Download Bickering Genes Shape Evolution

CREDIT: MARK MOFFETT
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breaking away from the Indian subcontinent
some 88 million years ago, the isolated,
France-sized landmass has produced oddities such as the 7-centimeter-long Madagascan hissing cockroach and the lemurs, our
big-eyed primate cousins. But the scale and
breadth of Madagascar’s radiations and their
significance to evolutionary biology have
become apparent only over the past 5 to 10
years of research, says Goodman. This is in
no small part due to Goodman’s own research on the phylogeny and distribution of
Madagascar’s biota. “Steve’s genius lies in
the combination of his abilities in the field
along with his ability to synthesize and communicate,” says Fisher.
In spite of all this biological wealth,
Madagascar has remained poorly studied
due to political turmoil and creaking infrastructure. Since the Malagasy people forced
out their French colonizers in 1960, the
country has lurched from dictatorship to dictatorship. Westerners have often been ejected from the country, and when they have
been allowed in, field biologists have always
had to grapple with the very sparse network
of passable roads. Many biological hot spots
are still a 100-kilometer walk from any road.
Tenacious researchers like Goodman
have opened up to the world the treasures
hiding on the island. Since first settling
here in 1989, Goodman has himself identified dozens of species new to science, and
the biologists he has trained or brought into
the field have added hundreds more. When
it comes to the challenging terrain of
Madagascar, says Fisher, “you can plunk
your finger down anywhere on the map,
and Steve is the guy who can make it in
there and get the data.”
In recent years, liberalization and international aid have made it easier for biologists to study Madagascar in depth. But their
work has revealed a bleak picture. Most of
Madagascar’s species are huddled together
in the 10% of the original forest cover that’s
still intact. These pockets of natural forest
are now dying a slow death by degradation
and fragmentation. Madagascar’s dense biodiversity, combined with looming ecological
disaster, has made it the top priority in the
eyes of many conservation biologists. Madagascar is home to what biologists call
“charismatic megafauna,” such as the
lemurs, which have helped conservation initiatives attract hundreds of millions of dollars over the past 3 decades. But much of
this money has disappeared into the country’s inefficient bureaucracy.
Another problem is that biologists have
tended not to include Malagasy scientists in
their projects, although their involvement is
required for any lasting conservation. Goodman’s inclusive work ethic has helped reverse this trend, says Robert Dewar, an ecol-
ogist and conservation biologist at the University of Connecticut, Storrs. “No one has
done as much to train Malagasy biologists
as Steve.” Working with WWF-Madagascar,
Goodman created the Ecological Training
Program (ETP) in 1993, which is the first of
its kind and is now being replicated elsewhere in Africa. More than 30 Malagasy
field biologists have gone through the ETP,
including Raselimanana, who is now
the chief biodiversity scientist for WWFMadagascar. Goodman still directs the program, spending about 6 months of the year
in the forests. Starting next month, he is taking the only substantial break from the field
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in years, but not for a vacation. He is putting
the finishing touches on a book that he
hopes will change the fate of Madagascar
(see sidebar).
Back at camp, night has fallen and Goodman is telling a joke in Malagasy, French, and
English so no one is left out. He looks a little
healthier. “I come down with a fever once a
month or so,” he says nonchalantly, due to the
malaria and other parasites he carries for life.
Would he trade it all in for a comfy teaching
job in the States? “Not a chance.” At long
last, Goodman feels at home.
–JOHN BOHANNON
John Bohannon is a writer based in Paris.
Meiotic Drive
Bickering Genes Shape Evolution
Not all genes follow the rules of inheritance; now researchers are discovering how
organisms adapt to the troublemakers
Reproduction is supposed to be an equal op- markedly affect the evolution of the whole
portunity event. Consider humans: In devel- genome,” says Catherine Montchampoping sperm, the sex chromosomes sort Moreau, an evolutionary biologist at CNRS,
50:50 such that half the sperm carry the the French basic research agency, in Gif-Surmale-defining Y chromosome and the rest Yvette. As such, the work is leading evolusport an X. Only the randomness of fertil- tionary biologists to see patterns in what once
ization leads to families of nine girls and no was considered a fluke of nature.
boys, for example. The same supposedly
Genes usually work together. Their surholds true for the rest of the genome.
vival depends on their collective ability to
But in humans, flies, mice, and perhaps make an individual run fast, eat well, repromany other organisms, guerrilla warfare duce efficiently, and ward off infections. Still,
within the genome sometimes pits one ele- as biologists are increasingly coming to realment against another. This often takes on the ize, not all versions—called alleles—of each
appearance of a battle between the sexes, but gene are alike. Some appear to look out for
it is really a fight between genes. In this themselves. Somehow, they are more adept at
struggle, typically one or more of the X chro- passing copies of themselves on, sometimes
mosome’s genes strike out against the Y’s even crowding other alleles out. It’s a game of
genes. Genes on other
chromosomes also can
get caught up in this
struggle, causing an escalating arms race.
