Threshold-dependent gene regulation and partial assortative mating determine wing dimorphism of an Insect

Wing dimorphism is a fantastic life-historical trait of insects which indicates the developmental trend of populations, going as migrants or staying as residents. The alternative wing morph enhances adaptability of insects to changing environments. However, the underlying mechanism for maintaining wing dimorphism remains vague. The brown planthoppers Nilaparvata lugens, a serious pest of rice, are either short-winged or long-winged. The shift between two wing morphs is determined by two insulin receptors. So, this pest is a better model organism to explore the mechanism of wing dimorphism. Here, the short- and long-winged strains of N. lugens were selected. Rates of a selected wing morph were linearly increased in populations, and the selection response of the short-winged morph was stronger than that of the long-winged. Selection enhanced the migratory or resident propensity. Directional selection for the long-winged morph resulted in longer and lighter forewings, while selection for the short-winged morph generated shorter and thicker wings and higher fecundity. Relative expression levels of wing development genes InR1, InR2, and FOXO were positively correlated with the short-winged rate in the short-winged strain, while they were negatively correlated with the long-winged rate in the long-winged strain at specific stages. The change rate of expression levels was approximately two times as high as that of the wing morph rates in populations, indicating a high threshold-dependent gene expressed regulation of a wing morph. A partial assortative mating behavior occurred between the nearly pure-bred lineages of short- and long-winged strains. The short-winged males preferred to mate with short-winged females while the long-winged males mated with the short- and long-winged females equally. The threshold-dependent mode is flexible to adjust the wing morph according to environmental conditions and the partial assortative mating promotes the genetic exchange between two wing morphs which drive the maintenance of wing dimorphism.翅多型（Wing dimorphism）是昆虫一类极具研究价值的生活史性状，可反映种群的发育走向——或是作为迁飞者扩散，或是作为居留者定居。这种可逆的翅型分化可增强昆虫对多变环境的适应能力。然而，维持翅多型的内在机制至今仍不甚明晰。褐飞虱（Nilaparvata lugens）是水稻的重大害虫，其翅型分为短翅型与长翅型两种，两种翅型的转换由两种胰岛素受体调控，因此该物种是探究翅多型机制的理想模式生物。本研究选取了褐飞虱的短翅型与长翅型品系进行选育：种群中目标选育翅型的比例呈线性升高趋势，且短翅型的选育响应强度高于长翅型。定向选育强化了种群的迁飞或居留倾向：对长翅型的定向选育可使前翅更长、更轻薄；而短翅型选育则会获得更短且粗壮的翅型，同时提升繁殖力。翅发育相关基因InR1、InR2与FOXO的相对表达量，在短翅型品系中与短翅型比例呈正相关；而在长翅型品系的特定发育阶段，其相对表达量则与长翅型比例呈负相关。基因表达量的变化幅度约为种群翅型比例变化幅度的两倍，这表明翅型调控存在阈值依赖性的基因表达机制。短翅型与长翅型品系的近纯合谱系间存在部分选型交配（assortative mating）行为：短翅型雄虫偏好与短翅型雌虫交配，而长翅型雄虫对长、短翅型雌虫的交配偏好无显著差异。这种阈值依赖模式可根据环境条件灵活调整翅型，而部分选型交配则促进了两种翅型种群间的基因交流，进而推动翅多型的维持。