SCIENTISTS' BOOKSHELF

The Dark Side of DNAFred Gould

GENES IN CONFLICT: The Biology of Selfish Elements. Austin Burt and Robert Trivers. x -i- 602 pp. TheBelknap Press of Harvard University Press, 2006. $35.

A lthough many of us have gotten usedto the idea that our bodies serve theneeds of a variety of viruses, bacteria,

mites and other parasitic species, it comesas a surprise to most people when they hearthat their bodies are also hosting alien para-sitic DNA.

Although typical morning glories are uniform in color {A, B),the insertion and excision of transposable genetic elements cancause variable "knockout" mutations in the gene for pigmentproduction, resulting in variegated flowers (C through F). FromGenes in Conflict.

Analysis of output from the Human GenomeProject makes it clear that just one form of suchalien DNA, transposons, makes up about 50percent of our genome. Every time one of yourcells divides, it uses time and energy to repli-cate this parasitic DNA. There is even evidencethat the size of your cells is set to accommodatethis extra genetic load. In return, this type ofDNA typically does nothing useful for you orany of the other organisms it inhabits.

So why do humans and the vast majorityof other species serve as homes for parasiticDNA? This is one of many questions aboutselfish genetic elements that Austin Burt andRobert Trivers address in their scholarly,thought-provoking new book. Genes in Con-flict. As can be gleaned from the title, the au-thors don't envision an easy alliance betweenselfish genes and the rest of the genome.

As background, it is worth noting that all spe-cific sequences of DNA manage to persist overtime by causing their host organisms to keeppassing them on to their progeny. There are twobasic evolutionary mechanisms that DNA se-quences use to improve their odds of gettinginto that next generation. The first method in-volves increasing the number of viable offspringproduced by the host relative to competing indi-viduals. This process fits within our typical un-derstanding of adaptation and natural selection.

The second evolutionary mechanism is fora DNA sequence somehow to increase the per-centage of the host's offspring in which it is con-tained. A DNA sequence that is represented byone copy in a diploid sexual organism is general-ly expected by Mendelian principles to be inher-ited by 50 percent of progeny If a DNA sequencecan manage to wind up in, say, 90 percent of theoffspring, it has a greater chance of persistingover time—even if that DNA sequence causesa decrease in fitness. Burt and Trivers considergenetic elements that use this second strategy tobe "selfish DNA." Of course, there is a balanc-ing act here, because if the negative impact onfitness is too great, the host species could goextinct, taking the selfish DNA with it.

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Over time, numerous types of genetic ele-ments have evolved diverse parasitic strategiesfor proliferation in genomes and, as a result,have become very abundant in many organisms.But some species appear to lack selfish DNAof any kind. Whenever selfish DNA reducesfitness, natural selection will favor any mutantgene that decreases the probability of that selfishDNA being passed on. Burt and Trivers providea long list of examples demonstrating a coevolu-tionary battle between selfish genetic elementsand genes that negate their impact. In some spe-cies it seems that the selfish DNA is winning; inothers it is taking a beating.

The dynamics of "gamete killer" genetic ele-ments in the fungus Neiirospora, and genes forresistance to these gamete killers, illustrate thiscoevolutionary tug-of-war. Neurospora has abrief diploid phase of its life cycle. This stageis followed by three cell divisions—^two mei-otic and one mitotic—giving rise to eight hap-loid spores arranged in a neat row. Researchersfound that when they made genetic crossesbetween two particular strains of this fungus,four of the resulting eight spores in a set werealways dead. Genetic analysis revealed that oneof the strains, called the gamete-killer strain,has a tightly linked set of genes that somehowkills the four spores in which it was not present.The current hypothesis is that during spore for-mation, one or more of the gamete-killer genescode for a toxic substance, which is depositedin all of the forming spores. Four spores cansurvive, though, because they inherit genesfrom the killer strain that neutralize the toxin.