Researchers have
caught glimpses of
these so-called intragenomic conflicts ever
since the 1920s. They
dubbed the phenomenon “meiotic drive.”
But only in the past
decade have they come
to appreciate just how
devious and pervasive
the aggressive genes—
called drivers—are,
and how dogged the
counterattacks can be. Emblem of excellence. Female stalk-eyed flies judge males (above) by the
This interplay “may length of their stalks, which reveal whether the male carries selfish genes.
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numbers, and the more prolific the DNA, the
greater its evolutionary success.
In recent years, researchers have discovered a few mechanisms by which one gene
can thwart a rival. During meiosis, chromosomes copy themselves, line up with their
matching partners, and then split up. First
the partners head into different halves of the
dividing cell; then the duplicates—so-called
sister chromatids—separate as that new cell
splits in two. In 2000, Montchamp-Moreau
and her group unraveled one cellular mechanism behind meiotic drive, a technique that
seems to be particularly widespread among
covered a similar phenomenon wherein a
chromosome bearing the “T” version of a
group of immune system genes called the T
locus was transmitted more often than the “t”
version, another example of what Hiraizumi
and Crow called segregation distortion. Now
researchers know that meiotic drive exists in
more than 20 species of flies, two species of
mosquito, an arachnid, a lemming, mice, humans, and some plants and fungi.
In the early 1990s, researchers began to
uncover just how complex this jockeying during reproduction could be and glimpse its potential consequences. Some who never intended to look at meiotic
drive became the
most avid researchers. MontchampMoreau stumbled
across female-biased
progeny in Drosophila simulans while
looking into how
mobile elements,
short stretches of
DNA that hop from
one part of a geBigger, better. When two chromosomes merge, they are more likely to be nome to another,
passed on to eggs than separate chromosomes are.
might interfere with
mating. At about the
insects. They found that certain fruit fly same time, Gerald Wilkinson, an evolutionary
driver genes caused a misstep when Y chro- biologist at the University of Maryland, Colmosome chromatids parted ways. “As a re- lege Park, discovered something strange about
sult, the corresponding [precursor sperm] tiny stalk-eyed flies that he and his colleagues
did not develop into functional Y-bearing had collected in Malaysia. “Some males were
sperm,” she says. But in mice and possibly producing all daughters,” he explains. And
humans, other researchers have since deter- Jeanne and David Zeh, evolutionary biologists
mined that the action takes place in the egg at the University of Nevada, Reno, unsuspectrather than the sperm.
ingly headed in this direction with Jeanne’s
To counter a selfish driver gene, one or work on a pseudoscorpion found in Central
more genes often evolve the ability to gang and South America. Still others were drawn to
up against it to keep it from proliferating mammals that demonstrated unequal inherimore than it should. The defensive behavior tance of certain genes and chromosomes.
appears by chance, but if effective, it is seMontchamp-Moreau and her colleagues
lected for through time. In other cases, new were the first to discover meiotic drive in
research is showing, meiotic drive can spur D. simulans. Typically, reproduction in these
the evolution of sexual selection or other fruit flies yields about equal numbers of
adaptations to quell selfish genes.
males and females. But her experiments upset the détente that maintained a balanced sex
Hidden intrigue
ratio. To look at mobile elements, she had beThomas Hunt Morgan of Columbia Univer- gun to breed flies from isolated populations.
sity in New York City first observed skewed Sometimes offspring of males and females
genetic inheritance patterns in the fruit fly from different places had skewed sex ratios.
