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PRIFYSGOL BANGOR / B ANGOR UNIVERSITY

Evolutionary consequences of multidriver environmental change in an


aquatic primary producer
Brennan, Georgina; Colegrave, Nick; Collins, Sinead

Proceedings of the National Academy of Sciences of the USA

DOI:
10.1073/pnas.1703375114

Published: 12/09/2017

Peer reviewed version

Cyswllt i'r cyhoeddiad / Link to publication

Dyfyniad o'r fersiwn a gyhoeddwyd / Citation for published version (APA):


Brennan, G., Colegrave, N., & Collins, S. (2017). Evolutionary consequences of multidriver
environmental change in an aquatic primary producer. Proceedings of the National Academy of
Sciences of the USA, 114(37), 9930–9935. https://doi.org/10.1073/pnas.1703375114

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13. Mar. 2020



 Evolutionary consequences of multidriver 

 


environmental change in an aquatic primary producer 

 'EORGINA "RENNAN .ICK #OLEGRAVE 3INEAD #OLLINS 
 
 
"ANGOR 5NIVERSITY 5NIVERSITY OF %DINBURGH  5NIVERSITY OF %DINBURGH 
 
 3UBMITTED TO 0ROCEEDINGS OF THE .ATIONAL !CADEMY OF 3CIENCES OF THE 5NITED 3TATES OF !MERICA 
 #LIMATE CHANGE IS ALTERING AQUATIC ENVIRONMENTS IN A COMPLEX WAY DPNQPTJUJPO PG UIF QPQVMBUJPO
DBO CF VOEFSTUPPE UISPVHI UIF 
 AND SIMULTANEOUS SHIFTS IN MANY PROPERTIES WILL DRIVE EVOLUTIONARY NPEF PG JOUFSBDUJPO PG UIF ESJWFST  
 )PXFWFS XF QSFWJPVTMZ 
 RESPONSES IN PRIMARY PRODUCERS AT THE BASE OF BOTH FRESHWATER AND TIPXFE UIBU XIFO NPSF UIBO UISFF ESJWFST DPPDDVS BWFSBHF 
 MARINE ECOSYSTEMS 3O FAR EVOLUTIONARY STUDIES HAVE SHOWN HOW QMBTUJD SFTQPOTFT JO HSPXUI BSF FYQMBJOFE CZ EPNJOBOU ESJWFST 

 CHANGES IN ENVIRONMENTAL DRIVERS EITHER ALONE OR IN PAIRS AFFECT CFDBVTF PG FJUIFS TNBMM JOUFSBDUJPOT CFUXFFO OPOEPNJOBOU PS 
 THE EVOLUTION OF GROWTH AND OTHER TRAITS IN PRIMARY PRODUCERS [FSPTVN JOUFSBDUJPOT CFUXFFO ESJWFST 
 (ERE WE EVOLVE A PRIMARY PRODUCER IN NINETY SIX UNIQUE ENVI 
"RVBUJD QSJNBSZ QSPEVDFST XJMM FWPMWF VOEFS HMPCBM DIBOHF
 RONMENTS WITH DIFFERENT COMBINATIONS OF BETWEEN ONE AND EIGHT 
EVF UP UIFJS SBQJE DFMM EJWJTJPO SBUFT BOE IJHI TUBOEJOH HFOFUJD
 ENVIRONMENTAL DRIVERS TO UNDERSTAND HOW EVOLUTIONARY RESPONSES 
WBSJBUJPO BOE BCJMJUZ UP HFOFSBUF HFOFUJD WBSJBUJPO   
 8F
 TO ENVIRONMENTAL CHANGE DEPEND ON THE IDENTITY AND NUMBER OF 
EP OPU DVSSFOUMZ IBWF BO FNQJSJDBMMZTVQQPSUFE HFOFSBM VOEFS
 DRIVERS %VEN IN MULTIDRIVER ENVIRONMENTS ONLY A FEW DOMINANT 
TUBOEJOH PG IPX OBUVSBM TFMFDUJPO EJGGFST CFUXFFO TJOHMF BOE NVM
 DRIVERS EXPLAIN MOST OF THE EVOLUTIONARY CHANGES IN POPULATION 
UJESJWFS FOWJSPONFOUT )PXFWFS DPNQMFY FOWJSPONFOUBM DIBOHF
 

