动物（不包括青蛙和鱼）也失去了感知水运动的感觉毛细胞的“侧线系统”（就像我们内耳的机械感觉毛细胞一样）；它们在头部和身体上呈直线分布（因此得名“侧线”），用于成群结队的行为，寻找猎物和探测捕食者。这项拨款提案中的实验旨在了解电感受器的胚胎发育和进化过程，这种改良的感觉毛细胞赋予水生脊椎动物这种迷人的“第六感”，以及它们与侧线系统的关系。虽然电感受器在进化上非常古老，但直到20世纪50年代才被发现，我们对它们的发展知之甚少。它们存在于所有主要的水生脊椎动物群体中，包括七鳃鳗（最原始的活脊椎动物）、软骨鱼（鲨鱼和鳐鱼）、原始硬骨鱼（鲟鱼、白鲟）、肺鱼（与陆地脊椎动物的祖先有关），甚至一些两栖动物（蝾螈）。尽管现代硬骨鱼的祖先失去了电感受器，因此大多数鱼不能探测到电场，但电感受器似乎在两个不同的现代硬骨鱼群体中至少独立地“重新进化”了两次，包括鲶鱼和“电鱼”。电鱼有改良的肌肉，可以产生放电来击晕猎物或迷惑捕食者，它们使用一些电感受器进行交流。现代硬骨鱼（如鲶鱼）的电感受器的“再进化”是否涉及与其他脊椎动物的电感受器发育重要的相同基因，还是硬骨鱼的电感受器使用了不同的基因？我们计划在广泛的脊椎动物群体中研究电受体发育的胚胎起源和基因，包括七鳃鳗、鲨鱼、肺鱼、白鲟、蝾螈和鲶鱼。具体来说，我们的目标是：(1)确定在所有电感受器脊椎动物的胚胎发育过程中，电感受器和侧线机械感觉毛细胞是否具有共同的起源。(2)了解不同的脊椎动物，包括“重新进化”电感受器的硬鱼，在多大程度上使用相同的基因来构建它们的电感受器，以及是否使用相同或不同的基因来构建侧线机械感受器。总的来说，这些实验将使我们深入了解电感受器的胚胎发育，电感受器的进化过程，以及感知电场和感知水运动的感觉毛细胞之间的区别。虽然我们自己不再拥有这种古老的“第六感”，但了解电感受器是如何发展的，将使我们更好地了解脊椎动物感觉系统的整体发展和进化。

We are used to experiencing the world with five senses: sight, smell, taste, touch and hearing (which really detects the mechanical displacement of tiny 'hairs' on specialised sensory 'hair cells' in our inner ears). However, land vertebrates (reptiles, birds and mammals, including humans), as well as frogs and most modern bony fish, have lost one of the most ancient vertebrate senses, the ability to detect weak electric fields in water. This sense, 'electroreception', is used for finding prey and for orientation. Land vertebrates (but not frogs or fish) have also lost the 'lateral line system' of sensory hair cells that detect water movement (just like the mechanosensory hair cells in our inner ears); these are distributed in lines over the head and body (hence the name, 'lateral line'), and used for schooling behaviour, finding prey and detecting predators. The experiments in this grant proposal are aimed at understanding the embryonic development and course of evolution of electroreceptors, the modified sensory hair cells that give aquatic vertebrates this fascinating 'sixth sense', and their relationship with the lateral line system. Although evolutionarily very ancient, electroreceptors were only discovered in the 1950s, and we know very little about their development. They are found in all major aquatic vertebrate groups, including lampreys (the most primitive living vertebrates), cartilaginous fish (sharks and rays), primitive bony fish (sturgeon, paddlefish), lungfish (related to the ancestors of land vertebrates), and even some amphibians (salamanders). Although the ancestors of modern bony fish lost electroreceptors, so that most of these fish cannot detect electric fields, electroreceptors seem to have independently 're-evolved' at least twice in two different groups of modern bony fish, including catfish and 'electric fish'. Electric fish have modified muscles that generate an electric discharge to stun prey or confuse predators, and they use some of their electroreceptors for communication. Did the 're-evolution' of electroreceptors in modern bony fish, such as catfish, involve the same genes that are important for electroreceptor development in other vertebrates, or do bony fish electroreceptors use different genes? We plan to investigate the embryological origins and genes underlying electroreceptor development in a wide range of vertebrate groups, including lamprey, shark, lungfish, paddlefish, salamander and catfish. Specifically, we aim to: (1) Determine whether or not electroreceptors and lateral line mechanosensory hair cells share a common origin during embryonic development, in all electroreceptive vertebrates. (2) Learn to what extent different vertebrates, including teleosts that 're-evolved' electroreceptors, use the same genes to build their electroreceptors, and whether or not the same or different genes are used to build lateral line mechanoreceptors. Overall, these experiments will give us insight into the embryonic development of electroreceptors, the course of electroreceptor evolution, and what makes the difference between sensory hair cells that detect electric fields and those that detect water movement. Although we no longer have this ancient 'sixth sense' ourselves, understanding how electroreceptors develop will give us a better understanding overall of the development and evolution of vertebrate sensory systems.