An Emerging Disease Causes Regional Population Collapse of a Common North American Bat Species


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An Emerging Disease Causes Regional Population Collapse of a Common North American Bat Species

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Title:
An Emerging Disease Causes Regional Population Collapse of a Common North American Bat Species
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Science
Creator:
Frick, Winifred F.
Pollock, Jacob F.
Hicks, Alan C.
Langwig, Kate E.
Reynolds, D. Scott
Turner, Gregory G.
Butchkoski, Calvin M.
Kunz, Thomas H
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English

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Wns ( local )
North America ( local )
Novel Disease ( local )
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serial ( sobekcm )

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White-nose syndrome (WNS) is an emerging disease affecting hibernating bats in eastern North America that causes mass mortality and precipitous population declines in winter hibernacula. First discovered in 2006 in New York State, WNS is spreading rapidly across eastern North America and currently affects seven species. Mortality associated with WNS is causing a regional population collapse and is predicted to lead to regional extinction of the little brown myotis (Myotis lucifugus), previously one of the most common bat species in North America. Novel diseases can have serious impacts on naïve wildlife populations, which in turn can have substantial impacts on ecosystem integrity.
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Science, Vol. 329, no. 5992.

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k26.3 ( USFLDC: LOCAL Handle )

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criticaltotesttheefficac yofspecificdiseasepreventionstrategiesappliednotonlywithindonor andrecipientcommunities,butalsointherealm wheretheyintersect.ReferencesandNotes1.J.O.Lloyd-Smith etal ., Science 326 ,1362 (2009). 2.C.E.Rupprecht,C.A.Hanlon,T.Hemachudha, Lancet Infect.Dis. 2 ,327(2002). 3.V.P.Hsu etal ., Emerg.Infect.Dis. 10 ,2082 (2004). 4.S.Riley etal ., Science 300 ,1961(2003). 5.A.Moya,E.C.Holmes,F.González-Candelas, Nat.Rev. Microbiol. 2 ,279(2004). 6.M.Anishchenko etal ., Proc.Natl.Acad.Sci.U.S.A. 103 , 4994(2006). 7.H.D.Song etal ., Proc.Natl.Acad.Sci.U.S.A. 102 ,2430 (2005). 8.C.R.Parrish etal ., Microbiol.Mol.Biol.Rev. 72 ,457 (2008). 9.T.Kuiken etal ., Science 312 ,394(2006). 10.J.D.Blanton,K.Robertson,D.Palmer,C.E.Rupprecht, J.Am.Vet.Med.Assoc. 235 ,676(2009). 11.D.A.Brass,in RabiesinBats:NaturalHistoryandPublic HealthImplications ,D.A.Brass,Ed.(LiviaPress, Ridgefield,CT,1994),pp.151 – 162. 12.J.S.Smith,L.A.Orciari,P.A.Yager, Semin.Virol. 6 ,387 (1995). 13.G.J.Hughes,L.A.Orciari,C.E.Rupprecht, J.Gen.Virol. 86 ,1467(2005). 14.O.R.P.Bininda-Emonds etal ., Nature 446 ,507 (2007). 15.Materialsandmethodsareavailableassupporting materialon Science Online. 16.D.M.deVienne,M.E.Hood,T.Giraud, J.Evol.Biol. 22 , 2532(2009). 17.G.S.Gilbert,C.O.Webb, Proc.Natl.Acad.Sci.U.S.A. 104 ,4979(2007). 18.T.J.Davies,A.B.Pedersen, Proc.Biol.Sci. 275 ,1695 (2008). 19.G.M.Baer,J.H.Shaddock,R.Quirion,T.V.Dam, T.L.Lentz, Lancet 335 ,664(1990). 20.S.Finke,K.K.Conzelmann, VirusRes. 111 ,120 (2005). 