LANKESTERIANA  ². DARWIN’S ORCHIDS: THEIR VARIATION, PLASTICITY, AND NATURAL SELECTION James D. ackerman1,4, mariely morales2 & raymonD Tremblay3 'HSDUWPHQWRI%LRORJ\DQG&HQWHUIRU$SSOLHG7URSLFDO(FRORJ\DQG&RQVHUYDWLRQ 8QLYHUVLW\RI3XHUWR5LFR32%R[6DQ-XDQ3586$ 2 'HSDUWPHQWRI%LRORJ\8QLYHUVLW\RI3XHUWR5LFR32%R[6DQ-XDQ3586$  'HSDUWPHQWRI%LRORJ\8QLYHUVLW\RI3XHUWR5LFR+XPDFDR3586$DQG&HQWHUIRU $SSOLHG7URSLFDO(FRORJ\DQG&RQVHUYDWLRQ8QLYHUVLW\RI3XHUWR5LFR6DQ-XDQ3586$  $XWKRUIRUFRUUHSRQGHQFHDFNHUPDQXSU#JPDLOFRP  absTracT3DWWHUQVRIYDULDWLRQDQGWKHLU¿WQHVVFRQVHTXHQFHVDUHFULWLFDOLQUHYHDOLQJQDWXUDOVHOHFWLRQ2QH RIWKHPRVWYDULDEOHJURXSVRISODQWVDUHWKHGHFHSWLRQSROOLQDWHGRUFKLGVSROOLQDWRUVRIZKLFKDUHGHFHLYHG LQWKHLUVHDUFKIRUDIRRGUHZDUG1HJDWLYHIUHTXHQF\GHSHQGHQWVHOHFWLRQDQGGLVUXSWLYHVHOHFWLRQKDYHEHHQ VXJJHVWHG DV WKH PHDQV E\ ZKLFK KLJK OHYHOV RI YDULDWLRQ DUH PDLQWDLQHG \HW LQ PRVW FDVHV VXFK VHOHFWLRQ KDVQRWEHHQGHWHFWHGSURPSWLQJDOWHUQDWLYHH[SODQDWLRQVLQFOXGLQJJHQHWLFGULIW&RXOGSKHQRW\SLFSODVWLFLW\ FORXG WKH HIIHFWV RI VHOHFWLRQ" 8VLQJ D Tolumnia variegata SRSXODWLRQ DV D PRGHO V\VWHP ZH FRQGXFWHG D UHFLSURFDO WUDQVSODQW H[SHULPHQW WR GHWHUPLQH WKH HIIHFWV RI OLJKW HQYLURQPHQW RQ YHJHWDWLYH LQÀRUHVFHQFH DQG ÀRUDO FKDUDFWHULVWLFVRYHU PXOWLSOHVHDVRQV7KH UHVXOWVZHUHFRPSOH[DQGVKRZHG VLJQL¿FDQWUHVSRQVHV WROLJKWIRUPRVWWUDLWVPHDVXUHGEXWRIWHQWKRVHFKDQJHVZHUHREVFXUHGE\YDULDEOHUHVSRQVHVDFURVV\HDUV OLNHO\DFRQVHTXHQFHRIGUDPDWLFDOO\GLIIHUHQWUDLQIDOO)UXLWSURGXFWLRQZDVVLPLODUIRUVXQDQGVKDGHVLWHVEXW WUDMHFWRULHVRIVHOHFWLRQRQDJLYHQWUDLWEHWZHHQWKHWZRVLWHVZHUHRIWHQLQFRQJUXHQW2XUGDWDLQGLFDWHGWKDW VHOHFWLRQLQDKHWHURJHQHRXVHQYLURQPHQWFDQLQGHHGEHEOXQWHGE\SKHQRW\SLFSODVWLFLW\EXWQRWDOOFKDUDFWHUV UHVSRQGLQWKHVDPHZD\ resumen/DVFRQVHFXHQFLDVGHORVSDWURQHVGHYDULDFLyQHQHOp[LWRGHXQDSODQWDVRQFUtWLFDVSDUDUHYHODUOD VHOHFFLyQQDWXUDO8QRGHORVJUXSRVPiVYDULDGRVGHSODQWDVVRQODVRUTXtGHDVTXHOOHYDQDFDERSROLQL]DFLyQ SRU HQJDxR ODV PLVPDV HQJDxDQ D ORV SROLQL]DGRUHV ORV FXDOHV EXVFDQ XQD UHFRPSHQVD DOLPHQWDULD HQ HOODV /DVHOHFFLyQQHJDWLYDGHSHQGLHQWHGHIUHFXHQFLD\ODVHOHFFLyQGLVUXSWLYDKDQVLGRVXJHULGDVSDUDH[SOLFDUHO PDQWHQLPLHQWRGHDOWRVQLYHOHVGHYDULDFLyQ(QODPD\RUtDGHORVFDVRVHVWDVVHOHFFLRQHVQRKDQVLGRGHWHFWDGDV SURYRFDQGRRWUDVH[SOLFDFLRQHVDOWHUQDVFRPRODGHULYDJHQpWLFD¢3RGUiODVHOHFFLyQQDWXUDOVHUQXEODGDSRUOD SODVWLFLGDGIHQRWtSLFD"8VDQGRSREODFLRQHVGHTolumnia variegata FRPRVLVWHPDPRGHORQRVRWURVUHDOL]DPRV XQH[SHULPHQWRGHWUDVSODQWHUHFtSURFRSDUDGHWHUPLQDUORVHIHFWRVGHODOX]HQODVFDUDFWHUtVWLFDVGHODSDUWH YHJHWDWLYDLQÀRUHVFHQFLD\ÀRUHVDWUDYpVGHGLIHUHQWHVpSRFDVGHODxR/RVUHVXOWDGRVIXHURQFRPSOHMRVOD PD\RUtDGHORVUDVJRVPHGLGRVSUHVHQWDURQUHVSXHVWDVVLJQL¿FDWLYDVDODOX]SHURODPD\RUtDGHHVWRVFDPELRV IXHURQREVFXUHFLGRVSRUUHVSXHVWDVYDULDGDVDWUDYpVGHORVDxRVSUREDEOHPHQWHSRUXQDGLIHUHQFLDGUDPiWLFD HQODSUHFLSLWDFLyQ/DSURGXFFLyQGHIUXWRVIXHVLPLODUHQWUHVLWLRVGHVRPEUD\VROSHURODVWUD\HFWRULDVGH