Submission PDF
GROWTH RATES -OST POPULATIONS CONVERGE ON THE SAME GROWTH RATE XJMM CF DPNNPO JO BRVBUJD FOWJSPONFOUT XJUI DPNCJOBUJPOT BOE
 BY THE END OF THE EVOLUTION EXPERIMENT (OWEVER POPULATIONS 
JOUFOTJUJFT PG ESJWFST IBWJOH TJHOJGJDBOU SFHJPOBM WBSJBUJPO 
TP JU
 ADAPT MORE WHEN THESE DOMINANT DRIVERS OCCUR IN THE PRESENCE 
JT WJUBM UIBU XF VOEFSTUBOE UIF KPJOU DPOUSJCVUJPOT PG UIF JEFOUJUZ
 OF OTHER DRIVERS 4HIS IS DUE TO AN INCREASE IN THE INTENSITY OF 
OVNCFS BOE JOUFOTJUZ PG ESJWFST UP USBJU FWPMVUJPO JO QSJNBSZ
 SELECTION IN ENVIRONMENTS WITH MORE DRIVERS WHICH ARE MORE 
QSPEVDFST 5XP OPOFYDMVTJWF NFDIBOJTNT DPVME DBVTF OBUVSBM TF
 LIKELY TO INCLUDE DOMINANT DRIVERS #ONCURRENTLY MANY OF THE TRAIT 
MFDUJPO UP BDU EJGGFSFOUMZ JO DBTFT PG DPNQMFY NVMUJESJWFS
WFSTVT
 CHANGES THAT OCCUR DURING THE INITIAL SHORT TERM RESPONSE TO BOTH 
TJNQMF TJOHMF ESJWFS
FOWJSPONFOUBM DIBOHF 'JSTU JG UIF OVNCFS
 SINGLE AND MULTIDRIVER ENVIRONMENTAL CHANGE REVERT AFTER ABOUT 
PG JOEFQFOEFOU USBJUT VOEFS TFMFDUJPO JODSFBTFT BT UIF OVNCFS
  GENERATIONS OF EVOLUTION )N FUTURE AQUATIC ENVIRONMENTS 
PG ESJWFST JO UIF FOWJSPONFOU JODSFBTFT QMFJPUSPQJD JOUFSBDUJPOT
 POPULATIONS WILL ENCOUNTER DIFFERING COMBINATIONS OF DRIVERS AND 
DPVME MJNJU BEBQUBUJPO JO DPNQMFY FOWJSPONFOUT NPSF UIBO JO
 INTENSITIES OF SELECTION WHICH WILL ALTER THE ADAPTIVE POTENTIAL OF 
TJNQMF POFT 
 4FDPOE JG TFMFDUJPO JOUFOTJUZ JODSFBTFT BT UIF
 PRIMARY PRODUCERS !CCURATELY GAUGING THE INTENSITY OF SELECTION 
OVNCFS PG ESJWFST JODSFBTFT UIFO UIF QSPCBCJMJUZ PG QPQVMBUJPO
 ON KEY PRIMARY PRODUCERS WILL HELP IN PREDICTING POPULATION SIZE 
FYUJODUJPO JODSFBTFT XJUI UIF OVNCFS PG ESJWFST CVU TVSWJWJOH
 AND TRAIT EVOLUTION AT THE BASE OF AQUATIC FOOD WEBS 
QPQVMBUJPOT XJMM BEBQU NPSF BOE NPSF SBQJEMZ JO FOWJSPONFOUT
 
XJUI NPSF ESJWFST 5IFTF UXP NFDIBOJTNT IBWF EJGGFSFOU FDPMPH
 
MULTIPLE ENVIRONMENTAL DRIVERS | ADAPTATION | MICROBIAL EVOLUTION | JDBM DPOTFRVFODFT *G EJGGFSFODFT JO FWPMVUJPOBSZ SFTQPOTFT BSF
 
#HLAMYDOMONAS NBJOMZ EVF UP EJGGFSFODFT JO QMFJPUSPQZ VOEFS NVMUJESJWFS DIBOHF
 
 
)NTRODUCTION
 
 " HSPXJOH CPEZ PG FWJEFODF GSPN FYQFSJNFOUT TIPXT UIBU GVOD 3IGNIlCANCE 
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PS $0 MFWFMT 
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 TIDRIVER ENVIRONMENTS &UNCTIONAL TRAITS CELL SIZE CHLOROPHYLL 
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QSFTFOU 5IJT IFMQT MJOL QBUUFSOT PG DPNQMFY NVMUJESJWFS
FOWJ GLOBAL CHANGE AND THE POTENTIAL RAMIlCATIONS FOR THEIR FUNC
 TION IN AQUATIC ECOSYSTEMS 
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 " TNBMM OVNCFS PG FYQFSJNFOUT IBWF JOWFTUJHBUFE UIF QMBTUJD 
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 5IFTF TUVEJFT DPOTJTUFOUMZ TIPX UIBU CPUI QMBTUJD BOE FWPMVUJPOBSZ 
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WWWPNASORG 0.!3 )SSUE $ATE 6OLUME )SSUE .UMBER  


