Neuronal Reorganization Underlies Evolution of Novel Adaptive Behavior

味觉系统对传达食物质量和营养价值信息的品尝者进行检测和区分。作为对含有糖的杀虫剂诱饵的选择的反应，德国蟑螂的种群已经对葡萄糖和果糖产生了反感。这种新出现的特征是遗传编码的，当含有葡萄糖或果糖的诱饵用于害虫控制时，它为蟑螂提供了巨大的优势。德国蟑螂是一种世界性的害虫，对社会的经济和医学影响都很大。它是可能引发哮喘的过敏原的主要来源，也是包括抗生素耐药菌株在内的病原微生物的媒介。这个项目将通过行为、电生理和遗传分析来描述导致这种新行为迅速出现的机制。这项研究在动物中是第一个：(A)描述了导致新的适应行为出现的味觉系统的快速变化；(B)详细描述了一种新的感觉机制，即相同强度的单一刺激通过激活不同的味觉神经元来驱动相反的接受和拒绝反应；以及(C)描述了对动物行为抵抗的最好理解的情况。虽然行为抗性经常被认为是有效控制害虫的主要障碍，但行为抗性背后的机制尚不清楚。这项研究代表了对感官机制的最清晰解释，这种机制是动物群体中行为抵抗性特征迅速出现的基础。这些发现被纳入了几本关于神经生物学、行为和进化的教科书和应用程序中。味觉多态通常被描述为味觉感受器神经元(GRN)在味觉模式中敏感度的变化，其表型从高度敏感到完全不敏感，对特定的化合物。拟议的项目解决了一种独特的功能获得性自然多态性，导致了一种高度适应性的行为。该项目将检验如下假说：(A)葡萄糖和果糖作为威慑物质被GRN处理；(B)不同的味觉器官在GRN组织中存在差异，从而有助于将味觉作为食欲和厌恶的刺激进行有效处理；以及(C)这种神经元变化的分子机制(S)涉及苦味GRN上的糖味觉受体(GRs)的错误表达或苦味GRN上苦味GRs的修饰以与葡萄糖或果糖亲和力。途径和方法将包括味觉接受和拒绝的行为观察，使用单一感受器准备的电生理研究，使用光、扫描和共聚焦显微镜的形态研究，以及人工选择的蟑螂谱系的遗传研究。遗传资源包括在每个世代为避免特定糖分而进行轮回回交的20个品系，以及将这些性状导入到近缘物种中的品系。基因组序列中所有化学受体的注释之后将采用Pool-Seq方法、全基因组重新测序和RNA-Seq。了解蟑螂的味觉系统将有助于更广泛地理解昆虫的味觉，到目前为止，昆虫的味觉主要集中在全变态和更高级的双翅目和膜翅目。

The taste system detects and discriminates among tastants that convey information about the quality and nutritional value of food. In response to selection with insecticide baits that contain sugars, populations of the German cockroach have become averse to glucose and fructose. This emergent trait is genetically-encoded and it provides a huge advantage to the cockroach when glucose- or fructose-containing baits are used in pest control. The German cockroach is a world-wide pest with significant economic and medical impacts on society. It is a principal source of allergens that can trigger asthma and vector of pathogenic microorganisms, including antibiotic resistant strains. This project will delineate the mechanisms responsible for the rapid emergence of this novel behavior with behavioral, electrophysiological and genetic analyses. This research is the first in any animal to (a) characterize rapid changes in the taste system that have resulted in the emergence of a new adaptive behavior; (b) describe in detail a novel sensory mechanism where a single stimulus at the same intensity drives opposite acceptance and rejection responses by activating different taste neurons; and (c) characterize the best understood case of behavioral resistance in animals. Although behavioral resistance is often cited as a major impediment to efficacious pest control, the mechanisms that underlie behavioral resistance are not known. This research represents the clearest explanation of sensory mechanisms that underlie the rapid emergence of a behavioral resistance trait in animal populations. The findings are being incorporated into several textbooks and apps on Neurobiology, Behavior and Evolution.Taste polymorphisms are often described as changes in sensitivity of gustatory receptor neurons (GRNs) within a taste modality, with phenotypes ranging from highly sensitive to completely insensitive to a particular compound. The proposed project addresses a unique gain-of-function natural polymorphism that results in a highly adaptive behavior. The project will test the hypotheses that (a) glucose and fructose are processed as deterrents by GRNs, (b) different taste organs differ in their GRN organization, contributing to effective processing of tastants as appetitive and aversive stimuli, and (c) that the molecular mechanism(s) that underlie this neuronal change involves either mis-expression of sugar-gustatory receptors (GRs) on bitter GRNs or modifications of bitter-GRs on bitter-GRNs for affinity for glucose or fructose. Approaches and methods will include behavioral observations of tastant acceptance and rejection, electrophysiological studies using a single sensillum preparation, morphological studies using light, scanning and confocal microscopy, and genetic studies with artificially selected lineages of cockroaches. Genetic resources include 20 lines of selection-with-recurrent-backcrossing at each generation for avoidance of specific sugars, as well as lines in which these traits have been introgressed into a closely related species. Annotation of all chemoreceptors in the genome sequence will be followed by a Pool-seq approach, whole-genome re-sequencing and RNA-seq. Understanding the gustatory system of cockroaches, a primitive hemimetabolous lineage, will contribute to a broader understanding of insect gustation that so far has centered mainly on holometabolous and more highly advanced Diptera and Hymenoptera.