A non-coding indel polymorphism in the fruitless gene of Drosophila melanogaster exhibits antagonistically pleiotropic fitness effects

The amount of genetic variation for fitness within populations tends to
exceed that expected under mutation-selection-drift balance. Several
mechanisms have been proposed to actively maintain polymorphism and
account for this discrepancy, including antagonistic pleiotropy (AP),
where allelic variants have opposing effects on different components of
fitness. Here we identify a non-coding indel polymorphism in the fruitless
gene of Drosophila melanogaster and measure survival and reproductive
components of fitness in males and females of replicate lines carrying
each respective allele. Expressing the fruitless region in a hemizygous
state reveals a pattern of AP, with one allele generating greater
reproductive fitness and the other conferring greater survival to
adulthood. Different fitness effects were observed in an alternative
genetic background, which may reflect dominance reversal and/or epistasis.
Our findings link sequence-level variation at a single locus with complex
effects on a range of fitness components, thus helping to explain the
maintenance of genetic variation for fitness. Transcription factors, such
as fruitless, may be prime candidates for targets of balancing selection
since they interact with multiple target loci and their associated
phenotypic effects.