VHOHFFLyQGHODVFDUDFWHUtVWLFDVHQWUHORVGRVOXJDUHVIXHURQHQVXPD\RUtDLQFRQJUXHQWHV1XHVWURVGDWRVLQGLFDQ TXHODVHOHFFLyQHQXQDPELHQWHKHWHURJpQHRSXHGHVHUGLVIUD]DGDSRUODSODVWLFLGDGIHQRWtSLFDSHURQRWRGDVODV FDUDFWHUtVWLFDVUHVSRQGHQGHODPLVPDPDQHUD key worDs2UFKLGDFHDH&KDUOHV'DUZLQÀRUDOYDULDWLRQGHFHLSWSROOLQDWLRQQDWXUDOVHOHFWLRQ  2QHKXQGUHGDQG¿IW\\HDUVDJR'DUZLQSXEOLVKHG KLV WUHDWLVH On the Origin of Species by Means of Natural Selection 8QTXHVWLRQDEO\ WKLV ZDV D ODQGPDUN HYHQW WKDW VKRRN WKH WHQHWV RI VFLHQFH DQG ZHVWHUQVRFLHW\7KLVSDJHDEVWUDFWHVWDEOLVKHGWKH IRXQGDWLRQ IRU HYROXWLRQDU\ WKHRU\ E\ GHVFULELQJ WKH SURFHVV E\ ZKLFK FKDQJH PD\ RFFXU WKURXJK QDWXUDO VHOHFWLRQ 'DUZLQ $VWKHVWRU\KDVEHHQWROGVR  LANKESTERIANA PDQ\ WLPHV IURP D SOHWKRUD RI SHUVSHFWLYHV 'DUZLQ ZDVVORZWRDPDVVVXSSRUWLQJGDWDDQGZDVSXVKHGWR FRPHIRUWKZLWKKLVWKHVLVZKHQ$OIUHG5XVVHO:DOODFH ZURWH WR KLP H[SUHVVLQJ HVVHQWLDOO\ WKH VDPH LGHDV :DOODFH  $OWKRXJK 'DUZLQ GLG QRW UHDFK WKH ELRORJLFDO GLYHUVH UHJLRQV RI WKH WURSLFDO $QGHV KH ZDV VWURQJO\ LQÀXHQFHG E\ KLV YLVLW WR DQRWKHU SDUW RI (FXDGRU WKH *DODSDJRV ,VODQGV 'DUZLQ   )URP WKRVH VWXGLHV DQG PDQ\ RWKHUV WKURXJKRXW WKH ZRUOGKHGHYHORSHGDVHQVHRIQDWXUDOKLVWRU\SHUKDSV XQPDWFKHGE\DOOWKRVHZKRSUHFHGHGKLPDQGWKRVH ZKRIROORZHG  2YHUWLPHZHKDYHFRPHWRNQRZ'DUZLQ¶VWKHRU\ RI QDWXUDO VHOHFWLRQ TXLWH ZHOO DQG KDYH EHHQ DEOH WR HQULFK LW ZLWK DFFXPXODWHG NQRZOHGJH RI ELRORJ\ HVSHFLDOO\ ZLWK D EHWWHU XQGHUVWDQGLQJ RI JHQHWLFV 1DWXUDOVHOHFWLRQLVQRZYLHZHGDVDSURFHVVZLWKWKUHH FRQGLWLRQV)LUVWDSRSXODWLRQPXVWKDYHYDULDWLRQD FRUQHUVWRQH WR WKH WKHRU\ WKRURXJKO\ DSSUHFLDWHG E\ 'DUZLQWKRXJKKHGLGQRWNQRZWKHJHQHWLFEDVLVIRU LW 6HFRQGO\ YDULDQWV ZLWKLQ D SRSXODWLRQ PXVW VKRZ GLIIHUHQWLDOUHSURGXFWLYHVXFFHVVDOVRNQRZQDV¿WQHVV $QG¿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rigin of SpeciesEXWWKH¿UVWERRNSXEOLVKHGDIWHU KLVODQGPDUNWUHDWLVHZDVOn the Various Contrivances by which British and Foreign Orchids Are Fertilised by InsectsDFRPSHQGLXPRISROOLQDWLRQPHFKDQLVPV DVVRFLDWHG ZLWK HQVXULQJ FURVVIHUWLOL]DWLRQ 'DUZLQ   +H UHJDUGHG WKRVH PHFKDQLVPV VRPH TXLWH IDQWDVWLF DV D FRQVHTXHQFH RI WKH DGYDQWDJHV IRU FURVVSROOLQDWLRQ 6XFK REVHUYDWLRQV DUH FRQYLQFLQJ DOWKRXJKWKH\PHUHO\UHSUHVHQWLQGLUHFWHYLGHQFHIRU QDWXUDOVHOHFWLRQ  7KH PHFKDQLVPV IRU FURVVIHUWLOL]DWLRQ DERXQG LQ SODQWVEXW'DUZLQNQHZWKDWLWZDVLQVXI¿FLHQWVLPSO\ WRFDWDORJXHWKHPWKDWKHDOVRKDGWRVKRZZKDWWKH LANKESTERIANA 11(3), December 2011. © Universidad de Costa Rica, 2011. DGYDQWDJHZDV2XWFDPH\HWDQRWKHUERRNLQVXSSRUW RIKLVWKHRU\RIQDWXUDOVHOHFWLRQThe Effects of Cross and Self Fertilisation in the Vegetable Kingdom 'DUZLQ :LWKPHWLFXORXVJDUGHQH[SHULPHQWV RQ D YDULHW\ RI SODQWV 'DUZLQ GHPRQVWUDWHG WKDW FURVVIHUWLOL]DWLRQSURGXFHGVWURQJYDULDEOHRIIVSULQJ ZKHUHDV UHSHDWHG VHOIIHUWLOL]DWLRQ SURGXFHG SURJUHVVLYHO\IHZHUDQGZHDNHUSURJHQ\DWUHQGWKDW FRXOG EH UHYHUVHG ZLWK D UHWXUQ WR FURVVIHUWLOL]DWLRQ :HLQWHUSUHWWKHUHVXOWVRIVHO¿QJDVVLPSO\LQEUHHGLQJ GHSUHVVLRQWKRXJK'DUZLQH[SUHVVHGLWPRUHHOHJDQWO\ LQ WKH ÀRZHU\ ODQJXDJH RI WKH WLPH ³,W LV KDUGO\ DQ H[DJJHUDWLRQ WR VD\ WKDW 1DWXUH WHOOV XV LQ WKH PRVW HPSKDWLF PDQQHU WKDW VKH DEKRUV SHUSHWXDO VHOI IHUWLOLVDWLRQ´ 'DUZLQ  2UFKLGVDQGÀRUDOYDULDWLRQ  2UFKLGV DUH QRW RQO\ DQ LGHDO PRGHO V\VWHP WR HOXFLGDWH WKH UHPDUNDEOH DGDSWDWLRQV DVVRFLDWHG ZLWK FURVVSROOLQDWLRQEXWWKH\DUHDOVRLGHDOEHFDXVHWKH\ DUHSHUKDSVWKHPRVWVSHFLHVULFKIDPLO\RIÀRZHULQJ SODQWV 7KLV GLYHUVLW\ KDV RIWHQ EHHQ DWWULEXWHG WR DGDSWLYHUDGLDWLRQDVVRFLDWHGZLWKGLYHUVHSROOLQDWLRQ ELRORJ\$OWKRXJKWKHIDPLO\LVUHODWLYHO\ROG 5DPtUH] et al ZHSHUFHLYHLWDVDG\QDPLFJURXSZKHUH QDWXUDOVHOHFWLRQVKRXOGEHSHUYDVLYH  8QOLNH 3RQFH GH /HyQ VRPH HYLGHQFH LQGLFDWHV WKDW RUFKLGV KDYH IRXQG WKH IRXQWDLQ RI \RXWK ZKHUH GLYHUVL¿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pUH] $]HYHGR et al-HUViNRYiet al  ackerman et al.²'DUZLQ¶VRUFKLGV $ VHFRQG SRVVLELOLW\ LV WKDW SHULRGLF JHQHWLF GULIW UHOD[HG VHOHFWLRQ  PD\ JHQHUDWH YDULDWLRQ SDUWLFXODUO\ ZKHQ SRSXODWLRQ VL]HV DUH VPDOO ZLWK HYHQ IHZHU UHSURGXFWLYH LQGLYLGXDOV ,QGHHG PDQ\ RUFKLGSRSXODWLRQVGRDSSHDUWREHVPDOODQGIUXLWVHW LVRIWHQORZ1DWXUDOVHOHFWLRQZRXOGKDYHWREHVWURQJ WRRYHUFRPHWKHVHFRQGLWLRQV7KHUHLVVRPHHYLGHQFH FRQVLVWHQWZLWKWKLVPHFKDQLVPRIJHQHUDWLQJXQXVXDOO\ KLJKOHYHOVRIYDULDWLRQ 7UHPEOD\ $FNHUPDQ 3HOOHJULQRet al6DO]PDQQet al *HQHWLF GULIW PD\ DOVR RFFXU LQ ODUJHU SRSXODWLRQV ZKHQ WKH GULYHURIVHOHFWLRQLVQRORQJHUUHOHYDQWDWOHDVWIRUD WLPH$OWKRXJK WKLV KDV EHHQ GHPRQVWUDWHG IRU VRPH DQLPDOV VXFK DV 'DUZLQ¶V *DODSDJRV ¿QFKHV DQG VXJJHVWHG IRU SODQWV *UDQW  *UDQW  5LYHUD 0DUFKDQG $FNHUPDQ ZHDUHQRWDZDUHRID VLPLODUH[DPSOHLQRUFKLGV  7KH WKLUG SRVVLELOLW\ IRU XQXVXDOO\ KLJK OHYHOV RI YDULDWLRQ FRPHV EDFN WR QDWXUDO VHOHFWLRQ ,Q PRVW FDVHVLWLVH[SHFWHGWKDWVHOHFWLRQZLOOUHGXFHYDULDWLRQ (QGOHU EXWWKHUHDUHW\SHVRIVHOHFWLRQWKDWFDQ LQFUHDVHYDULDWLRQVXFKDVGLVUXSWLYHVHOHFWLRQZKHUHE\ XQXVXDO YDULDQWV DUH WKRVH WKDW KDYH DQ DGYDQWDJH RYHU FRPPRQ IRUPV 0RVW À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³ZLUHG´WRUHFRJQL]HSRWHQWLDO IRRG VRXUFHV %HHV IRU H[DPSOH WHVW WKH DYDLODELOLW\ RIUHVRXUFHVWKURXJKH[SORUDWRU\YLVLWVVRRQDIWHUWKH\ HPHUJHIURPWKHLUFHOOVDQGODWHUDVWKHLUIDYRUHGSODQWV JRRXWRIÀRZHU7KH\YLVLWDQXPEHURIÀRZHUVRID FHUWDLQW\SHDQGLIWKH\IDLOWRH[WUDFWDUHZDUGWKHQ WKH\ZLOOPRYHWRVHHNDOWHUQDWLYHUHVRXUFHV +HLQULFK   7KH LGHD LV WKDW LI DOO ÀRZHUV ORRN WKH VDPH WKHQWKHEHHVZLOOOHDUQTXLFNO\WRDYRLGWKHVSHFLHV EXW LI ÀRZHUV DSSHDU GLIIHUHQW WKHQ LW WDNHV WKH EHHV ORQJHUWROHDUQDQGPRUHÀRZHUVZLOOEHYLVLWHGDVD FRQVHTXHQFH +HLQULFK 1RWRQO\ZRXOGIUXLWVHW  EHKLJKHULQYDULDEOHSRSXODWLRQVWKHEHHVZRXOGPRUH OLNHO\PRYHDPRQJSODQWVDIWHUHDFKIDLOHGH[SORUDWRU\ YLVLWUHVXOWLQJLQDQLQFUHDVHLQWKHSUREDELOLW\RIFURVV SROOLQDWLRQ -RKQVRQ 1LOVVRQ-RKQVRQet al.  -HUViNRYi  -RKQVRQ   7KXV XQXVXDO YDULDQWVZRXOGKDYHWKHDGYDQWDJHDQGWKHLUSURJHQ\ ZRXOGEHEHWWHUUHSUHVHQWHGLQWKHQH[WJHQHUDWLRQ  7KHKLJKOHYHOVRIYDULDWLRQLQGHFHSWLRQSROOLQDWHG SODQWV KDV EHHQ IUHTXHQWO\ FRPPHQWHG XSRQ EXW WKHUH LV RQO\ D VLQJOH SXEOLVKHG UHSRUW WKDW FRPSDUHV SRSXODWLRQYDULDWLRQLQGHFHSWLRQDQGUHZDUGSODQWVDQG WKLVZDVDVLQJOHVSHFLHVSDLURIAnacamptis 6DO]PDQQ et al.   :H GR KDYH DPSOH XQSXEOLVKHG GDWD WKDW LQGLFDWH GHFHSWLRQSROOLQDWHG SODQWV DUH LQGHHG JHQHUDOO\PRUHYDULDEOH $FNHUPDQ&XHYDVDQG+RI XQSXEOLVKHG +RZHYHUWKHFDXVHVRIVXFKKLJKOHYHOV RI YDULDWLRQ XVXDOO\ GR QRW PHHW WKH H[SHFWDWLRQV RI QHJDWLYH IUHTXHQF\GHSHQGHQW VHOHFWLRQ ,Q IDFW RQO\ RQHFDVHKDVEHHQUHSRUWHGDactylorhiza sambucina / 6RyDQGWKHUHLVVRPHGLVSXWHRYHUWKDW *LJRUG et al-HUViNRYiet al. 7KXVIDUDOORWKHU FDVHVVWXGLHG DOOXVLQJGLIIHUHQWPHWKRGRORJLHV KDYH IDLOHGWRGHWHFWWKLVW\SHRIVHOHFWLRQDQGKDYHLQGLFDWHG WKDWUHOD[HGVHOHFWLRQRUVRPHRWKHUIRUPRIVHOHFWLRQ PD\EHRFFXUULQJ $FNHUPDQet al.$UDJyQ  $FNHUPDQ  $FNHUPDQ  &DUURPHUR   7KLVLVQRWWRVD\WKDWQDWXUDOVHOHFWLRQRUHYHQPRUH VSHFL¿FDOO\ QHJDWLYH IUHTXHQF\GHSHQGHQW VHOHFWLRQ KDV QRW RU ZLOO QRW RFFXU EXW WKDW RQO\ GXULQJ WKH FRXUVHRIWKHVHSDUWLFXODUVWXGLHVLWZDVQRWKDSSHQLQJ 6HOHFWLRQWKHQLVHLWKHUGLI¿FXOWWRGHWHFWLQWKHVHSODQWV RURFFXUVIRUUHODWLYHO\EULHISHULRGVRIWLPHDVVKRZQ E\ WKH VSDVPRGLF GLYHUVL¿FDWLRQ PRGHO 7UHPEOD\ et al. 2IFRXUVHWKHUHLV\HWDQRWKHUH[SODQDWLRQ WKHPHWKRGVIRUGHWHFWLQJVHOHFWLRQZHUHQRWULJRURXV HQRXJK RU VXI¿FLHQWO\ VHQVLWLYH WR GHWHFW VHOHFWLRQ ZKHQLWRFFXUV 9DULDWLRQDQGSODVWLFLW\  9DULDWLRQLVRIWHQSUHVXPHGWREHKHULWDEOHEXWWKH JHQHWLFVRIWKHVHWUDLWVDUHUDUHO\H[DPLQHGLQRUFKLGV SULPDULO\EHFDXVHWUDGLWLRQDOPHWKRGVUHTXLUHFRPPRQ JDUGHQ H[SHULPHQWV DQG FURVVHV DPRQJ WKH YDULDQWV )RUWKLVRUFKLGVDUHQRWJRRGPRGHOV\VWHPVEHFDXVH RI WKH GLI¿FXOW\ LQ SURSDJDWLQJ SODQWV IURP VHHG HVSHFLDOO\ WHUUHVWULDO VSHFLHV  DQG WKH UHODWLYHO\ ORQJ SHULRG WR ¿UVW UHSURGXFWLRQ 6RPH SODVWLFLW\ LQ WUDLW LANKESTERIANA 11(3), December 2011. © Universidad de Costa Rica, 2011.  LANKESTERIANA H[SUHVVLRQRFFXUVDQGLVQRWOLNHO\GLUHFWO\LQKHULWHG )RUH[DPSOHLQÀRUHVFHQFHVRIPRVWVSHFLHV QRWMXVW RUFKLGV  KDYH PXOWLSOH ÀRZHUV DQG IUHTXHQWO\ WKH ¿UVWÀRZHUVSURGXFHGDUHODUJHUWKDQWKRVHWKDWFRPH ODWHU D SUREOHP RI LQÀRUHVFHQFH DUFKLWHFWXUH DQGRU UHVRXUFH DOORFDWLRQ 7UHPEOD\  +HUUHUD   3ODVWLFUHVSRQVHVPD\DOVRRFFXULQÀRUDOSURGXFWLRQ DIWHU D SROOLQDWLRQ HYHQW $FNHUPDQ  +DUGHU DQG -RKQVRQ   :H JHW DURXQG WKLV SUREOHP E\ PHDVXULQJ DOO ÀRZHUV RI DQ LQÀRUHVFHQFH RU MXVW WKH ORZHUPRVW ÀRZHU +RZHYHU SODVWLFLW\ DOVR RFFXUV LQ UHVSRQVHWRHQYLURQPHQWDOKHWHURJHQHLW\0LFURKDELWDW JUDGLHQWVRFFXUZLWKLQSRSXODWLRQVDQGSODQWVUHVSRQG DFFRUGLQJO\ (QYLURQPHQWDO FRQGLWLRQV FDQ DOVR YDU\ IURP\HDUWR\HDUDVKDELWDWVJRWKURXJKVXFFHVVLRQDO SURFHVVHV RU DV ORFDO FOLPDWH FKDQJHV ZKHWKHU WHPSRUDU\ (O1LxRRU/D1LxD RUUHODWLYHO\SHUPDQHQW ORFDO XUEDQL]DWLRQ RU JOREDO FKDQJHV  3KHQRW\SLF UHVSRQVHVIRUJLYHQJHQRW\SHVDUHZHOONQRZQDPRQJ SODQWV 3LJOLXFFL   \HW SODVWLFLW\ LQ RUFKLGV KDV UHFHLYHG VFDQW DWWHQWLRQ 6KRXOG SODVWLF YHUVLRQV RI WUDLWV UHVXOW LQ GLIIHUHQWLDO ¿WQHVV WKHQ GHWHFWLQJ VHOHFWLRQZLWKLQDSRSXODWLRQPD\EHFRPHDGGLWLRQDOO\ SUREOHPDWLF&HUWDLQO\SKHQRW\SLFSODVWLFLW\FDQEOXQW WKHSRZHURIVHOHFWLRQ 3ODVWLFLW\LQRUFKLGVDWHVWFDVH  +RZPXFKSODVWLFLW\RFFXUVLQRUFKLGPRUSKRORJ\ DQG KRZ LV WKLV UHODWHG WR ¿WQHVV":H DGGUHVVHG WKLV TXHVWLRQ LQ D UHFHQW SDSHU 0RUDOHV et al.   