To understand the evolutionary diversification of animals, the applicants will investigate the variation of phenotypes and their genetic basis in multiple species of fruitflies in the genus Drosophila. The connection to diverse phenotypic features has been mapped to protein-coding changes, cis-regulatory changes and lineage-specific genes. The applicants' recent discoveries showed that many young genes played essential roles in organism development. This research will (1) investigate the reproductive contribution of young genes using the evolutionary genetic analysis and gene silencing techniques, (2) detect their interactions with other genes in the genome using the gene-chip based techniques of experimental genomics, and (3) study their roles in the species divergence by comparative analysis of related species. These efforts will advance the understanding of fundamental problems of gene evolution and phenotypic evolution.
These studies will bring conceptual innovations in the understanding of biological systems. The applicants will also create new data and share with the public. Furthermore, the applicants will train undergraduate students, visiting students from other schools and different disciplines, to encourage more talented undergraduates to enter graduate schools and nurture cross-disciplinary investigation. The applicants will purposely initiate more collaborate with multiple research groups in various institutions both nationally and internationally. The knowledge on gene origination is important to the understanding of human evolution. The proposed project will be of general interest to the broad audience including scientists and non-scientists and the discoveries from this project will play a role in scientific education for the general public.
The evolution of the brain and behavior are two important related scientific problems, because they are critical for understanding basic biological processes and developing efficient drugs and treatments for related medical problems. Furthermore, the genetic bases for brain evolution are widely debated, yet whether or not newly evolved genes impact the evolution of the brain and behavior is vaguely understood. In this project, we investigated this scientific problem by experimentally examining recent gene evolution and its impact on the brain of Drosophila and we found that new genes frequently acquired neuronal expression, particularly in the mushroom bodies, the criticial components in the information processing of the brain. Using expression analysis techniques , e.g. the reverse transcription-polymerase chain reaction(RT-PCR), we found that a large proportion (49%) of the 330 young genes aged younger than 25 million years were expressed in Drosophila brains. The tissue-specific expression of new genes detected by enhancer-trapping and RNAseq revealed the non-random distribution of new genes on the mushroom body and antennal lobes (the brain neurons which received information input from the antenna). Surprisingly, we found the newer structure (alpha/beta lobes) of the mushroom body evolved with the origination of new genes, suggesting these genes were related to the evolution of the newer brain structure. Evolutionary signatures combined with expression profiling showed that natural selection influenced the evolution of young genes expressed in the brain, notably in mushroom bodies. An immediate prediction of these experiments was some of these newly evolving brain genes might impact the behaviors, especially the foraging behaviors in two genes which expressed in some of the antennal lobes in brain, the neural structure that was shown to be involved in foraging. We created a handy apparatus and powerful technique to quantitatively measure the foraging behaviors of fruit flies in various genetic conditions of gene expression. Using this technique, the behavioral experiment testing of this prediction by knocking down Xcbp1 and Desr confirmed that the two genes were expressed in the olfactory circuit and facilitate foraging behavior. Comparative behavioral analysis in two groups of species which contain or do not contain the new genes under examination, revealed significant divergence in foraging behavior between these species. Our experiments suggest that during adaptive evolution, new genes gain expression in specific brain structures and evolve new functions in neural circuits, which might contribute to the phenotypic evolution of animal behavior. In short, our experiments found that two new genes recently originated and drove the evolution of foraging behaviors in a few closely related Drosophila species. More details of these experiments and data have been published in a journal rigorously reviewed by experts (Chen et al, 2012, Cell Reports. Volume 1: 118-132.)
