Population density modulates insect progenitive plasticity through the regulation of dopamine biosynthesis

Insect fecundity is a quantitative phenotype strongly affected by genotypes and the environment. However, interactions between genotypes and environmental factors in modulating insect fecundity remain largely unknown. This study investigated the impact of population density on the fecundity of Nilaparvata lugens (brown planthopper; BPH) carrying homozygous high- (HFG) or low- (LFG) fecundity homozygous genotypes. Under low population densities, the fecundity and population growth rate of both genotypes showed similar increasing trends across generations, while the trends between HFG and LFG under high population densities were opposite. Through a combination of temporal analysis and weighted gene co-expression network analyses on RNA-seq data of HFG and LFG under low and high population densities in the 1st, 3rd, and 5th generations, we identified 2 gene modules that were associated with these density-dependent progenitive phenotypes. Four pathways related to the neural system were simultaneously enriched by the 2 gene modules. Furthermore, Nlpale, which encodes a tyrosine hydroxylase, was identified as a key gene. The RNA interference of this gene and manipulation of its downstream product dopamine significantly affected the basic and density-dependent progenitive phenotypes of BPH. These findings indicated that dopamine biosynthesis is the key regulatory factor that determines fecundity in response to density changes in different BPH genotypes. Thus, this study provides insights into the interaction of a typical environmental factor and insect genotype during the process of population regulation.