E\ VWXG\LQJ D SRSXODWLRQ RI Tolumnia variegata 6Z  %UDHPDGHFHSWLRQSROOLQDWHGWZLJHSLSK\WHRFFXUULQJ LQWKH*UHDWHU$QWLOOHVIURPWKH9LUJLQ,VODQGVLQWKH HDVW WR ZHVWHUQ &XED 7KLV LV D VSHFLHV IRU ZKLFK DWWHPSWV ZHUH PDGH WR GHWHFW QHJDWLYH IUHTXHQF\ GHSHQGHQW VHOHFWLRQ EXW ZLWKRXW VXFFHVV $FNHUPDQ et al ,QIDFWQRVHOHFWLRQRIDQ\NLQGRQDQ\ ÀRUDO FKDUDFWHULVWLF LQFOXGLQJ IUDJUDQFH SURGXFWLRQ  ZDV UHYHDOHG H[FHSW IRU GLVUXSWLYH VHOHFWLRQ RQ ÀRZHULQJSKHQRORJ\DQGZHDNGLUHFWLRQDOVHOHFWLRQRQ WKHQXPEHURIÀRZHUV 6DEDWDQG$FNHUPDQ   /DUJH SRSXODWLRQV RI T. variegata DUH QRW XQFRPPRQDQGFDQEHIRXQGIURPGU\IRUHVWVWRZHW PRQWDQHUHJLRQV $FNHUPDQLQSUHVV 3ODQWVDUHVPDOO ZLWK V\PSRGLDO JURZWK 0RUSKRORJLFDO DQG JHQHWLF GLYHUVLW\ DUH KLJK )LJ   *HQHWLF GLIIHUHQWLDWLRQ DPRQJSRSXODWLRQVLVORZDQGHVWLPDWHVRIJHQHÀRZ LANKESTERIANA 11(3), December 2011. © Universidad de Costa Rica, 2011. Figure9DULDWLRQLQÀRZHUVIURPDVLQJOHSRSXODWLRQRI Tolumnia variegataLQ3XHUWR5LFR(DFKÀRZHUFDPH IURPDGLIIHUHQWSODQW3KRWR-DPHV'$FNHUPDQ DUH KLJK SDUWLFXODUO\ DPRQJ SRSXODWLRQV RI D JLYHQ LVODQG $FNHUPDQDQG*DODU]D3pUH]$FNHUPDQ DQG :DUG   )ORZHUV DUH VHOILQFRPSDWLEOH DQG SROOLQDWRUV DUH IHPDOH Centris decolorata $SLGDH $FNHUPDQ et al.   SUHVXPDEO\ GHFHLYHG E\ ÀRZHUVDSSHDULQJDVDQRLOUHVRXUFH  7R LQGXFH SODVWLF UHVSRQVHV ZH FRQGXFWHG D UHFLSURFDO WUDQVSODQW H[SHULPHQW ZKHUH RXU HQYLURQPHQWDO JUDGLHQW RI LQWHUHVW ZDV OLJKW 3ODQWV JUHZLQWKHRSHQXQGHUIXOOVXQDQGDOVRLQWKHVKDGH :H XVHG  SODQWV IURP WZR VXQ VLWHV DQG  SODQWV IURP WZR VKDG\ VLWHV DOO RI ZKLFK ZHUH ZLWKLQ D  P UDGLXV 3ULRU WR WUDQVSODQWLQJ WKH RUFKLGV ZH IRXQG WKDW VKDGH SODQWV KDG ODUJHU OHDYHV DQG ORQJHU LQÀRUHVFHQFHVEXWIHZHUÀRZHUVWKDQVXQSODQWV$IWHU WUDQVSODQWLQJZHIROORZHGWKHVHSODQWVIRUWZR\HDUV DQG UHFRUGHG D QXPEHU RI YHJHWDWLYH LQÀRUHVFHQFH DQGÀRUDOFKDUDFWHULVWLFVRQHDFKSODQWDQGPRQLWRUHG IHPDOH UHSURGXFWLYH VXFFHVV IUXLW SURGXFWLRQ  7KH ¿UVW \HDU DIWHU WUDQVSODQWLQJ   ZDV D ZHW RQH DERXW  PP DERYH QRUPDO SUHFLSLWDWLRQ 7KH VHFRQG\HDU  ZDVDGU\RQHZLWKSUHFLSLWDWLRQ DSSUR[LPDWHO\PPEHORZQRUPDO  8VLQJ UHSHDWHG PHDVXUHV $129$ WR DQDO\]H UHVXOWV RI WKH WUDQVSODQW H[SHULPHQW ZH IRXQG WKDW SODQWUHVSRQVHVZHUHFRPSOH[ 0RUDOHVet al.  /HDIFKDUDFWHULVWLFVRISODQWVWUDQVSODQWHGIURPVXQWR VKDGHRYHUWLPHORRNHGPXFKOLNHWKRVHWKDWRULJLQDWHG DQGVWD\HGLQWKHVKDGH/LNHZLVHWKRVHWKDWZHQWIURP VKDGHWRVXQEHFDPHPRUHOLNHVXQSODQWV/HDIVL]HLQ JHQHUDOZDVVWURQJO\DIIHFWHGE\GURXJKWFRQGLWLRQVLQ WKHVHFRQG\HDU  ackerman et al.