21.Forhelpfuldiscussionandcomments,wethankP.Beerli, J.Davies,S.Altizer,A.Park,P.Rohani,J.Allgeier, B.Han,P.Stephens,andthreeanonymousreviewers. Forcontributingrabidbats,wethanktheArizonaState PublicHealthLaboratory,theCaliforniaDepartmentof PublicHealth,theGeorgiaDepartmentofCommunity Health,theFloridaDepartmentofHealth,theIdaho DepartmentofHealthandWelfare,theIndianaState DepartmentofHealth,theUniversityofIowa ’ sUniversity HygienicLaboratory,theMississippiStateDepartment ofHealth,theNewJerseyDepartmentofHealthand SeniorServices,theTennesseeDepartmentofHealth, theTexasDepartmentofStateHealthServices,the VirginiaConsolidatedLaboratory,andtheWashington StateDepartmentofHealth.Forprovidingmuseumvoucheredbattissues,wethanktheAngeloStateNatural HistoryCollection,theCarnegieMuseumofNatural History,theCentrodeInvestigacionesBiológicasdel Noroeste,theLouisianaStateUniversityMuseumof NaturalScience,theMuseumofVertebrateZoology,the U.S.NationalMuseumofNaturalHistory,theRoyal OntarioMuseum,andtheUniversityofAlaskaMuseum. Thesequencesgeneratedinthisstudycanbefoundat GenBankunderaccessionnumbersGU644641to GU645012andGU722925toGU723257(tableS1). ThisworkwassupportedbyAssociationofPublicHealth Laboratories/CentersforDiseaseControlEmerging InfectiousDiseasesandNSFGraduateResearch FellowshipstoD.G.S.,NSF-NIHEcologyofInfectious Diseasegrant0430418toG.F.M.,andfundingfrom theU.S.ArmyEngineerResearchDevelopment Center – ConstructionEngineeringResearchLaboratory andWesternMichiganUniversitytoM.J.V.SupportingOnlineMaterialwww.sciencemag.org/cgi/content/full/329/5992/676/DC1 MaterialsandMethods SOMText Fig.S1 TablesS1toS9 References 26February2010;accepted10June2010 10.1126/science.1188836AnEmergingDiseaseCausesRegional PopulationCollapseofaCommon NorthAmericanBatSpeciesWinifredF.Frick,1,2* JacobF.Pollock,3AlanC.Hicks,4KateE.Langwig,4,1D.ScottReynolds,5,1GregoryG.Turner,6CalvinM.Butchkoski,6ThomasH.Kunz1White-nosesyndrome(WNS)isanemergingdiseaseaffectinghibernatingbatsineastern NorthAmericathatcausesmassmortalityandprecipitouspopulationdeclinesinwinter hibernacula.Firstdiscoveredin2006inNewYorkState,WNSisspreadingrapidlyacrosseastern NorthAmericaandcurrentlyaffectssevenspecies.MortalityassociatedwithWNSiscausinga regionalpopulationcollapseandispredictedtoleadtoregionalextinctionofthelittlebrown myotis( Myotislucifugus ),previouslyoneofthemostcommonbatspeciesinNorthAmerica.Novel diseasescanhaveseriousimpactsonnaïvewildlifepopulations,whichinturncanhavesubstantial impactsonecosystemintegrity.Emerginginfectiousdiseasesareincreasinglyrecognizedasdirectandindirect agentsofextinctionoffree-rangingwildlife( 1 – 4 ).Introductionsofdiseaseintonaïve wildlifepopulationshaveledtoseriousdeclines orlocalextinctionsofdifferentspeciesinthe pastfewdecades,includingamphibiansfrom chytridiomycosis( 5 , 6 ),rabbitsfrommyxomatosis intheUnitedKingdom( 7 ),Tasmaniandevilsfrom infectiouscancer( 3 ),andbirdsinNorthAmerica fromWestNilevirus( 8 ).Herewedemonstrate thatwhite-nosesyndrome(WNS),anemerging infectiousdisease,iscausingunprecedentedmortalityamonghibernatingbatsineasternNorth Americaandhascausedapopulationcollapse thatisthreateningregionalextinctionofthelittle brownmyotis( Myotislucifugus ),aoncewidespread andcommonbatspecies. WNSisassociatedwithanewlydescribed psychrophilicfungus( Geomycesdestructans )that growsonexposedtissuesofhibernatingbats, apparentlycausingprematurearousals,aberrant