The important result here is that the gam-ete-killer genes wind up in 100 percent of theviable spores instead of just 50 percent. If evenone spore in a population had this set of genes,it would in some situations be expected to in-crease in frequency until it was carried by allindividuals, despite the substantial decrease inreproductive capacity experienced when onlya minority of spores carry these genes.

A survey of Neurospora populations aroundthe world found that these gamete-killer genotypes are typically rare but can indeed reacha frequency of 100 percent in populations ofsome species. Genes that confer resistance tothe gamete killers are typically more commonthan the killer genes. Once a resistance geneenters a population and negates the abilityof the killer genes to be over represented inprogeny, the killer genes are selected against ifthey cause fitness reduction. So in the case ofNeurospora, the selfish DNA seems to be losingthe coevolutionary battle.

These gamete-killer genes, which are alsofound in invertebrates and vertebrates, are justone form of selfish genetic element, and theyare far from the most diverse type. Transposons,sometimes called "jumping genes," are foundin a wide array of taxa and vary dramatically

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554 EINSTEIN'S JURY: The Race to Test Relativity. By Jeffrey Cretinsten.Reviewed by Suman Seth. Einstein loas catapulted to fame when ob-servations of bending starlight gathered during a 1919 eelipse verifiedhis tlieory of general relativity. But tfiat experimental confirmation wasnot nearly as clear-cut as many people believe

556 ARTHUR CAYLEY: Mathematician Laureate of the Victorian Age.By Tony Crilli/. • JAMES JOSEPH SYLVESTER: Jewish Mathemat-cian in a Victorian World. By Karen Hunger Parslmlt. Reviewed byDaniel S. Silver. For a time, these highly regarded mathematicians oflSth-eentury Britain, pioneers in the development of linear algebra, hadday jobs as lawyers

559 THE FIRST HUMAN: The Race to Discover Our Earliest Ancestors.By Ann Gibbons. Reviewed by Jeffrey K. McKee. Tlie attentiongiven to high-profile animosities among paleoanthropologists obscuresthe fact that cooperation is just as prevalent as competition

561 IN SEARCH OF MEMORY. By Eric R. Kandel. Reviewed by LarryR. Squire. This scientific memoir of a Nobel laureate reveals how thestudy of psychology in the wake of Freud gave luay to a focus on thevarious cellular and molecular mechanisms operating in the brain

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564 THE RELUCTANT MR. DARWIN: An Intimate Portrait of CharlesDarwin and the Making of His Theory of Evolution. By DavidQuammen. Reviewed by Bettyarm Holtzmann Kevles. hi thisconcise biograp^hy, acclaimed science writer David Quammen examineswhy it took Darwin so long to publish his revolutionary ideas

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567 ONE PLANET: A Celebration of Biodiversity. By Nicholas Huht.Reviewed by Roger Harris. This collection of images highlights whatloe stand to lose every time another species disappears

568 TECHNOLOGY MATTERS: Ouestions to Live With. By David E.Nye. Reviewed by David M. Hart. An enlightening—and madden-ing—text tliat introduces some of the most important debates in thefield of history of technologi/

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571 NANOVIEWS. Short takes on three books: How Everything Works •Another Day in the Frontal Lobe • The Structure and Dynamicsof Networks

www.americanscientist.org 2006 November-[)ecember 553

in the mechanisms they use to becomeoverrepresented in offspring. Burt andTrivers devote an entire chapter to trans-posons, which are able to replicate them-selves within a genome and move tonew locations on the chromosomes. Anindividual organism can start life withone copy of a transposon and end upwith two or more in its germline cells.

Barbara McClintock discoveredtransposons in 1952, but the first self-ish genetic elements revealed them-selves as early as 1906. And new formsare still being found. A challenge to re-searchers is to think creatively enoughto anticipate what an as-yet-unde-scribed selfish element might look likeand how to design experiments for itsrecognition. Burt and Trivers discussa wonderful example of this creativethinking by the renowned evolution-ary biologist George Williams, who in1988 wrote.

Perhaps it is just a matter of timebefore someone discovers (or in-vents in the lab) an all-male spe-cies. It makes diploid sperm thatinseminate eggs of related spe-cies and give rise to diploid nucleithat exclude the egg pronuclei.