 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 &IG  3CHEMATIC DIAGRAM ILLUSTRATES THE EXPERIMENTAL DESIGN OF THE 
STUDY ! 4HE FOUNDING POPULATION WAS ESTABLISHED FROM ONE COLONY OF #
 
REINHARDTII GROWN FROM A SINGLE CELL " 4HE FOUNDING POPULATION WAS GROWN
 FOR ONE WEEK UNDER CONTROL CONDITIONS THEN SPLIT INTO NINETY SIX DIFFERENT

 REGIMES SQUARE BOXES WITH ONE TO EIGHT ENVIRONMENTAL DRIVERS REGIMES 
 ARE SHOWN AS DIFFERENT PATTERN BACKGROUNDS AND A CONTROL ENVIRONMENT 
 WHITE BACKGROUND  # 0OPULATIONS EVOLVED IN EACH REGIME FOR NINETY 
 lVE TRANSFERS 4HIS PROVIDES ENOUGH TIME FOR ADAPTIVE VARIANTS TO ARISE AND 
 INCREASE IN FREQUENCY $ !FTER NINETY lVE TRANSFERS THE MULTIDRIVER EVOLVED 




Submission PDF
POPULATIONS WERE ASSAYED IN THEIR REGIME AND THE CONTROL ENVIRONMENT 4HE
CONTROL POPULATIONS WERE ASSAYED IN ALL TEST REGIMES

XF FYQFDU UIBU TIJGUT JO DPNNVOJUJFT SFTVMU NBJOMZ GSPN DIBOHFT






 
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AVERAGE NUMBER OF CELL DIVISIONS D  RELATIVE TO CONTROL POPULATIONS ASSAYED
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 GPS UIJT FYQFSJNFOUBM EFTJHO NFBO UIBU PVS GJOEJOHT DBOOPU CF RATE OF CONTROL POPULATIONS IN THE CONTROL ENVIRONMENT 
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MJHIU BCTPSQUJPO 
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BOE QSFEBUJPO 
 
 SFEVDFE MJHIU JOUFOTJUZ SFEVDFE QIPTQIBUF BDJEJGJDBUJPO SFEVDFE 
OVUSJFOUT BOE UIF BEEJUJPO PG IFSCJDJEF GPS ∼ BTFYVBM HFO 2ESULTS
 
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Submission PDF SFTQPOTF JODSFBTJOH XJUI UIF OVNCFS PG ESJWFST B IJHIFS QSP
QPSUJPO PG SFHJNFT DPOUBJOFE QPQVMBUJPOT XJUI B QPTJUJWF EJSFDU
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&OOTLINE !UTHOR 0.!3 )SSUE $ATE 6OLUME )SSUE .UMBER 


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BOE DIMPSP TVHHFTU UIBU JU DPVME BMTP CF VTFGVM XIFO DPOTJEFSJOH IPX QSJNBSZ 
 

Submission PDF
QIZMM BVUPGMVPSFTDFODF QFS DFMM WPMVNF JO FWPMWFE QPQVMBUJPOT QSPEVDFST NBZ FWPMWF VOEFS EJGGFSFOU DMJNBUF DIBOHF DMVTUFST
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GPS EJGGFSFOU UBYB XIFO BTTFTTJOH XIFUIFS PS 
QPQVMBUJPOT JO UIF DPOUSPM FOWJSPONFOU  ±  µN  NFBO
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± 4%
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–
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NPEFMFE SFHJPOBM DIBOHFT UP NVMUJESJWFS
 
