Neuronal Reorganization Underlies Evolution of Novel Adaptive Behavior

味觉系统检测并区分传达食物质量和营养价值信息的促味剂。为了应对含有糖的杀虫剂诱饵的选择，德国小蠊的种群已经变得厌恶葡萄糖和果糖。这种新出现的特征是基因编码的，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。德国小蠊是一种世界性的害虫，对社会具有重大的经济和医学影响。它是引发哮喘的过敏原的主要来源，也是病原微生物（包括抗生素耐药菌株）的载体。本计画将以行为学、电生理学及遗传学的分析，来探讨这种新行为快速出现的机制。这项研究是第一次在任何动物中（a）表征味觉系统的快速变化，导致新的适应行为的出现;（B）详细描述了一种新的感觉机制，其中相同强度的单一刺激通过激活不同的味觉神经元驱动相反的接受和拒绝反应;（c）表征动物行为抵抗的最佳理解情况。虽然行为抗性经常被认为是有效防治害虫的主要障碍，但行为抗性的机制尚不清楚。这项研究代表了对动物群体中快速出现行为抵抗特征的感觉机制的最清晰的解释。这些发现被纳入了神经生物学、行为学和进化的几本教科书和应用程序中。味觉多态性通常被描述为味觉感受神经元（GRN）在味觉模态中的敏感性变化，其表型范围从对特定化合物高度敏感到完全不敏感。拟议的项目解决了一个独特的获得功能的自然多态性，导致高度适应性的行为。该项目将测试以下假设：（a）葡萄糖和果糖作为阻吓剂被GRNs加工，（B）不同的味觉器官在其GRN组织中存在差异，有助于有效加工作为食欲和厌恶刺激的促味剂，和（c）这种神经元变化的分子机制涉及苦味GRN上糖味觉受体（GR）的错误表达或苦味GRN的修饰。GRs对葡萄糖或果糖的亲和力。途径和方法将包括味觉接受和拒绝的行为观察，电生理学研究，使用一个单一的感器制备，形态学研究，使用光，扫描和共聚焦显微镜，和遗传研究与人工选择的蟑螂谱系。遗传资源包括20个品系的选择与反复回交，在每一代避免特定的糖，以及线，其中这些特征已渗入到一个密切相关的物种。基因组序列中所有化学感受器的注释之后将是Pool-seq方法、全基因组重测序和RNA-seq。了解蟑螂的味觉系统，一个原始的hemimetabolous血统，将有助于更广泛地了解昆虫味觉，到目前为止，主要集中在holometabolous和更先进的双翅目和膜翅目。

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.