We evaluated the influence of pre- and post-copulatory sexual selection upo
n male reproductive traits in a naturally promiscuous species, Drosophila m
elanogaster. Sexual selection was removed in two replicate populations thro
ugh enforced monogamous mating with random mate assignment or retained in p
olyandrous controls. Monogamous mating eliminates all opportunities for mat
e competition, mate discrimination, sperm competition, cryptic female choic
e and, hence, sexual conflict. Levels of divergence between lines in sperm
production and male fitness traits were quantified after 38-81 generations
of selection. Three a priori predictions were tested: (i) male investment i
n spermatogenesis will be lower in monogamy-line males due to the absence o
f sperm competition selection, (ii) due to the evolution of increased male
benevolence, the fitness of females paired with monogamy-line males will be
higher than that of females paired with control-line males, and (iii) mono
gamy-line males will exhibit decreased competitive reproductive success rel
ative to control-line males. The first two predictions were supported, wher
eas the third prediction was not. Monogamy males evolved a smaller body siz
e and the size of their testes and the number of sperm within the testes we
re disproportionately further reduced. In contrast, the fitness of monogamo
us males land their mates) was greater when reproducing in a non-competitiv
e context: females mated once with monogamous males produced offspring at a
faster rate and produced a greater total number of surviving progeny than
did females mated to control males. The results indicate that sexual select
ion favours the production of increased numbers of sperm in D. melanogaster
and that sexual selection favours some male traits conferring a direct cos
t to the fecundity of females.