behavior,andprematurelossofcriticalfatreserves( 9 , 10 )(Fig.1).TheoriginofWNSand itsputativepathogen, G.destructans ,isuncertain( 9 ).Aplausiblehypothesisfortheorigin ofthisdiseaseinNorthAmericaisintroduction viahumantradeortravelfromEurope,basedon recentevidencethat G.destructans hasbeen observedonatleastonehibernatingbatspecies inEurope( 11 ).Anthropogenicspreadofinvasive pathogensinwildlifeanddomesticanimal populations,so-calledpathogenpollution,poses substantialthreatstobiodiversityandecosystem integrityandisofmajorconcerninconservation efforts( 1 , 2 ). WNShasspreadrapidlyandnowoccurs throughoutthenortheasternandmid-Atlantic regionsintheUnitedStatesandinOntarioand QuébecprovincesinCanadaandcurrentlyaffects atleastsevenspeciesofhibernatingbats(Fig.2). ManyspeciesofbatsintemperateNorthAmerica hibernateincavesandmines( 12 )inaggregations ofuptohalfamillionindividualsinasinglecave ( 13 ).Inlatespring,thesewinteraggregationstypicallydisperseintosmallersex-segregatedgroups ofconspecifics,whenadultfemalesformmaternitycoloniesandadultmalesmostlyroostalone ( 14 , 15 ).FromAugusttoOctober,femalesand malesassembleathibernaculaorswarmingsites tomatebeforehibernating( 16 , 17 ).Themechanismsforthepersistenceandtransmissionof G. destructans duringsummerandfallmonthsare unknown,butspreadofthefungustonewgeographicregionsandtootherspeciesmayresult fromsocialandspatialmixingofindividualsacross spaceandtime. Duringthepast4years,WNShasbeenconfirmedinatleast115bathibernaculainthe UnitedStatesandCanadaandhasspreadover 1200kmfromHoweCavenearAlbany,New York,whereitwasfirstobservedinFebruary 1CenterforEcologyandConserv ationBiology(CECB),DepartmentofBiology,BostonUniversity,5CummingtonStreet, Boston,MA02215,USA.2DepartmentofEnvironmentalStudies, UniversityofCaliforniaSantaCruz,1156HighStreet,SantaCruz, CA95064,USA.3DepartmentofEcologyandEvolutionary Biology,UniversityofCaliforn iaSantaCruz,1156HighStreet, SantaCruz,CA95064,USA.4EndangeredSpeciesUnit,New YorkStateDepartmentofEnvir onmentalConservation,625 Broadway,Albany,NY12233,USA.5St.Paul ’ sSchool,Concord, NH03301,USA.6WildlifeDiversityDivision,PennsylvaniaGame Commission,2001EmertonAv enue,Harrisburg,PA16669,USA. *Towhomcorrespondenceshouldbeaddressed.E-mail: wfrick@batresearch.orgwww.sciencemag.org SCIENCE VOL3296AUGUST2010679REPORTS

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2006( 9 )(Fig.2).Decreasesinbatsatinfected hibernacularangefrom30to99%annually,with aregionalmeanof73%,andallsurveyedsites havebecomeinfectedwithin2yearsofthediseasearrivingintheirregion(Fig.3,AtoC).Such sharpdeclinesandrapidspreadraiseseriousconcernsabouttheimpactofWNSonthepopulation viabilityofaffectedbatspecies. Weinvestigatedtheimpactsofdiseaseassociatedmortalityontheregionalpopulationof littlebrownmyotisinthenortheasternUnited Statesbycomparingtrendsinpre-andpost-WNS populationsandsimulating100yearsofpost-WNS populationdynamicstoassesstheconsequences oftheintroductionofthediseaseforbatpopulationviability( 18 ).Weusedapopulationmatrix modelparameterizedwithsurvivalandbreeding probabilitiesestimatedfrom16years(1993 – 2008) ofmarkandrecapturedataatamaternitysiteof littlebrownmyotis( 19 )toestimatepopulation growthbeforeWNS(tableS1).Wealsocalculatedgeometricmeangrowthratesfromwinter countsurveysofthisspeciesconductedoverthe past30yearsat22hibernacularangingacross