²'DUZLQ¶VRUFKLGV  0HDVXUHVRIUHSURGXFWLYHHIIRUWJDYHPL[HGUHVXOWV 7KHQXPEHURIÀRZHUVGLGQRWFKDQJH3HGXQFOHOHQJWK ZDVVWURQJO\DIIHFWHGE\\HDUZKHUHDVWKHQXPEHURI LQÀRUHVFHQFHV ZDV PRUH DIIHFWHG E\ HQYLURQPHQWDO YDULDWLRQ  )ORUDOFKDUDFWHULVWLFVZHPHDVXUHGZHUHDVVRFLDWHG ZLWKÀRUDOGLVSOD\QRWZLWKSROOLQDWLRQPHFKDQLFV$OO DSSHDUHGWREHSODVWLFDQGDOOZHUHDIIHFWHGE\\HDU 2ULJLQRIWUDQVSODQWVKDGDVLJQL¿FDQWHIIHFWLQWKUHHRI ¿YHPHDVXUHVDQGÀRZHUVLQWKHVKDGHZHUHODUJHULQ WKUHHRI¿YHPHDVXUHVDVZHOO  +RZGLGWUDQVSODQWVGLIIHULQUHSURGXFWLYHVXFFHVV" 6XUSULVLQJO\IUXLWVHWZDVQRWDIIHFWHGE\HQYLURQPHQW HYHQ WKRXJK WKHUH ZHUH VLJQL¿FDQW GLIIHUHQFHV LQ SODQW WUDLWV EHWZHHQ WKH VXQ DQG VKDGH VLWHV :H GLG QRW PHDVXUH PDOH UHSURGXFWLYH VXFFHVV ZKHUH DOO WKH DFWLRQPD\RFFXUDVKDVEHHQVKRZQLQRWKHURUFKLG V\VWHPV $FNHUPDQ &DUURPHUR   %HFDXVH WKH SLFWXUH WKXV IDU LV FOHDU RQO\ LQ WKH VHQVHWKDWLWLVPXGG\ZHGHFLGHGWRWDNHDQDOWHUQDWLYH DSSURDFKWRGHWHFWLQJSDWWHUQVRIVHOHFWLRQE\XVLQJWKH QRQSDUDPHWULF FXELF VSOLQH UHJUHVVLRQ DQDO\VLV VHH 7UHPEOD\ et al.   :H XVHG GDWD IRU RQO\ WKRVH FKDUDFWHULVWLFV WKDW VKRZHG VLJQL¿FDQW UHVXOWV LQ WKH UHSHDWHGPHDVXUHV$129$V:HIRXQGWKDWIRUSHWDO ZLGWKWKHRYHUDOOSDWWHUQZDVIRUGLVUXSWLYHVHOHFWLRQ DQG WKLV ZDV DOVR UHÀHFWHG LQ WKH LQGLYLGXDO SDWWHUQV IRU VKDGH DQG VXQ SODQWV 7KXV WKH WZR KDELWDWV EHKDYHG WKH VDPH ZLWK UHVSHFW WR WKLV FKDUDFWHU )RU ÀRZHU QXPEHU WKHUH ZDV DQ RYHUDOO WUHQG IRU ODUJHU LQÀRUHVFHQFHV WR KDYH JUHDWHU ¿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¿FXOWWRGHWHFWDW WKHSRSXODWLRQOHYHO6XFKFRQÀLFWVPD\RFFXUDFURVV KDELWDWVDVZHOODVRYHUWLPH &RQFOXVLRQV  7KH GLI¿FXOW\ LQ GHWHFWLQJ VHOHFWLRQ LQ RUFKLG SRSXODWLRQV PD\ EH H[SODLQHG E\ WKH SRVVLELOLW\ WKDW VHOHFWLRQ LV QRW RFFXUULQJ RU DV ZH GLVFXVVHG KHUH VHOHFWLRQ PD\ JR LQ GLIIHUHQW GLUHFWLRQV GHSHQGLQJ RQ ZKHUH WKH\ DUH LQ D KHWHURJHQHRXV KDELWDW 7KH SLFWXUHFDQJHWHYHQPRUHRSDTXHZKHQRQHFRQVLGHUV SKHQRW\SLF UHVSRQVHV RYHU D QXPEHU RI VHDVRQV ZKHQ HQYLURQPHQWDO FRQGLWLRQV FKDQJH IURP \HDU WR \HDU 8VLQJ D %D\HVLDQ DSSURDFK ZLWK GDWD IURP WKLV Tolumnia VWXG\ SOXV GDWD IURP D SRSXODWLRQ RI Caladenia 7UHPEOD\ et al.   IRXQG WKDW LQGHHG VHOHFWLRQWUDMHFWRULHVFDQYDU\QRWRQO\DPRQJKDELWDWV EXW DOVR DPRQJ \HDUV DQG VLJQL¿FDQWO\ VR 7KXV ZH ¿QG\HWDQRWKHUUHDVRQZK\VHOHFWLRQPD\EHGLI¿FXOW WRGHWHFWLQRUFKLGV7KHQRWLRQWKDWVHOHFWLRQQHHGQRW EHRSHUDWLRQDODOOWKHWLPHVKRXOGFRPHDVQRVXUSULVH &RQVHTXHQWO\ZH¿QGWKDWWKHVHVWXGLHVDUHFRQVLVWHQW ZLWK WKH VSDVPRGLF PRGHO RI RUFKLG GLYHUVL¿FDWLRQ ZKHUHE\ SHULRGV RI GULIW QR VHOHFWLRQ  PD\ EH SXQFWXDWHG E\ EULHI EXW VWURQJ ERXWV RI VHOHFWLRQ 7UHPEOD\et al.  LITERATURE CITED Ackerman, J. D. 1986. Mechanisms and evolution of fooddeceptive pollination systems in orchids. Lindleyana 1: 108-113. Ackerman, J. D. 1989. Limitations to sexual reproduction in Encyclia krugii (Orchidaceae). Syst. Bot. 14: 101-109. Ackerman, J. D. In press. Flora of the Greater Antilles: Orchidaceae. Memoirs of the New York Botanical Garden, Bronx, USA. Ackerman, J. D. & W. Carromero. 