Drosophila melanogaster. Some populations
Driver genes were at fault, she discovhad more females than males, and through ered. These genes were normally unbreeding experiments he linked this bias to detectable because other genes—the
the sex chromosome. In the 1950s, Yuichiro suppressors—had evolved ways to keep the
Hiraizumi and James Crow of the University driver in check. But in these experiments,
of Wisconsin, Madison, observed biased in- the second-generation flies often inherited
heritance wherein certain crosses between suppressors from one population and drivers
white-eyed and red-eyed flies yielded only from another. The suppressors were unred-eyed offspring, rather than a mix of the equipped to neutralize new aggressors—
two. Thirty years later, Mary Lyon, a geneti- uncloaking meiotic drive.
cist at the Medical Research Council’s MamSuppressors had been found in other
malian Genetics Unit in Harwell, U.K., dis- species. However, “for the first time, we de-
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scribed a complete suppression of drive,
which restored an equal sex ratio in the populations even though the drivers were at high
frequency,” says Montchamp-Moreau. The
cloaking had fooled her and others
into thinking that this species was free of
drivers, and so were most others.
The discovery helped explain why drivers persist. Uncontrolled, drivers can be their
own worst enemy. Theoretical work indicates that aggressive alleles can cause a
population—and the driver it hosts—to go
extinct. Each generation would have fewer
males, until none would be left to mate with
females. A suppressor diverts a driver from
its destructive path. Montchamp-Moreau’s
discovery prompted others to search for this
hidden antagonism. And, according to David
Hall, an evolutionary biologist at the University of Texas, Austin, “a lot of cryptic drivers
are now showing up.”
The evolution of meiotic drive can take
different trajectories, Montchamp-Moreau
has found. In some D. simulans populations, the drivers seem to be spreading; in
others, drivers show signs of becoming ineffective; and in a few, drivers are completely disarmed and are probably breaking
down within the genome.
Driving evolution
Laboratory breeding studies also alerted the
University of Maryland’s Wilkinson to meiotic drive. He became curious about why
some male stalk-eyed flies produce only female young. He ruled out infections with
Wolbachia, a bacterium that distorts sex ratios in its hosts. More breeding experiments
traced the cause of the skewed sex ratio to
the X chromosome. Then, in 1998, he and
his colleagues discovered a connection between meiotic drive and a male ornament:
the eye stalk. But suppressor genes weren’t
keeping the drivers in check, the team
found—sexual selection was.
Males have longer eye stalks than females, and females often prefer males with
particularly long stalks. This favoritism allows females to avoid driver genes, which are
associated with short stalks, Wilkinson and
colleagues found. Stalk length is determined
largely by a gene on the X chromosome. That
gene is close to the driver gene—so close that
the two are inherited as a unit, Wilkinson’s
postdoctoral fellow Philip Johns reported in
June at the Evolution 2003 meeting in Chico,
California. The allele for a shorter stalk is
hooked up to the allele causing meiotic drive,
whereas that for a longer stalk is joined to the
nondriving allele.
“Our results surprisingly implicate meiotic drive as a potent evolutionary agent that
can catalyze sexual selection,” Wilkinson
points out. Before, researchers thought that
females evaluate ornamental male traits as a
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CREDIT: KATHY KAISER-ROGERS/UNC
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CREDIT: JEANNE ZEH/UNIVERSITY OF NEVADA, RENO
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way to tell which males are the healthiest. In a driver’s power.
landed less than 500 years ago, mouse
this case, general health seems to be secondPardo-Manuel de Villena, Sapienza, and chromosome numbers now range from 22
ary. Instead, this preference seems to have colleagues have begun to focus on a chro- to 28. When those with 22 breed with mice
evolved in reaction to a selfish gene. Meiotic mosomal rearrangement called a Robertson- carrying 28, the offspring are infertile.
drive “might have a fairly significant input ian translocation, common in both humans “This is really evolution working fast,” says
on behavior,” concludes Laurence Hurst, a and mice. In some individuals, two chromo- Pardo-Manuel de Villena.
genetic evolutionary biologist at the Univer- somes merge to form a single long one—
sity of Bath, U.K.
causing the total number in humans to drop Genetic weaponry
In addition to luring more females, stalk- to 45 from 46. In 1991, Sapienza and Pardo- Gradually researchers are homing in on the
eyed males without the driver genes have a Manuel de Villena reported that such identity of drivers and the strategies that let
second defense, Wilkinson’s graduate stu- translocations could foster meiotic drive in them proliferate more than other DNA.
dent Catherine Fry reported at the Evolution females. The Siamese-twin chromosome, Pardo-Manuel de Villena’s lab is now busy
meeting. She mated the same female with with its sole working centromere, somehow searching for genes involved in meiotic
males that carried the driver and other males gets the jump on the two individual chro- drive in mammals. In one case, “we have
that didn’t. When sperm from both are in the mosomes during meiosis and is more likely mapped the first gene to a region of 200,000
bases,” he says. They must check out the
female reproductive tract, “less than 10% of to survive.
the offspring are fathered by the [male with
The reduced chromosome number thus functions of the half-dozen genes in that rethe] driver,” says Wilkinson. Fry’s work becomes ever more common: In humans, gion to pinpoint the right one. Driver strategies vary from species to species,
indicates that seminal fluid from
but usually a malfunctioning prothe nondriver male is toxic to the
tein is involved.
driver male’s sperm.