fivestatesinthenortheasternUnitedStatesto determineregionalpopulationtrendsbeforethe emergenceofWNS(tableS2). Deterministicpopulationgrowthcalculated fromthepopulationmatrixmodelofmeanvital rateswaspositive[yearlypopulationgrowthrate ( l )=1.008],demonstratingthatpopulationgrowth wasstableorincreasingbeforetheemergenceof WNS.Estimatesoflong-termgrowthratesover thepast30yearsindicatethat86%ofhibernacula ( n =19outof22)hadstableorincreasingpopulations( l =>1).Regionalmeangrowthequaled 1.07(range:0.98to1.2)(tableS2),suggesting thattheregionalpopulationwasgrowingbefore WNSandthatvitalratesestimatedfromthe maternitysiterepresentregionalpatterns.The growthofhibernatingpopulationsoverthepast 30yearsmaybeinresponsetoconservationmeasures,suchasprotectivegatingofminesand caves( 20 ),theinstallationofbathouses( 21 ),and thepotentialameliorationofimpactsfrompesticidesbannedinthe1970s( 22 ). Toassesstheimpactofdisease-relatedmortalityonpopulationviability,wesimulatedpopulationdynamicsusingastochasticpopulation modelthatincludeddemographicdatafromboth infectedandsusceptible(uninfected)populations( 18 ).Weperformed1000simulationsof 100yearsofgrowthfromastartingpopulation of6.5millionbats,usingmeans,variances,and correlationsfromvitalrates( 19 )thatincorporated environmentalvariability( 23 ).Theprobabilityof extinctionforeachyearwasdefinedastheproportionof1000runsforwhichthesimulated populationdroppedbelowaquasi-extinction thresholdduringthatyear.Quasi-extinctionwas specifiedas0.01%ofthestartingpopulation(that is,650bats).Definingextinctionthresholdsat lowpopulationsizesaccountsforprocessessuch asdemographicstochasticityandpotentialAllee effects( 23 – 26 ). Inthesimulationmodel,thesusceptible populationretainedpre-WNSvitalratesestimatedfromthe16-yearmarkandrecapture data( 19 ),andinfectedpopulationsweregiven vitalratesassociatedwithannualdeclinescalculatedfrominfectedhibernaculawhereconsecutiveyearlycountswereavailable( n =22) ( 18 ).TheincreaseofprevalenceofWNSwas estimatedasthepercentageofuninfectedhibernaculathatbecameinfectedeachyear(2007, 5%;2008,49%;2009,59%)andwasincorporatedintothesimulationastheproportionof thesusceptiblepopulationthatbecomesinfected eachyear. Becauseoftheinherentuncertaintyinpredictingthedynamicsofarecentlyemergentdisease, weevaluatedthepotentialfordiseasefadeout anditsinfluenceonpopulationviability.Weestimatedannualdeclinesforeachof3yearsafter infectionandconstructednineapriorimodelsto testhypothesesregardingtheinfluenceofdensityandtimesinceinfectiononpopulationgrowth ratesatinfectedhibernacula(tableS3).Fromthese estimates,thereislittleevidenceofdensitydependentdeclines,althoughmodelresultssuggestthattherateofdeclineameliorateswiththe timesinceinfection(Fig.3DandtableS3).To incorporatethistimeameliorationeffectintothe simulationmodel,weusedpredictedvaluesof populationgrowthfromanonlinearmodel[ l = 1 1.16×exp( – 0.31× t ),where t =yearssince infection]foreachof16yearsafterinfection, whenpredictedpopulationgrowthstabilized( l = 1)(Fig.3D). Wesimulatedpopulationgrowthforfive scenariosrelatedtothistimeameliorationeffect,includingdeclinesamelioratedaccording topredictedvalues(Fig.3D)ateachyearly timestepandthatpersistedat45%(3rd-year actualmean),20%(6th-yearpredictedmean), 10%(8th-yearpredictedmean),5%(10th-year predictedmean),and2%(13th-yearpredicted mean)peryear(Fig.4).Bycomparingthe probabilitiesofextinctionover100yearsfor thesefivescenarios,weevaluatedthevulnerabilityoftheregionalpopulationtoextinction, Fig.1. ( A )Photographofhibernatinglittlebrownmyotis infectedwithWNS.Whitefungusisvisibleon wings,ears,muzzle,andotherexposedskintissues.