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UP NBLF RVBMJUBUJWF QSFEJDUJPOT BCPVU TIJGUT JO CJPHFPHSBQIZ
 
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 WWWPNASORG &OOTLINE !UTHOR


 UIF DPOUSPM FOWJSPONFOU QSPEVDF TNBMM DFMMT BOE IJHI QSPQPS EVDFST FWPMWF JO NVMUJESJWFS FOWJSPONFOUT " TFDPOE DIBMMFOHF 
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SFEVDFE QIPTQIBUF 
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Submission PDF
MBUJPO GJUOFTT UIF GJSTU CFOFGJDJBM NVUBUJPO GJYFE PGUFO IBT B MBSHF DPOUSPM FOWJSPONFOU BSF DPOUSPM QPQVMBUJPOT "MM QPQVMBUJPOT
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BOE DBO DIBOHF TFWFSBM USBJUT TJNVMUBOFPVTMZ 5IJT NBZ XFSF QSPQBHBUFE CZ CBUDI DVMUVSF 4FF 4* "QQFOEJY GPS EFUBJMT 
 CF GPMMPXFE CZ DPNQFOTBUPSZ NVUBUJPOT UIBU JODSFBTF GJUOFTT CZ 
"TTBZT PG QPQVMBUJPO HSPXUI SBUFT
 SFWFSTJOH UIF FGGFDU PG UIF JOJUJBM NVUBUJPO PO USBJUT XIFSF DIBOHF 
"O BDDMJNBUJPO QFSJPE PG POF USBOTGFS DZDMF XBT VTFE GPS BMM
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 4FDPOE IFSJUBCMF FQJHFOFUJD NVUBUJPOT 
BTTBZT TFF 4*

 PS USBOTHFOFSBUJPOBM QMBTUJDJUZ DBO DPOUSJCVUF UP FBSMZ BEBQUBUJPO 
 5IF BWFSBHF SBUF PG DFMM EJWJTJPO QFS EBZ XBT DBMDVMBUFE PWFS 

CVU FWFOUVBMMZ CF SFQMBDFE CZ HFOFUJD NVUBUJPOT –
 6O B TJOHMF CBUDI DVMUVSFMFOHUI UJNF VTJOH FRVBUJPO  
 4FF 4*
 EFSTUBOEJOH IPX USBJU SFWFSTJPO JT MJOLFE UP BEBQUBUJPO QSFTFOUT BO 
 "QQFOEJY GPS EFUBJMT 
PQQPSUVOJUZ UP JNQSPWF PVS QSFEJDUJPOT PG GVODUJPOBM USBJU WBMVFT
 JO QSJNBSZ QSPEVDFST JO BRVBUJD FOWJSPONFOUT 
 -BCPSBUPSZ FWPMVUJPO FYQFSJNFOUT VTF TJNQMJGJFE FOWJSPO 
 NFOUT BOE QPQVMBUJPOT UP HBJO JOTJHIUT JOUP UIF GVOEBNFOUBM 
 BDUJPO PG OBUVSBM TFMFDUJPO "QQMZJOH UIF SFTVMUT PG UIJT FYQFSJNFOU 
()
 UP OBUVSBM QIZUPQMBOLUPO QPQVMBUJPO SFRVJSFT UBLJOH JOUP BDDPVOU 
 IPX QPQVMBUJPO TJ[F BOE EJWFSTJUZ BNPOH PUIFS GBDUPST TVDI BT /U JT UIF DFMM EFOTJUZ DFMMT NM
BU UJNF U IPVST
BOE /  JT UIF DFMM 
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BGGFDU BEBQUBUJPO 
 1SFWJPVT XPSL IBT EFOTJUZ BU UJNF U  
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 QPQVMBUJPOT UP FWPMWF GBTUFS –
 4JNJMBSMZ SFDPNCJOBUJPO UIF HSPXUI PG B NVMUJESJWFSFWPMWFE QPQVMBUJPO BOE B DPOUSPM 
 BOE QMBTUJDJUZ  
DBO CPUI TQFFE VQ BEBQUBUJPO 
5IF QPQVMBUJPO JO UIF TBNF NVMUJESJWFS SFHJNF 'JH 
 5IF EJSFDU 
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TJHIU JOUP IPX OBUVSBM TFMFDUJPO XPSLT BQQMZJOH UIFTF JOTJHIUT SF UP UIF OVNCFS PG EJWJTJPOT E
PG UIF DPOUSPM QPQVMBUJPO JO UIF
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SFMFWBOU SFHJNF 4FF 4* "QQFOEJY GPS EFUBJMT
 BOE GPS UIF TQFDJGJD CJPMPHZ PG XJME QPQVMBUJPOT 
 
 #ONCLUSIONS 
 () 
 8F TIPX UIBU QPQVMBUJPOT BEBQU NPSF JO SFTQPOTF UP EPNJOBOU  
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7E THANK ! 0HILLIMORE AND * (ADlELD FOR DISCUSSION ON STATISTICS ( 


+UEHNE AND - 7ATERFALL FOR TECHNICAL AND mOW CYTOMETRY ASSISTANCE 4HIS
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