Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements.
Morgan E WirthlinTobias A SchmidJulie E ElieXiaomeng ZhangAmanda KowalczykRuby RedlichVarvara A ShvarevaAshley RakuljicMaria B JiNinad S BhatIrene M KaplowDaniel E SchäfferAlyssa J LawlerAndrew Z WangBaDoi N PhanSiddharth AnnaldasulaAshley R BrownTianyu LuByung Kook LimEiman Azimnull nullNathan L ClarkWynn K MeyerSergei L Kosakovsky PondMaria ChikinaMichael M YartsevAndreas R PfenningGregory AndrewsJoel C ArmstrongMatteo BianchiBruce W BirrenKevin R BredemeyerAna M BreitMatthew J ChristmasHiram ClawsonJoana DamasFederica Di PalmaMark DiekhansMichael X DongEduardo EizirikKaili FanCornelia FanterNicole M FoleyKarin Forsberg-NilssonCarlos J GarciaJohn GatesySteven GazalDiane P GenereuxLinda GoodmanJenna GrimshawMichaela K HalseyAndrew J HarrisGlenn HickeyMichael HillerAllyson G HindleRobert M HubleyGraham M HughesJeremy JohnsonDavid JuanIrene M KaplowElinor K KarlssonKathleen C KeoughBogdan KirilenkoKlaus-Peter KoepfliJennifer M KorstianAmanda KowalczykSergey V KozyrevAlyssa J LawlerColleen LawlessThomas LehmannDanielle L LevesqueHarris A LewinXue LiAbigail LindKerstin Lindblad-TohAva Mackay-SmithVoichita D MarinescuTomas Marques-BonetVictor C MasonJennifer R S MeadowsWynn K MeyerJill E MooreLucas R MoreiraDiana D Moreno-SantillanKathleen M MorrillGerard MuntanéWilliam J MurphyArcadi NavarroMartin NweeiaSylvia OrtmannAustin OsmanskiBenedict PatenNicole S PaulatAndreas R PfenningBaDoi N PhanKatherine S PollardHenry E PrattDavid A RaySteven K ReillyJeb R RosenIrina RufLouise RyanOliver A RyderPardis C SabetiDaniel E SchäfferAitor SerresBeth ShapiroArian F A SmitMark SpringerChaitanya SrinivasanCynthia SteinerJessica M StorerKevin A M SullivanPatrick F SullivanElisabeth SundströmMegan A SuppleRoss SwoffordJoy-El TalbotEmma TeelingJason Turner-MaierAlejandro ValenzuelaFranziska WagnerOla WallermanChao WangJuehan WangZhiping WengAryn P WilderMorgan E WirthlinJames R XueXiaomeng ZhangPublished in: Science (New York, N.Y.) (2024)
Vocal production learning ("vocal learning") is a convergently evolved trait in vertebrates. To identify brain genomic elements associated with mammalian vocal learning, we integrated genomic, anatomical, and neurophysiological data from the Egyptian fruit bat ( Rousettus aegyptiacus ) with analyses of the genomes of 215 placental mammals. First, we identified a set of proteins evolving more slowly in vocal learners. Then, we discovered a vocal motor cortical region in the Egyptian fruit bat, an emergent vocal learner, and leveraged that knowledge to identify active cis-regulatory elements in the motor cortex of vocal learners. Machine learning methods applied to motor cortex open chromatin revealed 50 enhancers robustly associated with vocal learning whose activity tended to be lower in vocal learners. Our research implicates convergent losses of motor cortex regulatory elements in mammalian vocal learning evolution.