[Photo:RyanVonLinden]( B )Batcarcassespiledon acavefloor,illustratingmassmortalityathiber naculainfectedwithWNS.[Photo:AlanHicks]( C )Skulls, bones,anddecomposedcarcassescoveringthecave flooraftermultipleyearsofinfection.[Photo: MarianneMoore] 6AUGUST2010VOL329 SCIENCE www.sciencemag.org680REPORTS

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giventheuncertaintyinhowdeclinesfrom diseasemortalitymaypersistinthefuture. Usingvitalratesderivedfrommeandeclines inthefirst3yearsofinfectionandpersistingat theobservedthird-yearmeandeclineof45% peryearthereafter(Fig.3D),weexpecta99% chanceofregionalextinctionoflittlebrown myotiswithinthenext16years(Fig.4A).Ifdeclinescontinuetoamelioratewithtimesinceinfection,timelinestoprobableextinctionlengthen butremaingreaterthan90%by65years,evenif declinesameliorateandstabilizeat10%peryear (Fig.4A).Modelresultsindicatethatannual declinesfromWNSwouldhavetoameliorateto lessthan5%peryeartosignificantlyreducethe chanceofextinctionover100years(Fig.4A). Evenifdiseasemortalitylessensovertime,the regionalpopulationisexpectedtocollapsefrom anestimatedstartingpopulationof6.5millionbats tofewerthan65,000(1%ofthepre-WNSpopulation)inlessthan20years(Fig.4B). Ourresultspaintagrimpictureofaoncehealthypopulationofanabundantandwidelydistributedspeciesnowexperiencingunprecedented lossesfromWNSandfacingaseriousthreatof regionalextinctionwithinthenext16years(Fig. 4).Suchaseverepopulationdecline,especially ifthediseasespreadsfarthersouthandwestof itscurrentdistributionineasternNorthAmerica, mayresultinunpredictablechangesinecosystem Fig.3. ( A to C )Populationtrendsoflittlebrown myotisoverthepast30yearsat(A)small(<1500 bats),(B)medium(<5000bats),and(C)large (>5000bats)hibernatingcoloniesinthenortheasternUnitedStates.Solidlinesrepresentsites withbatsinfectedwithWNS;dottedlinesrepresent uninfectedsites.HibernaculainfectedwithWNS experiencedasignificantreductioninnumbersas comparedtothelowestavailablecountfromthepast 30years(Wilcoxontest=190; P <0.002).Large decreasesinwintercountsatafewhibernaculainthe mid-1990swererelatedt owinterfloodevents.( D ) Populationgrowth( l )athibernacula(blackcircles) byyearsinceinfection.Thecurvedfittedlinerepresentsthenonlineartime -dependentmodel,showing ameliorationofmortalityfromWNSuntilpopulation growthreachesequilibriumat l =1in16years sincethefirstyearofinfection(verticaldottedline). Thehockey-sticklinerepresentsdeclinesfromWNS persistingatthethird-yearmeanof45%peryear, afterafirst-yeardeclineof85%andasecond-year declineof62%. 5,000 10,000 15,000 20,000 25,000 30,000198519901995200020052010 Winter count Winter countWNS200 400 600 800 1,000 1,2001980198519901995200020052010WNSC A1,000 2,000 3,000 4,0001980198519901995200020052010WNSBWinter countYear510 15 200.0 0.2 0.4 0.6 0.8 1.0 Year of infectionPopulation growth ( )D INTEREST AREA OF2010 (Likely) 2010 2009 (Likely) 2009 2008 2007 2006by County/DistrictWhite Nose Syndrome0250500Kilometers Fig.2. MapofcurrentdistributionandspreadofWNSacrosseasternNorthAmerica. www.sciencemag.org SCIENCE VOL3296AUGUST2010681REPORTS

