EDGE CMT: The genomic basis of male fitness variation in wild populations of Drosophila

Fitness refers to the ability of an organism to survive and reproduce in its natural habitat. It is one of the most important attributes of any species. Fitness varies greatly among individuals within most species and this variation is ‘complex’ in multiple aspects.

First, differences in fitness are caused by both differences in the environment experienced by organisms and in the genes they carry. Second, fitness involves multiple distinct components including survival, mate acquisition, fecundity and even the competitive success of gametes (sperm or egg). This research project develops and executes a collection of novel experimental and statistical methods to provide an unprecedented characterization of fitness variation in the model fruit fly species.

The experiments will dissect fitness differences into their many distinct genetic causes by linking genetic variants at the DNA level to their effects on survival, mating success, and competition among gametes. The research exploits recent technological developments in genome sequencing, facilitating large-scale experiments, and enabling powerful hypothesis testing.

The experimental results in the model fruit fly will provide proof-of-principal for the subsequent study of many different organisms. The project will also build our scientific workforce through training of students and postdoctoral researchers in genomic and quantitative science. Finally, the project will provide generalizable software that will be distributed to the scientific community for the analysis of similar experiments in genetics and genomics.

A mechanistic understanding of natural selection requires that we (1) identify the processes generating fitness variation among individuals and (2) quantitatively estimate how that variation results in allele frequency change. This project employs massive-scale genome sequencing combined with field collections and experimental crosses to estimate the importance of differential survival relative to differential reproductive success.

It estimates the frequency and strength of gametic selection, defined broadly to include meiotic drive, relative to fitness differences among diploid individuals. Synthesis of estimates within and across experiments will determine if different components of selection, such as viability and sexual selection, are typically reinforcing or conflicting. A substantial component of the project is theoretical, to develop algorithms and then make them publicly available (software development).

These algorithms use genomic data to estimate fitness differences from their immediate effects, specifically the change in allele frequency at loci across the genome as they experience selection. The second phase of experimental work is a series of lab experiments using wild-derived genomes. These experiments test alternative hypotheses about how different aspects of male reproduction generate fitness variation at genes across the genome of Drosophila melanogaster.

Finally, the project will train the scientific workforce in genomic and quantitative science and advance discovery in other systems by the dissemination of generalizable software that will be disseminated to the scientific community.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.