All cells in the body share the same genome yet assume different identities and perform different functions. The functional capacity of an organ depends on the composition of its transcriptome - the subset of genes that are actively expressed in that organ. In the course of evolution, transcriptome turnover - qualitative remodeling of tissue-specific transcriptomes through gains and losses of gene expression - can lead to major changes in organ function. This is particularly true in the male reproductive system, which shows the highest rate of evolutionary divergence in all animals including humans and their closest relatives. The overall goal of this project is to achieve a systematic understanding of the genomic mechanisms responsible for transcriptome turnover in the male reproductive system using a group of closely related Drosophila species as a model. These genomic mechanisms span the range from the origin of entirely new genes to the recruitment of old genes for novel functions.
Our first aim i s to quantify the rate at which each of these mechanisms contributes to transcriptome turnover, in order to understand the relative importance of each mechanism in shaping organ function. In addition, we will determine whether transcriptome turnover occurs at a steady rate, or is accelerated during the origin of particular species.
Our second aim i s to characterize the changes in genetic regulatory networks that result from the recruitment of new genes into the reproductive organs. To accomplish this, we will develop a new transgenic method for in vivo protein modification, and use this method to identify the downstream targets of the regulatory genes that were recruited into the male reproductive system recently in evolution.
Our third aim i s to understand how the introduction of new genes into the transcriptome affects organ function and, especially, male fertility. This will be accomplished by systematically knocking out recently recruited genes of different age specifically in the reproductive organs. Finally, we will use computational methods to understand how tissue-specific recruitment events influence the subsequent evolution of genes and genomes. Together, these approaches will help elucidate the evolutionary processes that influence male fertility and, more generally, the genomic mechanisms that promote complexity and diversity in animal evolution.

Public Health Relevance

Genes expressed in the male reproductive system show by far the greatest divergence between humans and their closest relatives. However, the genomic processes that lead to the expression of different genes in the reproductive organs of different species are poorly understood. The goal of this project is to determine how new genes are recruited into the reproductive organs in the course of evolution, and how their incorporation affects organ function and male fertility.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM112776-03
Application #
9185987
Study Section
Genetic Variation and Evolution Study Section (GVE)
Program Officer
Janes, Daniel E
Project Start
2014-12-15
Project End
2018-11-30
Budget Start
2016-12-01
Budget End
2018-11-30
Support Year
3
Fiscal Year
2017
Total Cost
Indirect Cost
Name
University of California Davis
Department
Anatomy/Cell Biology
Type
Schools of Medicine
DUNS #
047120084
City
Davis
State
CA
Country
United States
Zip Code
95618