fruit flies

Arthur L. Baron (abaron@STU.ATHABASCAU.CA)
Mon, 22 Jul 1996 13:18:55 MDT

My apologies if this is old news to some.

>From Science Magazine, May 1996

Flies Unmask Evolutionary Warfare Between Sexes
By Virgina Morell

There's yet another front in that most enduring of all wars, the
battle between the sexes. Since the 1970's, evolutionary
biologists have suspected that males and females are locked in a
coevolutionary struggle to achieve reproductive success at their
mates expense, and in many species the female's reproductive
tract was thought to be a key battlefield. There, the
sexes produce various proteins that affect everything from sperm
mobility to female sexual desire, apparently in an effort to
chemically outgun each other.

In an ingenious experiment with fruit flies, William R. Rice an
evolutionary biologist at the University of California, Santa
Cruz, has decoupled what he terms the sexes coevolutionary dance,
forcing the females to stand still, in evolutionary terms, while
the males continued their adaptive moves. And he discovered that
the dance is actually more of a duel. Rice found that males
rapidly evolved to take advantage of the females. After about 40
generations, the "supermale" flies fathered more offspring,
prevented their competitors from siring progeny in their common
mates - and caused their female partners to die young.

Rice's study thus provides elegant experimental support for a
basic tenet of sociobiology - that the reproductive interests of
males and females are essentially at odds, and that this
antagonism fuels at least some evolutionary change. "The sexes
do coevolve through time, just as do host [organisms] and
parasites, or predators and prey," Rice says. "We've always
thought that this [coevolution] was going on, but it's very hard
to see," says Dan Howard, an evolutionary biologist at New Mexico
State University at Las Cruces. "Rice has finally unmasked the
chemical antagonism between the sexes." Howard thinks that Rice
has also unmasked a possible consequence of this warfare: it can
put up barriers to fertilization, leading to genetic divergence
between populations and thus to the formation of new species.

Rice investigated these questions in a species known to wage
intersexual chemical combat - the fruit fly. Researchers already
knew that the seminal fluid of male fruit flies contains some
proteins that are toxic to the female. For example, one male
peptide both encourages the female to increase her egg-laying
rate and dampens her sexual appetite - chemical tricks that the
male may use to ensure that only his sperm fertilize the eggs.
Another male protein apparently kills of rivals' sperm and
inadvertently poisons females in the process.

The female, in turn, secretes chemicals in her own oviduct that
may fend off the male's proteins; other proteins may reduce the
number of sperm or switch of the male's sexual suppressant, or
both. These countermeasures help turn the female's reproductive
tract in a gauntlet for the male's would-be progeny. Many of the
5000 or so sperm that a male may ejaculate into a female simply
fall out, or perhaps are weakened by the female secretions. The
female can only store about 500 sperm, which she holds in special
internal pockets until her eggs are ready for fertilization.

The reason for this chemical antagonism is that "the interests of
males and females are not the same." says Howard. "The male's
overriding interest is to fertilize the egg and do it before a
rival male does, while the female's goal is to make sure that the
egg is fertilized with only one sperm" in order to avoid
developmental problems. The female also seeks to have plenty of
sperm available at the right time for egg-laying while receiving
as few toxins as possible. "As far as I can tell, all a female
[fly] wants is sperm" - sperm without toxins, says Rice. "But
what she gets is sperm plus the seminal fluid, which the male may
use to control her and keep out other males, turning her body
into a battlefield."

This power struggle has evolutionary consequences, as Rice
revealed by permitting only male flies to evolve. He managed
this feat in part by taking advantage of a genetic idiosyncrasy
of fruit flies: each offspring receives one set of genes from its
father and one from its mother; in male flies, these genes do not
recombine. By using specially constructed chromosomes, Rice
enabled the paternal set of genes (or the male haplotype) to be
transmitted exclusively from father to son. The maternally
derived genes ( the female haplotype) also passed to sons, but
had no effect on the population, because Rice culled the female
haplotypes. Thus the males in Rice's experiment were essentially
cloned, while the females were merely "egg-laying machines." he
says. As a result the males could follow their own evolutionary
path, separate from the females.

Rice then mated each generation of cloned males with females from
a large stock population, in which normal mating presumably kept
the sexes in an evolutionary steady state. With no opportunity
to adapt to the experimental males, the females were evolutionary
"stuck." But the male clones continued to adapt to the target
females, as mutations beneficial to male reproductive success
were passed on from father to son.

Rice found that those genetic advantages accumulated quickly, and
in only 41 generations the males achieved stunning reproductive
success. Like stars in a fruit fly version of a bad B movie,
these supermales persuaded the females to mate with them more
often than their rivals (possibly via sheer persistence or
seductive pheromones), and they fathered a disproportionate
number of offspring. But the male's success brought no
corresponding increase in the females' fecundity. In fact, these
females who mated with these Don Jaun flies died young,
apparently because of the potent load of toxins in the males'
seminal fluids, says Rice. "There was no benefit to the females
at all from mating with these guys,. It was deleterious to
them." Even females who mated only once with the supermales died

The experiment reveals that under normal circumstances, there is
"perpetual coevolution of males and females," says Rice. For
every move by the male to increase his success at the expense of
the female, she would normally make a countermove. But when the
females' countermoves were blocked, the males' interest
prevailed. The findings complemented long-standing evidence for
behavioral warfare between the sexes, such as forced copulation
between ducks and deceitful matings in some primates, notes John
Alcock, a behavioral ecologist at Arizona State University in
Temple: "This study demonstrates the level of chemical warfare
that exists as well."

The quick genetic respose of the evolving males to the sitting
duck females also "shows the speed with which males can exploit
females for their own reproductive advantage," says Alcock. And
Howard suggests that the speedy evolutionary change means that
"barriers to fertilization [between species] can also arise
quickly. In fact, you can see such a barrier in its initial
stages right there in Rice's experiment." Because the supermales
fertilized most of the eggs, normal males were effectively shut
out and longer contributed their genes to the population. When
genes don't move freely between groups, the populations are
considered reproductively isolated - and thus separate species.
Indeed, the reproductive tract right after insemination may be
the setting where barriers to gene flow first arise, says Howard,
Rice, and many other researchers in evolutionary biology and
genetics. "Intersexual competition can thus be seen as a major
engine of speciation,"says Rice.

But although Rice's demonstration of the evolutionary duel
between the sexes wins plaudits all around, not everyone agrees
that this intersexual is driving speciation. For example, Chung-
I Wu, an evolutionary geneticist at the University of Chicago,
puts his money on male-male competition as having a bigger role
in speciation, because male reproductive traits evolve faster.
"The genetic blueprint for males to make sperm changes at a much
more dramatic rate than do equivalent genes in females. It's ten
times faster," he notes. Counters Rice, "Even if sexual
coevolution only contributes 10% to the process, that's still

To show that the female's response is also an important factor in
driving evolutionary change, Rice may have to reverse his
experiment, and hold the males in check and let the females
evolve. Sexual conflict theory more or less predicts that the
females will turn into the equivalent of fruit fly Ice Queens,
mating with only one or two males to limit the amount of toxins
they receive and to get "just enough sperm to get the job done,"
Rice speculates. Will the male partners of such superfemales
also meet an early death? Stay tuned: the battle of the sexes is
far from over. End.

And so it goes.