2005. Is reproductive success related to color polymorphism in a deceptionpollinated, tropical terrestrial orchid? Caribbean J. Sc. 41: 234-242. Ackerman, J. D. & M. Galarza-Pérez. 1991. Patterns and maintenance of extraordinary variation in the Caribbean orchid, Tolumnia (Oncidium) variegata. Syst. Bot. 16: 182-194. Ackerman, J. D. & S. Ward. 1999. Genetic variation in a widespread, epiphytic orchid: where is the evolutionary potential? Syst. Bot. 24: 282-291. $UDJyQ 6  - ' $FNHUPDQ  'RHV ÁRZHU FRORU variation matter in deception pollinated Psychilis monensis (Orchidaceae)? Oecologia 138: 405-413. Azevedo, C., E. L. Borba & C. van den Berg. 2007. Evidence of natural hybridization and introgression in Bulbophyllum involutum Borba, Semir & F. Barros and LANKESTERIANA 11(3), December 2011. © Universidad de Costa Rica, 2011.  LANKESTERIANA B. weddellii (Lindl.) Rchb. f. (Orchidaceae) in the Chapda Diamantina, Brazil, by using allozyme markers. Rev. Brasil. Bot. 29: 415-421. Darwin, C. 1845. Journal of researches into the natural history and geology of the countries visited during the voyage of H.M. S. Beagle round the world under the command of Capt. Fitz Roy, R. N. John Murray, London, UK. Darwin, C. 1859. On the origin of species by means of natural selection. John Murray, London, UK. Darwin, C. 1862. On the various contrivances by which British and foreign orchids are fertilised by insects. John Murray, London, UK. Darwin, C. 1877. The effects of cross and self fertilisation in the vegetable kingdom. John Murray, London, UK. Endler, J. A. 1986. Natural selection in the wild. Princeton University Press, USA. Gigord, L. D. C., M. Macnair & A. Smithson. 2001. Negative frequency-dependent selection maintains a GUDPDWLF ÁRZHU FRORU SRO\PRUSKLVP LQ WKH UHZDUGOHVV orchid Dactylorhiza sambucina (L.) Soó. Proc. Nat. Ac. Sc. USA 98: 6253-6255. Grant, B. R & P. Grant. 2006. Evolution in Darwin’s ÀQFKHVDUHYLHZRIDVWXG\RQ,VOD'DSKQH0DMRULQWKH Galápagos Archipelago. Zoology 106: 255-259. +HLQULFK %  %HH ÁRZHUV D K\SRWKHVLV RQ ÁRZHU variety and blooming times. Evolution 29: 325-334. Heinrich, B. 1979. Bumblebee economics. Harvard University Press, Cambridge, Massachusetts, USA. Herrera, C. M. 2009. Multiplicity in unity. Plant subindividual variation and interaction with animals. University of Chicago Press, Chicago, Illinois, USA. -HUViNRYi- 6'-RKQVRQ/DFNRIÁRUDOQHFWDU UHGXFHV VHOISROOLQDWLRQ LQ D Á\SROOLQDWHG RUFKLG Oecologia 147: 60-68. Jersáková, J., P. Kindlmann & S. S. Renner. 2006. Is the colour dimorphism in Dactylorhiza sambucina maintained by differential seed viability instead of frequency-dependent selection? Folia Geobot. 41: 61-76. Johnson, S. D. & L. A. Nilsson. 