Solved by a verified expert:The article “How Beach Life Favors Blond Mice” talks about the genetics behind the evolution of coat color in mice on beaches in the Florida panhandle. What is the selective force thought to drive the change in coat color? What genes are involved in this evolutionary change? Why is it thought that starting with a dark coat color, the mutations leading to the light “beach” coat would have to happen in a certain order? What violations of Hardy-Weinberg equilibrium would be involved in going from the dark inland coat to the light coat?How Beach Life Favors Blond MiceSand Hills of Nebraska (Science, 28 August,p. 1095). “We’re finally at the point wherewe can start to identify the genes responsiblefor phenotypic variation,” says Hoekstra.And while working in Arizona, she says sheIn June, at a meeting in Cold Spring Harpicked up far too many “presents” bulging with bor, New York, Hoekstra described the thirdan angry rattlesnake. Fortunately, this trap of the three genes responsible for coat-colorweighs too little to have a snake inside, and no variation in Peromyscus mice and laid out herdeadly spiders are expected.view of the order in which mutations leadingIn a line of about 100 traps, Hoekstra to paler mice occurred. “We’re trying toretrieves eight mice; her companions turn up reconstruct the evolutionary path, genetic stepfour more, not a bad take for a full-moon by genetic step,” she says. “Understandingnight, when mice tend to be less active.how characters evolve is a critical question,The mice are part of a project started 6 years and she is bringing a significant contribution,”ago to figure out the genetic changes that says developmental geneticist Claude Desplanunderlie adaptations these animals make to the of New York University. He adds that her workworld around them. Biologists have long mar- demonstrates that “one can really identifyveled at how oldfield mice living on beaches evolving traits.”are much paler than those living inland, andHoekstra and her team are part of aHoekstra is searching for pigment genes genomics explosion in natural history studresponsible for the color variation.ies. “This is an example of workShe’s combining molecular, devel… merging the ‘green’ andopmental, genetic, and ecological‘white’ side of biology, in whichapproaches, including putting sciencemag.orgwe learn about trait evolutionthousands of clay decoys onfrom the biochemical levelsPodcast interviewbeaches to test the effects of coatwithin cells to how those traitswith authorcolor on predation risk and map- Elizabeth Pennisi.are selected for or against in natping genes and testing pigmentural populations,” says Hansprotein function in cell cultures. “We’re attack- Ellegren, an evolutionary biologist at Upping the system from all sides,” says Hoekstra.sala University in Sweden. Mark McKone, aOn this trip, Hoekstra and her team are biologist at Carleton College in Northfield,looking not just at coat-color variation but Minnesota, agrees: The work “could be aalso at variation in burrow-building. Most model for how to approach evolution in thedeer mice build short, shallow burrows; old- postgenomic period,” when genetic inforfield mice go for deeper, longer ones. Back mation and tools are more readily available.in the lab, Harvard graduate student EvanKingsley is trying to pin down the genetics New tools, classic modelof tail length: Mice in forests have longer Hoekstra’s team represents the latest genertails. Recently, Hoekstra postdoc Catherine ation of researchers tracking down genesLinnen described a genetic change under- that underlie so-called quantitative traitslying light-colored deer mice that match the such as height or body mass, which—FREEPORT, FLORIDA—It’s a hot, stickyJuly night here in western Florida, but toHopi Hoekstra, it feels like Christmas Eve.Hoekstra, a Harvard University evolutionarybiologist, and her field crew have set outmore than 400 small metal boxes, throwing ahandful of sunflower seeds into each boxbefore setting it on the ground, usually nextto a mound of sand representing the debrisfrom a mouse burrow. When she inspectsthese live animal traps the following morning, she says it will be like “unwrappingpresents.” Her eagerness is palpable.