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structureandfunction( 27 , 28 ).TherapidgeographicspreadofWNSsince2006,coupled withtheseverityandrapidityofpopulationdeclines,supportthehypothesisofintroductionof anovelpathogenintoanaïvepopulationanddemonstratetheseriousnessofpathogenpollutionas aconservationissue( 1 ).Ouranalysisfocused onlittlebrownmyotisinthenortheasternUnited States,butseveralotherbatspeciesareexperiencingsimilarmortalityfromWNSandmayalso beatsignificantriskofpopulationcollapseor extinction.Thisrapiddeclineofacommonbat speciesfromWNSdrawsattentiontotheneed forincreasedresearch,monitoring,andmanagementtobetterunderstandandcombatthisinvasivewildlifedisease( 1 ).ReferencesandNotes1.P.Daszak,A.A.Cunningham,A.D.Hyatt, Science 287 , 443(2000). 2.H.McCallum,A.Dobson, TrendsEcol.Evol. 10 ,190(1995). 3.H.McCallum, TrendsEcol.Evol. 23 ,631(2008). 4.A.M.Kilpatrick,C.J.Briggs,P.Daszak, TrendsEcol.Evol. 25 ,109(2010). 5.L.Berger etal ., Proc.Natl.Acad.Sci.U.S.A. 95 ,9031 (1998). 6.K.R.Lips etal ., Proc.Natl.Acad.Sci.U.S.A. 103 ,3165 (2006). 7.F.Fenner, FEMSMicrobiol.Rev. 24 ,123(2000). 8.S.L.LaDeau,A.M.Kilpatrick,P.P.Marra, Nature 447 , 710(2007). 9.D.S.Blehert etal ., Science 323 ,227(2009). 10.A.Gargas,M.T.Trest,M.Christensen,T.J.Volk, D.S.Bleher, Mycotaxon 108 ,147(2009). 11.S.J.Puechmaille etal ., Emerg.Infect.Dis. 16 ,290(2010). 12.T.J.O'Shea,M.A.Bogan, MonitoringTrendsinBat PopulationsoftheUnitedStatesandTerritories:Problems andProspects (BiologicalResourcesDiscipline,Information andTechnologyReportUSGS/BRD/ITR-2003-003, U.S.GeologicalSurvey,Washington,DC,2003). 13.R.Barbour,W.Davis, BatsofAmerica (Univ.Pressof Kentucky,Lexington,KY,USA,1969). 14.T.H.Kunz,L.F.Lumsden,in BatEcology, T.H.Kunz, M.B.Fenton,Eds.(Univ.ofChicagoPress,Chicago,IL, 2003),pp.3 – 89. 15.T.H.Kunz,D.S.Reynolds,in( 12 ),pp.9 – 20. 16.W.H.Davis,H.B.Hitchcock, J.Mammal. 46 ,296(1965). 17.D.W.Thomas,M.B.Fenton,R.M.R.Barclay, Behav.Ecol.Sociobiol. 6 ,129(1979). 18.Informationonmaterialsandmethodsisavailableon Science Online. 19.W.F.Frick,D.S.Reynolds,T.H.Kunz, J.Anim.Ecol. 79 , 128(2010). 20.E.T.Posluszny,C.Butchkoski,in ProceedingsofBat ConservationandMining:ATechnicalInteractiveForum (BatConservationInternationalandU.S.Departmentof theInterior,OfficeofSurfaceMining,St.Louis,MO, 2000),pp.159 – 168. 21.M.D.Tuttle,D.Hensley, Bats 11 ,3(1993). 22.K.N.Geluso,J.S.Altenbach,D.E.Wilson, Science 194 , 184(1976). 23.W.F.Morris,D.F.Doak, QuantitativeConservation Biology:TheoryandPracticeofPopulationViability Analysis (Sinauer,Sunderland,MA,2002). 24.F.Courchamp,T.Clutton-Brock,B.Grenfell, TrendsEcol.Evol. 14 ,405(1999). 25.P.A.Stephens,W.J.Sutherland, TrendsEcol.Evol. 14 , 401(1999). 26.F.Courchamp,B.Grenfell,T.Clutton-Brock, Proc.Biol.Sci. 266 ,557(1999). 27.K.J.Gaston, Science 327 ,154(2010). 28.G.W.Luck,G.C.Daily,P.R.Ehrlich, TrendsEcol.Evol. 18 ,331(2003). 29.FundingwasprovidedbygrantsfromtheU.S.Fishand WildlifeService(USFWS)toW.F.F.,J.F.P.,D.S.R.,T.H.K.,and G.G.T.Wethankthreeanonymousreviewers,J.P.Hayes, andD.F.DoakforhelpfulreviewsandA.M.Kilpatrickfor fruitfuldiscussion.Fundingforwintercountsofbatsat hibernaculawasprovidedbyUSFWSSection6andState WildlifeGrantsissuedtothePennsylvaniaGame Commission,andbyFederalAidinWildlifeRestoration GrantWE-173-GissuedtotheNewYorkStateDepartment ofEnvironmentalConservation.Countdatafromhibernating