1999. Pollen carryover, geitonogamy, and the evolution of deceptive pollination systems in orchids. Ecology 80: 2607-2619. Johnson, S. D., C. L. Peter & J. Ágren. 2004. The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio. Proc. Royal Soc., London B 271: 803-809. Morales, M., J. D. Ackerman & R. L. Tremblay. 2010. 0RUSKRORJLFDO ÁH[LELOLW\ DFURVV DQ HQYLURQPHQWDO gradient in the epiphytic orchid, Tolumnia variegata: FRPSOLFDWLQJ SDWWHUQV RI ÀWQHVV %RW - /LQQ 6RF 163: 431-446. LANKESTERIANA 11(3), December 2011. © Universidad de Costa Rica, 2011. Pellegrino, G., A. M. Palermo, M. E. Noce, F. Bellusci, & A. Musacchio. 2007. Genetic population structure in the Mediterranean Serapias vomeracea, a nonrewarding orchid group. Interplay of pollination strategy and stochastic forces? Pl. Syst. Evol. 263: 145-157. Pigliucci, M. 2001. Phenotypic plasticity: beyond nature and nurture. The Johns Hopkins University Press, Baltimore, Maryland, USA. Ramírez, S. R., B. Gravendeel, R. B. Singer, C. R. Marshall & N. E. Pierce. 2007. Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448: 10421045. Rivera-Marchand, B. & J. D. Ackerman. 2006. Bat pollination breakdown in a Caribbean columnar cactus, Pilosocereus royenii. Biotropica 38: 635-642. Sabat, A. & J. D. Ackerman. 1996. Fruit set in a deceptive RUFKLG WKH HIIHFW RI ÁRZHULQJ SKHQRORJ\ GLVSOD\ VL]H DQGORFDOÁRUDODEXQGDQFH$PHU-%RW Salzmann, C. C., A. M. Nardella, S. Cozzolino & F. P. 6FKLHVWO9DULDELOLW\LQÁRUDOVFHQWLQUHZDUGLQJDQG deceptive orchids: the signature of pollinator-imposed selection? Ann. Bot. 100: 757-765. Simpson, B. B. & J. L. Neff. 1983. Evolution and diversity RI ÁRUDO UHZDUGV 3S  in: C. E. Jones and R. J. Little (eds.). Handbook of experimental pollination biology. 6FLHQWLÀF DQG $FDGHPLF (GLWLRQV 1HZ <RUN USA. 7UHPEOD\ 5 /  7KH HIIHFW RI ÁRZHU SRVLWLRQ RQ male and female reproductive success in a deceptively pollinated tropical orchid. Biol. J. Linn. Soc. 151: 405410. 7UHPEOD\5/DQG-'$FNHUPDQ*HQHÁRZDQG effective population size in Lepanthes (Orchidaceae): a case for genetic drift. Biol. J. Linn. Soc. 72: 47-62. Tremblay, R. L., J. D. Ackerman & M.-E.3pUH]5LGLQJ DFURVV WKH VHOHFWLRQ ODQGVFDSH ÀWQHVV FRQVHTXHQFHV RI annual variation in reproductive characteristics. Philos. Trans. Royal Soc. London, B 365: 491-498. Tremblay, R. L., J. D. Ackerman, J. K. Zimmerman & R. N. Calvo. 2005. Variation in sexual reproduction in orchids DQGLWVHYROXWLRQDU\FRQVHTXHQFHVDVSDVPRGLFMRXUQH\ WRGLYHUVLÀFDWLRQ%LRO-/LQQ6RF Wallace, A. R. 1858. On the tendency of varieties to depart LQGHÀQLWHO\ IURP WKH RULJLQDO W\SH - 3URF /LQQ 6RF London 3: 46-50. Withner, C. L. 1974. Observations on equitant oncidiums as examples of introgressive hybridization. Pp. 34-45 in: H. H. Szmant & J. Wemple (eds.). First symposium on WKH VFLHQWLÀF DVSHFWV RI RUFKLGV Chemistry Department, University of Detroit, Detroit, Michigan, USA.