“You’re going to be blown away by thisfield,” graduate student Jesse Weber had toldHoekstra when they first drove down a sandroad into the Lafayette Creek Wildlife Management Area, a 13-square-kilometer expanseof overgrown fields kept open in part by controlled burns. Never before had Weber andHarvard postdoc Vera Domingues seen such adense concentration of burrows dug by theoldfield mice, Peromyscus polionotus, thatthey study.By 7:30 the next morning, Hoekstra,Domingues, Weber, and Harvard undergraduate Diane Brimmer are making theirway from trap to trap, sidestepping fire anthills, prickly pear, and thorny vines while keeping an eye out for pygmy rattlers. Typically, thetrapdoors are still ajar, and at most a grasshopper or two jumps out into Hoekstra’s face asshe empties the sunflower seeds. But three trapsdown the line, the door is closed and Hoekstrasenses something inside. At past field sites,she’s had to worry about lethal spiders crawlingin, positioned to nab any unsuspecting hand.133011 SEPTEMBER 2009OnlineVOL 325SCIENCEPublished by AAASwww.sciencemag.orgCREDITS (LEFT TO RIGHT): SHAWN CAREY/MIGRATION PRODUCTIONS; J. B. MILLER/FLORIDA PARK SERVICEA young evolutionary biologist tackles the genetic complexity of aclassic case of adaptation in miceDownloaded from www.sciencemag.org on October 6, 2009NEWSFOCUS Lighten up. Several genes transformed mainlandmice (left) into paler beach mice that blend in betterwith their environment.unlike, say, eye color—vary by degree andare influenced by multiple genes. It ispainstaking work.Researchers home in on such genesthrough intensive breeding studies combined with careful analysis of trait characteristics: spots, stripes, and so on for coat color;depth, length, and angle for burrowingbehavior. They correlate the traits with specific markers in genetic maps to pinpointstretches of DNA known as quantitative traitloci (QTLs) that contain the genes of interest. “This is done well in insects but is muchmore difficult in mammals,” says Desplan.Over the past 20 years, several studies haveidentified QTLs in mammals, but few havemanaged to narrow the search to specificHer animal of choice is a textbook case ofadaptation. Peromyscus mice are distant relatives of house mice. For more than a century,researchers had observed them in the wild,describing their looks and behaviors. In 1909,light-colored P. polionotus were discoveredon Florida’s barrier islands, a sharp contrastto dark-brown, gray-bellied mainland mice ofthe same species. Some 6000 years ago, darkoldfield mice moved into these newly formedbeaches and islands. Today, eight subspeciesof these light-colored P. polionotus exist onFlorida’s coasts.In the late 1920s, natural historian FrancisSumner guaranteed P. polionotus a place inthe textbooks when he drove from Florida’sGulf Coast inland 150 kilometers collecting mice in eight places along the way, noting a correlation between soil and mousecolor. When he started, he was convincedthat humidity caused the variation in color.light areas of their bodies, traits duly noted foreach individual. This variation indicated thatmore than one gene was involved, but becausethe second generation still contained somemice that looked like the parents, Hoekstraknew that relatively few genes were important. “It wasn’t one, it wasn’t 100,” Hoekstrarecalls. So she decided to go after them all.Weber and Cynthia Steiner, now at theSan Diego Zoo Institute for ConservationResearch in California, developed andapplied a set of more than 100 microsatellitemarkers, small pieces of variable DNAlocated across the genome. They correlatedthe markers with the presence or absence ofthe various color pattern traits. That workyielded three hot spots—QTLs—that seemedto determine what the mice looked like.The researchers looked at the sequences ofthe house mouse and rat genomes for pigmentrelated genes at those locations and foundDISTRIBUTION OF BEACH AND MAINLAND MICEMainlandmouseLafayette CreekmiceSanta Rosa Islandbeach mouseAnastasia Islandbeach mouseAlabamabeach mouseLOCATIONPerdido Keybeach mouseChoctawhatcheebeach mouseSt. Andrewbeach mousePallidbeach mouse**extinct subspeciesSoutheasternbeach mouseCREDIT: ADAPTED FROM C. STEINER ET AL., MOL. BIOL. EVOL. 26, 35 (2009), FIG. 1Mouse of a different color. Mice from different locales have evolved site-specific coat colors, except those at Lafayette Creek, which have a variety of pelt patterns.genes, let alone identify mutations thatresult in changes such as coat color.The discovery in 2005 by David Kingsleyof Stanford University in Palo Alto, California, and colleagues that a change in theectodysplasin gene led to the loss of armor infreshwater sticklebacks (Science, 25 March2005, p. 1928) “got the field excited,” saysHoekstra. It was the first QTL study usingnatural populations to come up with a genethat was not already suspected to beinvolved and, later, to pin down its mutation.Hoekstra hopes to go into more detail withher mouse studies. Whereas Kingsleyfocused on the gene with the biggest effect,she is searching for several genes. “If