Molecular evolution of the sex peptide network in Drosophila

Successful reproduction depends on interactions between numerous proteins
beyond those involved directly in gamete fusion.   While
such reproductive proteins evolve in response to sexual selection
pressures, how networks of interacting proteins arise and evolve as
reproductive phenotypes change remains an open question.  Here,
we investigated the molecular evolution of the “sex peptide network” of
Drosophila melanogaster, a functionally well-characterized reproductive
protein network.  In this species, the peptide hormone sex
peptide (SP) and its interacting proteins cause major changes in female
physiology and behavior after mating.  In contrast, females of
more distantly related Drosophila species do not respond to SP. 
In spite of these phenotypic differences, we detected orthologs of all
network proteins across 22 diverse Drosophila species and found evidence
that most orthologs likely function in reproduction throughout the
genus.  Within SP-responsive species, we detected the recurrent,
adaptive evolution of several network proteins, consistent with sexual
selection acting to continually refine network function.  We also
found some evidence for adaptive evolution of several proteins along two
specific phylogenetic lineages that correspond with increased expression
of the SP receptor in female reproductive tracts or increased sperm
length, respectively.  Finally, we used gene expression profiling
to examine the likely degree of functional conservation of the paralogs of
an SP network protein that arose via gene duplication.  Our
results suggest a dynamic history for the SP network in which network
members arose before the onset of robust SP-mediated responses and then
were shaped by both purifying and positive selection.