This would seem to be the ultimatein parasitic DNA—an entire eukary-otic genome that has no body of itsown, surviving only by stealing theeggs of a related species in each gen-eration. Although it may seem to be

Crossing normal Netirospora with the gam-ete-killer strain of this fungus produces arosette of spores. Each linear appendage con-tains eight spores, only four of which carrythe set of gamete-killer genes. The presenceof these genes somehow allows those fourspores to remain viable (black). Evidently,this set of genes codes for both a toxic sub-stance, one that gets into all eight spores ear-ly on, and its antidote, which is present onlyin the four spores containing this special setof genes. From Genes in Conflict.

the subject matter for a science-fictionnovel, this type of system was recentlydiscovered in a clam, a conifer and astick insect. Very cool!

But these examples are only the tipof the iceberg. In their 602-page opus,Burt and Trivers provide a plethora ofexciting case studies. Although there isno lack of data to discuss, the authorsemphasize repeatedly how little wereally know about this area of evolu-tion and biodiversity.

I found the tone of this book to bevery engaging. It is full of details thathave been woven together into a veryreadable, well-organized package. Ofimportance for the nonspecialist read-er, Burt and Trivers succeed in convey-ing complex concepts in populationgenetics without using mathemati-cal equations. Detailed mathematicaltreatment of these topics is certainlywarranted, but that will be anotherbook. The authors clearly reveal theirattitude in the first chapter:

We review the evidence in moredetail than we can make senseof and we describe logic beyondwhat the evidence will verify. Ouraim is to strike a balance betweenwhat is known and what is not,the better to invite others to join ingenerating the missing logic andevidence.

What a gift to graduate studentsand all researchers who are just enter-ing this field of evolutionary biology!I found at least a dozen good projectsfor Ph.D. theses suggested within thepages of this book, and I am sure thatthere are many more.

Fred Coiiid is a professor in tlir Deimrtments of En-

tomology and Genetics at North Carolina State Uni-

ivrsity. His current research is focused on assessing

how naturally occurring and artificially engineered

selfish genetic elements can be used for controlling or

altering pest populations.

HISTORY

Paradigm LostSuman Seth

EINSTEIN'S JURY: The Race to Test Relativity. Jeffrey Crelinsten. xxx + 397 pp. PrincetonUniversity Press, 2006. $35.

In a letter written on February 6,1920, astronomer Keivin Bums ofCalifornia's Lick Observatory ex-

pressed his doubts about Einstein'sgeneral theory of relativity. "Of courseno one at Lick believes in the Einsteineffect," he wrote, referring to the gravi-tational redshift in spectroscopic linespredicted by the theory, "it being con-trary to philosophy, judgment, andhorse sense. But since so much is beingsaid on the subject it is necessary to beinterested. It may take a long while to

show the error of the ways of the Eng-lish astronomers."

The timing, location and subject ofBums's epistle are all central to our un-derstanding of the early reception andtesting of one of the pillars of modemphysical theory. Most popular accountsof Einstein's theory tend to depict the1919 eclipse expedition, led by ArthurStanley Eddington, as the crucial testfor general relativity. Eddington's an-nouncement that the patKs of starlightwere deflected or "bent" by the Sun's

gravitational field by almost exactly theamount predicted by the theory wasmet with incredulity and amazementamong scientists and sparked an inter-national press furor. Within two weeksof the first media reports, the Britishhumor magazine Punch recorded inlines of doggerel that an English "pa-triot" had been forced to write a fu-neral march, "To record, as he said, thata Jewish-Swiss-Teuton / Had partiallyscrapped the Principia of Newton."

As Jeffrey Crelinsten's crisply writ-ten and impressively researcheci bookshows, however, the "patriot fiddler-composer of Luton" gave up his faithin Newtonian physics long beforeAmerican astronomers were convincedto do so. The ongoing skepticism of theAmericans was to have real import, forin the 1920s it was increasingly to theLick and Mount Wilson observatories,both in Califomia, that European and

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