weidentify multiple genes and understand theinteractions between those genes, we canalso learn something new about evolutionary processes,” she explains.By the project’s end, he was more convinced that genetics caused the differences,driven by selection for camouflage. “It’sone of the best studies of intraspecific variation,” says Hoekstra.Giants in evolutionary biology, includingErnst Mayr, Theodosius Dobzhansky, JohnMaynard Smith, J. B. S. Haldane, and SewallWright, have cited the work as a classicexample of adaptation. Others followedSumner, looking at various aspects of beachmice ecology, but they were unable to pindown the genetics. Hoekstra saw an opportunity: “We now have the molecular tools toanswer the questions that they were askingmore than a half-century ago.”She and her colleagues bred dark and lightmice, then generated 800 second-generationoffspring. These hybrid mice differed in theirstripes and splotches and the extent of dark orwww.sciencemag.orgSCIENCEVOL 325Published by AAASDownloaded from www.sciencemag.org on October 6, 2009NEWSFOCUSpromising candidates. One was Mc1r, whichcodes for a receptor protein in pigmentproducing cells. Hoekstra was at first skeptical. In her studies of black pocket mice on volcanic rock in Arizona, one version of that genewas responsible for the black mice and anotherfor light mice; it was not clear how the genemight play a role in determining fine detailssuch as nose blazes and tail stripes.But not only did they prove that Mc1r wasinvolved, they also found a single-basechange that led to an amino acid mutation thatdampened receptor activity (Science, 15 July2005, p. 374; 7 July 2006, p. 101). A secondcandidate gene, Agouti, panned out as well.In this case, the versions of the gene in darkand light mice were identical; yet the gene inbeach mice was much more active, leadingto much more messenger RNA and presumably protein that reduced dark-pigment pro-11 SEPTEMBER 20091331 NEWSFOCUSMouse maven. Hopi Hoekstra combinesmolecular and field expertise to studythe genetics of wild mice.1332laboratory mice, made for dirty-blond mice.Corin was also active in the hair follicles ofoldfield mice, Hoekstra reported in June at“Evolution: The Molecular Landscape” inCold Spring Harbor. The gene in light anddark mice was almost the same, but it wasmuch more active in light mice. Thus, aswith Agouti, a change in regulation may bekey to the change in coat color.In the simplest scenario, the effect ofthese genes would be additive: Two “light”versions of the variable genes would lead to apaler mouse than one version would, and the11 SEPTEMBER 2009VOL 325SCIENCEPublished by AAASpalest mice would have “light” versions of allthree. But that’s not the case with Agouti,Corin, and Mc1r. These genes have epistaticinteractions: A “dark” Agouti version counters any lightening effect of a “light” Corinor Mc1R, for example.These epistatic effects can dictate theorder in which alleles in a population mustpop up in order to be selected for and spread.“You need to have the agouti allele first,”says Hoekstra, because the “light” versionsof Corin or Mc1r would be invisible to selection if only the “dark” agouti were present.www.sciencemag.orgCREDIT: E. PENNISI/SCIENCEduction, particularly in the cheeks, tail, andeyebrows, Hoekstra, Weber, and Steinerreported in 2007.They had a false start with the thirdregion identified in the QTL studies. Harvard graduate student Emily Jacobs-Palmereventually ruled out several pigmentationgenes, including a promising one called Kitthat turned out to lie outside the QTL. Thenlast year, Bruce Morgan of Harvard MedicalSchool in Boston and his colleaguesreported that mutating a gene called Corin,which was expressed in the hair follicles ofDownloaded from www.sciencemag.org on October 6, 2009Park. She studied the biomechanics of invertebratesthroughout the school year. During that time, JamesPatton, curator of mammals at the Berkeley Museum ofVertebrate Zoology, got her hooked on four-legged furrycreatures by taking her to trap gophers in Arizona. Andbefore starting graduate school, she spent 3 months asshipboard mammalogist on a joint Japanese, Russian,and American expedition to collect animals in theKuril Islands off Russia.Her Ph.D. dissertation at the University of Washington, Seattle, involved months of fieldwork in the Andestracking down a sex chromosome polymorphism in mice.Some females seemed to have both a big and a small X,which later proved to be a Y chromosome, even thoughthese females were completely fertile, producing moreyoung than the typical female with two X chromosomes.