colonieswerekindlyprovidedbytheConnecticutDepartment ofEnvironmentalProtection;thePennsylvaniaGame Commission;theNewYorkDepartmentofEnvironmental Conservation;VermontFishandGame;theMassachusetts DivisionofFisheriesandWildlife;andK.Berner,State UniversityofNewYorkatCobleskill.Wearegratefultothe manyindividualswhowereinvolvedinconductingannual countsofbatsathibernaculaoverthepast30years.Data areavailableuponrequestfromtheauthors.SupportingOnlineMaterialwww.sciencemag.org/cgi/content/full/329/5992/679/DC1 MaterialsandMethods Figs.S1andS2 TablesS1toS3 References 22February2010;accepted24May2010 10.1126/science.1188594Sex-SpecificParent-of-OriginAllelic ExpressionintheMouseBrainChristopherGregg,1,2JiangwenZhang,3JamesE.Butler,1,2DavidHaig,4CatherineDulac1,2* Genomicimprintingresultsinpreferentialgeneexpressionfrompaternallyversusmaternally inheritedchromosomes.Weusedagenome-wideapproachtouncoversex-specificparent-of-origin alleliceffectsintheadultmousebrain.Ourstudyidentifiedpreferentialselectionofthematernally inheritedXchromosomeinglutamatergicneuronsofthefemalecortex.Moreover,analysisofthe cortexandhypothalamusidentified347autosomalgeneswithsex-specificimprintingfeatures.In thehypothalamus,sex-specificimprintedgenesweremostlyfoundinfemales,whichsuggests parentalinfluenceoverthehypothalamicfunctionofdaughters.Weshowthat interleukin-18 ,a genelinkedtodiseaseswithsex-specificprevalence,issubjecttocomplex,regional,and sex-specificparentaleffectsinthebrain.Parent-of-origineffectsthusprovidenewavenuesfor investigationofsexualdimorphisminbrainfunctionanddisease.Genomicimprintingisanepigeneticmode ofgeneregulationinvolvingpreferential expressionofthepaternallyormaternallyinheritedallele( 1 ).Sexualdimorphismisa centralcharacteristicofmammalianbrainfunctionandbehaviorthatinfluencesmajorneurologicaldiseasesinhumans( 2 ).Hereweaddress thepotentialexistenceofdifferentialgenomic imprintinginthebrainaccordingtothesexof individuals.Imprintingreferstogeneexpression differencesbetweenmaternalandpaternalchromosomes( 3 )andisalsousedmorestrictlyto definecompleteallele-specificsilencing( 4 ).Our analysisencompassessexdifferencesinparent1DepartmentofMolecularandCellularBiology,Harvard University,Cambridge,MA02138,USA.2HowardHughes MedicalInstitute,HarvardUniversity,Cambridge,MA02 138, USA.3FASResearchComputing,HarvardUniversity,Cambridge, MA02138,USA.4DepartmentofOrganismicandEvolutionary Biology,HarvardUniversity,Cambridge,MA02138,USA. *Towhomcorrespondenceshouldbeaddressed.E-mail: dulac@fas.harvard.edu 0.0 0.2 0.4 0.6 0.8 1.0 20406080100 Cumulative probability of extinction 0 50,000 100,000 150,000 200,000 250,000 20406080100 45% 20% 10% 5% 2% 6,500,000 Regional population sizeYears into future A B Fig.4. ( A )Cumulativeprobabilityofregional extinctionoflittlebrownmyotisforfivescenariosoftime-dependentameliorationofdisease mortalityfromWNS,basedonmatrixmodel simulationresults.Eachscenariorepresentspredictedtime-dependentdeclinesforaspecified numberofyearsafterinfectionandthenholds thedeclinerateconstantateither45,20,10,5, or2%todemonstratetheimpactofameliorationontheprobabilityofextinctionoverthe next100years.( B )Populationsizeineachyear averagedacross1000simulationsforeachof thefivescenariosoftime-dependentameliorationofmortalityfromWNS. 6AUGUST2010VOL329 SCIENCE www.sciencemag.org682REPORTS


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