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Aphid Thermal Tolerance Is Governed by a Point Mutation in Bacterial Symbionts.doc

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Aphid Thermal Tolerance Is Governed by a Point Mutation in Bacterial Symbionts

o PL SBIOLOGY AphidThermalToleranceIsGoverned byaPointMutationinBacterialSymbionts Helen E.Dunbar, Alex C.C.Wilson¤,Nicole R.Ferguson, Nancy A.Moran* DepartmentofEcologyandEvolutionaryBiology,UniversityofArizona,Tucson,Arizona,UnitedStatesofAmerica Symbiosis is a ubiquitous phenomenon generating biological complexity, affecting adaptation, and expanding ecologicalcapabilities.However,symbionts,whichcanbesubjecttogeneticlimitationssuchasclonalityandgenomic degradation, also impose constraints on hosts. A model of obligate symbiosis is that between aphids and the bacterium Buchnera aphidicola, which supplies essential nutrients. We report a mutation in Buchnera of the aphid Acyrthosiphon pisum that recurs in laboratory lines and occurs in field populations. This single nucleotide deletion affects a homopolymeric run within the heat-shock transcriptional promoter for ibpA, encoding a small heat-shock protein.ThisBuchneramutationvirtuallyeliminatesthetranscriptionalresponseofibpAtoheatstressandlowersits expression even at cool or moderate temperatures. Furthermore, this symbiont mutation dramatically affects host fitnessinamannerdependentonthermalenvironment.Followingashortheatexposureasjuveniles,aphidsbearing short-allelesymbiontsproducedfewornoprogenyandcontainedalmostnoBuchnera,incontrasttoaphidsbearing symbionts without the deletion. Conversely, under constant cool conditions, aphids containing symbionts with the shortallelereproducedearlierandmaintainedhigherreproductiverates.Theshortallelehasappreciablefrequencies infieldpopulations(upto20%),furthersupportingtheviewthatloweringofibpAexpressionimproveshostfitness under some conditions. This recurring Buchnera mutation governs thermal tolerance of aphid hosts. Other cases in whichsymbiontmicroevolutionhasamajoreffectonhostecologicaltolerancearelikelytobewidespreadbecauseof thehighmutationratesofsymbioticbacteriaandtheircrucialrolesinhostmetabolismanddevelopment. Citation:DunbarHE,WilsonACC,FergusonNR,MoranNA(2007