Chemical Warfare in the Battle
of the Sexes
Daniel E. L. Promislow1,2 and Matt Kaeberlein1
Merely perceiving the opposite sex can shorten
an animal’s life span.
It may not be a complete surprise to learn that prolonged exposure to the opposite sex could be detrimental to your health.
This is certainly true for some invertebrates,
such as nematode worms and fruit flies (1,
2). In this issue, Shi et al. (3) on page 536
and Maures et al. (4) on page 541 provide
important new insights into the genetic and
molecular processes that account for “
male-induced demise” in worms. The battle of the
sexes goes both ways, however, and on page
544, Gendron et al. (5) report that female-produced pheromones in the fruit fly can
have similar detrimental effects on longevity and other age-related traits in male flies.
Together, these studies pose some interesting evolutionary questions that touch on sex,
death, and aging.
It has long been known that having the
opposite sex around can reduce fitness in
some species. Fitness is determined by the
number of offspring an individual produces,
but is limited by costs of reproduction (6).
The costs of courtship, mating, and offspring
production are paid in higher mortality,
reduced immunity, loss of future reproduction, and many other traits.
The studies of Shi et al., Maures et al., and
Gendron et al. take this idea to a new level
by showing that costs of reproduction can
be incurred just by perceiving the opposite
sex. This is sufficient to decrease fat stores,
increase mortality, and as demonstrated by
Shi et al., shrink an animal’s overall size.
Interestingly, a similar importance for sensory perception of food has been observed.
In both fruit flies and worms, just the smell
of a rich diet is enough to increase mortality rate and prevent many of the benefits of
a low-calorie diet (7, 8). Gendron et al. show
that the scent of a female fruit fly (Drosophila
melanogaster), even when that smell comes
from another male fruit fly genetically altered
to produce female pheromones, is sufficient
to shorten the male’s life span substantially.
Similarly, in the worm Caenorhabditis ele-
gans, a species in which the vast majority of
animals are self-fertilizing hermaphrodites,
This effect is seen even in sterile mutants, dis-
tinguishing it from direct energetic costs of
These new observations raise two related
questions: What are the proximate mechanisms that reduce life span (and in the case of
the study by Shi et al., shrink females)? That
is, what lies in the “black box” between the
sensory input that turns on these pathways,
and the anatomical, physiological, and demographic consequences that lie downstream
(see the figure)? And, why, from an evolutionary perspective, does the presence of the
opposite sex shorten life span? The answer to
the first question will come from additional
mechanistic studies. But answers to both
questions will also benefit from an evolutionary perspective.
Previous studies suggest that the relation-
ship between mating and mortality could have
been shaped by sexually antagonistic coevo-
lution (9). According to this concept, the
behaviors by which a female can maximize
her evolutionary fitness are often in conflict
with those of her male partner and vice versa.
Research suggests that in the fruit fly, sexu-
ally antagonistic coevolution has led male
Drosophila to evolve ejaculate proteins that
manipulate female behavior and physiology
in ways that increase the male’s fitness (1).
And to counter the ways that males reduce
female fitness, selection acts on females to
evolve mechanisms to mitigate the male’s
effects (10). The two sexes are in a continuous
arms race, both trying to maximize their own
fitness, even if at the expense of the other sex.
Despite their different mating systems,
flies and worms are likely to have been influ-
enced by sexually antagonistic coevolution.
For example C. elegans are female hermaph-
rodites that can self-fertilize their own eggs.
Males are rare, typically less than 1% in nature
and can only reproduce by mating with her-
maphrodites. Hermaphrodites will generally
avoid outcrossing with males, which dilutes
their genetic contribution to offspring by half.
While selection should favor females that use
their own sperm, at the same time it should
select for males that do everything possible
to mate, even if that means coercing females,
Mating and mortality. (A) Female fruit flies can shorten the life span of males through a pheromone
pathway and unknown downstream mechanisms. (B) Signals from male worms can shorten the life span of
recipient hermaphroditic worms through various pathways that are not yet fully understood.
1Department of Pathology, University of Washington, Seattle, WA 98195 USA. 2Department of Biology, University of
Washington, Seattle, WA 98195, USA. E-mail: promislo@