“This was an oddball system,” Hoekstra recalls. Afterward, “I got interested in more general questions.”Fascinated by the genetics underlying adaptation,Melding Mammals and Molecules to Track Evolutionshe spent her postdoc trapping black mice on ancientArizona volcanoes and tracking down the gene responsiSelf-described as a bubbly California girl, Hopi Hoekstra entered the Uni- ble for the change. In these field studies, she developed a yen for herversity of California, Berkeley (UCB), not thinking about being a scientist. camp meal of choice: cold SpaghettiOs and mini meat balls straight fromHer goal was to become the U.S. ambassador to the Netherlands—both her the can, with a Miller Light.parents are Dutch—and an accomplished collegiate volleyball player. ThenShe considers herself a molecular person: “We’re interested in the molshe got her first summer job: Dressed in white, she hiked the Berkeley Hills ecules that are important to the organism,” she says. Yet she also knowsjust east of campus, a tick target for researchers assessing where and when just how much cornmeal it takes when skinning a mouse to ensure the pelthikers were most susceptible to attacks by Lyme disease–transmitting ticks. won’t be greasy and that shrews have fragile skin that’s hard to pull off.“It still makes me itch just to think about it,” she says.The breadth of projects include an analysis of shrew venom proteinsBut the experience made Hoekstra itch for more fieldwork and, even- and a collaboration on a genetic study of mice in Bulgaria that seem totually, a life as a biologist. Two years ago, she moved from the University cooperate to build large mounds that they coinhabit to get throughof California, San Diego, to Cambridge, Massachusetts, as a Harvard Uni- harsh winters.versity evolutionary biologist. She is also currently curator of mammals at“Being able to be a molecular biologist and be comfortable with theHarvard’s Museum of Comparative Zoology. Although only in her mid- whole organism—few people do that as well as Hopi, and that’s where30s, “Hopi has rapidly made herself a name in the evolutionary biology progress [in the field] will be made,” says Mark McKone, a biologist atcommunity,” says Hans Ellegren of Uppsala University in Sweden. Her Carleton College in Northfield, Minnesota. “When you put [her research]honors include a young investigator award from the Arnold and Mabel together, it’s more than the sum of its parts.”Beckman Foundation and prizes from her professional societies and herHoekstra doesn’t get out into the field much anymore. Instead, sheuniversities. “She’s just about one of the deepest thinkers in the area,” lives vicariously through her students and postdocs, with the goal of spendsays Carlos Bustamante of Cornell University, who adds that her beach ing time at least once with each of them in the field. “When they have amice experiments “are beautifully thought out and designed.”really good day, they call and leave a message,” she says, or send a photoShe traces her professional roots back to her UCB experience, where from their phones, such as an image of 44 traps stacked up against a brickshe managed to do research almost year-round, even as an undergraduate. wall, signaling that their trapping yielded a bonanza. “They just send a picOne summer, she analyzed pack rat middens in Yellowstone National ture [without words] because they know I know what it means.”–E.P. CREDIT: E. PENNISI/SCIENCEBurrowing inWeber has taken on an even more challengingproject: using these mice to look at the genetics underlying burrowing behavior. “It’s pathbreaking work on the evolution of behavior ina natural environment,” says field biologistPeter Grant of Princeton University. “QTLstudies are widespread in general but rare inbehavior studies of organisms in nature.”Unlike coat color, almost nothing isknown about genes that might guide burrowing. Yet oldfield mice and their sister species,deer mice, differ dramatically and, it seems,consistently in the burrows they build. Thelatter tend to knock off their digging less than10 centimeters down. Oldfield mice shoveldown 1 meter, even 2, hollow out a nest chamber, and then excavate an escape tunnel thattends to shoot directly back up to just belowHere in Freeport, he’s doing someground-truthing. He catches the mice in theburrows so he can correlate their DNA withthe tunnels’ dimensions. He picks what lookslike a freshly dug hole, shovels out some dirt,then drops to his knees to scoop the sand andclay away with his hands until he sees around, light-colored spot in the wall of thehole. His f inger easily pokes through it,revealing it to be a plug of sand blocking theburrow tunnel. Alternating between shoveling and