It doesn’t take much to mess
Meiotic drive can affect another
up chromosomal inheritance, Barbehavioral aspect of mating behavry Ganetzky, a geneticist at the
ior, says Jeanne Zeh. During the
University of Wisconsin, Madi1990s, she and her colleagues began
son, and his colleagues reported
studying paternity patterns in
in the 14 May 2002 issue of the
a strange arachnid—a pseudoscorProceedings of the National
pion—that hitches rides on the abAcademy of Sciences. A signaling
domens of harlequin beetles. “The
molecule called ranGAP helps
results were quite unexpected,” she
transport molecules into and out
recalls. Females, which brood their
of the nucleus. His team had alyoung in translucent sacs carried
ready shown that mutated forms
under their abdomens, mated with
of this protein spell trouble for dean unusually large number of males.
veloping Drosophila sperm. But
In one case, there were four fathers
recently the researchers found that
for seven young. Moreover, females
even the normal protein distorts
that had just one or two mates
tended to abort their embryos.
Turf war. Pseudoscorpions, here dueling on a harlequin beetle, extend the inheritance of certain chromoZeh’s group studied the litera- their rivalry to within the female reproductive tract. Multiple matings somes if it is present in excess. In
this case, a driver gene—possibly
ture and found that spontaneous by females may counteract driver or suppressor genes.
just a second copy of the fruit fly’s
abortion is common soon after fertilization, particularly in mammals and live- for example, “a female with 45 chromo- ranGAP gene—increases the amount of
bearing arachnids. She blames incompatibil- somes has more offspring with 45 than with ranGAP in competitor sperm, which is
ity between the male and female contribu- 46,” Pardo-Manuel de Villena points out. enough to cause problems.
Prions, too, get caught up in intragenomic
tions to the offspring’s genome, some of Males with this reduced number of chromowhich may be caused by driver or suppres- somes father equal numbers of offspring conflict, Henk Dalstra of Wageningen Unisor genes. To hedge against losing her em- with 45 and 46 chromosomes, indicating versity, the Netherlands, and his colleagues
bryos, the female has evolved to take sperm that the chromosomal competition is being reported earlier this year. Spores produced
from multiple males into her reproductive played out in eggs rather than sperm. He during the sexual phase of reproduction in
tract. There the immune system weeds out thinks that meiotic drive at Robertsonian the filamentous fungus Podospora anserina
unsuitable sperm, Zeh speculates.
translocations might explain why humans contain either an allele that prompts prion
Although studies such as these follow have two fewer chromosomes than chimps. formation or one that codes for a normal
the effects of meiotic drive on the natural And it might help explain why in some Eu- protein. Spores containing the prionhistory of organisms, geneticists Fernando ropean mice, as other geneticists have forming allele somehow get rid of spores
Pardo-Manuel de Villena of the University shown, the chromosome number has with the other allele, they reported in the 27
of North Carolina, Chapel Hill, and Car- dropped from 40 chromosomes 5000 years May 2003 issue of the Proceedings of the
National Academy of Sciences.
men Sapienza of Temple University in ago to 22 today.
The accumulation of examples of meiotPhiladelphia have been homing in on how
Sometimes the opposite process can also
meiotic drive affects evolution within the fuel meiotic drive. When a chromosome ic drive suggests that deep inside every indigenome. Meiotic drive in mammals, they’re breaks apart, causing an uneven distribu- vidual—and in more species than refinding, seems to shape the genome in a tion of centromeres, offspring may be more searchers realize—there’s a lot of conflict
different setting and through a different likely to inherit the newly enlarged set. going on. “It’s like kids at dinner,” Hurst exmechanism. Mammalian drivers bias inher- Here again meiotic drive seems to have in- plains. “Underneath that lovely perfection of
itance patterns by exerting their effects in fluenced speciation. For example, on the 50:50 sex ratio, there’s a lot of kicking
–ELIZABETH PENNISI
the egg; in insects, sperm bear the brunt of Madeira Island off Portugal, where mice under the table.”
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