scooping and probing the tunnel witha long, flexible, plastic tube(sprinkler tubing), he excavatesthe tunnel, eventually breakingBagging burrows. The beach micefield crew measures a mouse burrowinto a widened area filled withafter making a cast of its tunnels.nesting material. “This nest isgigantic,” he says.He confers with Hoekstraabout where she should stand inanticipation of mice emergingfrom the invisible escape hatch.She shifts to the right a halfmeter, then bends her legsslightly, hands on her knees. Shelooks like the volleyball playershe used to be, expecting aserve, except she’s lookingdown, not up.Weber pokes the tubing in alittle farther. Suddenly, two headspop up about 20 centimeters toHoekstra’s right. She dives toclamp her gloved hands over theheads. But as she peeks throughher f ingers, one dashes outbetween her legs, and the otherheads full speed in the oppositedirection. Both she and Weberpursue that one, darting fromthe surface. The mice plug up the burrow bush to bush after the mouse until finallyabout 15 centimeters from the entrance, seal- Weber has it in hand. The other is long gone.ing themselves safely in underground.While Weber measures the size andBack in the lab, Weber has filled 10 boxes, shape of the burrow, Hoekstra measures theeach 122 cm by 152.5 cm by 92.5 cm tall, sacrificed mouse, then dissects out its liverwith 1.5 tons of premium playground sand. to save for DNA tests, removes the skin toHe has crossed oldfield with deer mice, then mount the pelt for future studies of the colorcrossed their offspring back with either par- pattern, and saves the skeleton for theent, and he’s looking at what sorts of burrows museum’s collections. The sun sets brightthese backcrossed progeny dig. The distribu- red in front of her, and the full moon is a bigtion of burrow sizes in this second generation white ball in the sky behind her.will provide a rough indication of how manyWeber and Hoekstra seem tired but congenes are involved in determining burrow- tent. The burrows they’ve dug up wereing behavior. Weber squirts household insu- deeper and longer than usual; shovelinglating foam from a spray can down the bur- heavy, wet sand was tough going. They’verows. The foam expands to fill the nest and been up since before dawn and have anpassageways and hardens to provide a three- evening of setting traps ahead of them.dimensional model of the burrow. So far he’s “But once in a while, it’s good if it’s hard,”tested 200 mice and has partially filled the Hoekstra says. “Then you appreciate itattic of the Museum of Comparative Zoology when it’s easy.”with casts of their burrows.–ELIZABETH PENNISIwww.sciencemag.orgSCIENCEVOL 325Published by AAAS11 SEPTEMBER 2009Downloaded from www.sciencemag.org on October 6, 2009By backcrossing the second-generationmice with their parents and f iguring outwhich version of each of the three genes theoffspring had, Hoekstra’s team was able totease out the interactions among the genes.The light-mouse version of Corin lightensthe coat only when the light-mouse versionsof both of the other genes are also present,Hoekstra reported. Thus, it is likely thatgenetic change in Corin occurred after thechanges to Mc1r and Agouti.Meanwhile, Domingues and graduatestudent Lynne Mullen are tryingto track down the exact basechanges involved in the Agoutiand Corin regulatory regions.Working with postdoc BrantPeterson, they are figuring out away to sequence 200,000-basechunks surrounding each of thesegenes in multiple individuals.They plan to scan for differencesthat correlate with coat color patterns. “We will probably see lotsof differences,” says Hoekstra.“The question is, ‘What are theimportant ones?’ ”The work Domingues is doinghere might help answer thatquestion. The landscape is dottedwith spots of white sand sparselybroken up by vegetation amidfields solidly covered with lowbush and plants, and in a fewplaces, meter-tall trees havetaken hold. When local fish andwildlife managers first directedher to this spot, Dominguesexpected the mice to be uniformly dark, but quite a few hadbeachlike features.Hoekstra and Domingues eagerly discussthe pelage of each catch. How far a darkstripe extends down the tail, the expanse ofwhite on the cheeks, the presence of a noseblaze all matter, as they signal somethinginteresting going on in the genetics of thesesupposed-to-be-dark mainland mice.Domingues plans to try to pin down thegenes—and mutations—involved in all thevariation she sees, using the three genesimplicated in beach mouse paleness as ajumping-off point.1333
Expert answer:The article “How Beach Life Favors Blond Mice”
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