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0%230%#4)6%
)NSECT RESISTANCE TO "T CROPS EVIDENCE VERSUS THEORY
"RUCE % 4ABASHNIK !ARON * 'ASSMANN $AVID 7 #ROWDER 9VES #ARRIRE
%VOLUTION OF INSECT RESISTANCE THREATENS THE CONTINUED SUCCESS
OF TRANSGENIC CROPS PRODUCING "ACILLUS THURINGIENSIS "T TOXINS
THAT KILL PESTS 4HE APPROACH USED MOST WIDELY TO DELAY INSECT
RESISTANCE TO "T CROPS IS THE REFUGE STRATEGY WHICH REQUIRES
REFUGES OF HOST PLANTS WITHOUT "T TOXINS NEAR "T CROPS TO PROMOTE
SURVIVAL OF SUSCEPTIBLE PESTS (OWEVER LARGE
SCALE TESTS OF THE
REFUGE STRATEGY HAVE BEEN PROBLEMATIC !NALYSIS OF MORE THAN
A DECADE OF GLOBAL MONITORING DATA REVEALS THAT THE FREQUENCY
OF RESISTANCE ALLELES HAS INCREASED SUBSTANTIALLY IN SOME FIELD
POPULATIONS OF (ELICOVERPA ZEA BUT NOT IN FIVE OTHER MAJOR PESTS
IN !USTRALIA #HINA 3PAIN AND THE 5NITED 3TATES 4HE RESISTANCE
OF ( ZEA TO "T TOXIN #RY!C IN TRANSGENIC COTTON HAS NOT CAUSED
WIDESPREAD CROP FAILURES IN PART BECAUSE OTHER TACTICS AUGMENT
CONTROL OF THIS PEST 4HE FIELD OUTCOMES DOCUMENTED WITH
MONITORING DATA ARE CONSISTENT WITH THE THEORY UNDERLYING THE
REFUGE STRATEGY SUGGESTING THAT REFUGES HAVE HELPED TO DELAY
RESISTANCE
RESISTANCE IF ONE OR MORE POPULATIONS WITH A HISTORY OF EXPOSURE TO THE
TOXIN IN THE FIELD ARE LESS SUSCEPTIBLE THAN CONSPECIFIC FIELD POPULATIONS OR
LABORATORY STRAINS THAT HAVE HAD LESS EXPOSURE $ECREASED SUSCEPTIBILITY
IS TYPICALLY DEMONSTRATED AS A SIGNIFICANT INCREASE IN THE TOXIN CONCENTRA
TION KILLING ,# OF THE INSECTS TESTED OR IN THE PERCENTAGE OF INSECTS
SURVIVING EXPOSURE TO A FIXED AMOUNT OF TOXIN ,ABORATORY DOCUMENTA
TION OF RESISTANCE HOWEVER DOES NOT ALWAYS INDICATE CONTROL PROBLEMS IN
THE FIELD
)N THE SECTIONS BELOW WE ANALYZE THE RESULTS OF STUDIES FROM !USTRALIA
#HINA 3PAIN AND THE 5NITED 3TATES MONITORING THE RESISTANCE TO "T CROPS
IN FIELD POPULATIONS OF SIX MAJOR INSECT PESTS (ELICOVERPA ARMIGERA ( ZEA
(ELIOTHIS VIRESCENS /STRINIA NUBILALIS 0ECTINOPHORA GOSSYPIELLA AND 3ESAMIA
NONAGRIOIDES .EXT FOR EACH OF THESE SIX PESTS WE COMPARE THE EVIDENCE
FROM MONITORING STUDIES TO RESULTS FROM COMPUTER MODELING OF RESISTANCE
EVOLUTION THAT IS BASED ON THE THEORY UNDERLYING THE REFUGE STRATEGY 7E
CONCLUDE WITH A DISCUSSION OF THE IMPLICATIONS OF OUR FINDINGS FOR MANAG
ING INSECT RESISTANCE TO CURRENT AND FUTURE TRANSGENIC CROPS
2APID RESPONSES TO LABORATORY SELECTION SHOW THAT MANY PESTS NATURALLY
HARBOR GENETIC VARIATION IN SUSCEPTIBILITY TO "T TOXINS AND THUS HAVE THE
POTENTIAL TO EVOLVE RESISTANCE TO "T CROPS IN THE FIELDn !LTHOUGH SOME
NEWER VARIETIES OF "T CROPS PRODUCE TWO "T TOXINS HTTPWWWEPAGOV
PESTICIDESBIOPESTICIDESPIPSPIP?LISTHTM WE FOCUS HERE ON FIRST
GENERA
TION "T CROPS THAT TARGET LEPIDOPTERAN PESTS AND PRODUCE ONLY ONE "T TOXIN
COTTON PRODUCING "T TOXIN #RY!C REFERRED TO HEREAFTER AS "T COTTON AND
CORN PRODUCING "T TOXIN #RY!B REFERRED TO HEREAFTER AS "T CORN "T COT
TON AND "T CORN HAVE BEEN GROWN ON MORE THAN MILLION HA WORLDWIDE
GENERATING ONE OF THE LARGEST SELECTIONS FOR INSECT RESISTANCE EVER KNOWN
4HE THEORY UNDERLYING THE REFUGE STRATEGYn FOR DELAYING INSECT RESISTANCE
IS THAT MOST OF THE RARE RESISTANT PESTS SURVIVING ON "T CROPS WILL MATE WITH
ABUNDANT SUSCEPTIBLE PESTS FROM REFUGES OF HOST PLANTS WITHOUT "T TOXINS
)F INHERITANCE OF RESISTANCE IS RECESSIVE THE HYBRID OFFSPRING PRODUCED BY
SUCH MATINGS WILL BE KILLED BY "T CROPS MARKEDLY SLOWING THE EVOLUTION
OF RESISTANCE 2ESULTS FROM MODELS AND SMALL
SCALE EXPERIMENTS SUGGEST
THAT REFUGES CAN DELAY RESISTANCE BUT COMPARISONS BETWEEN OBSERVED AND
PREDICTED OUTCOMES IN COMMERCIAL AGRICULTURE HAVE BEEN LIMITEDn
4HE MAJOR PESTS TARGETED BY "T CROPS HAVE BEEN MONITORED FOR THE EVOLU
TION OF RESISTANCE WHICH IS A HERITABLE DECREASE IN A POPULATIONS SUSCEPTI
BILITY TO A TOXIN 3USCEPTIBILITY IS USUALLY MEASURED BY SAMPLING INSECTS
FROM A FIELD POPULATION AND DETERMINING HOW THEIR PROGENY RESPOND TO
THE TOXIN IN LABORATORY BIOASSAYS 3UCH BIOASSAYS DOCUMENT FIELD
EVOLVED
%VIDENCE FROM RESISTANCE MONITORING STUDIES
!NALYSIS OF THE PUBLISHED MONITORING DATA FOR SIX MAJOR LEPIDOPTERAN PESTS
TARGETED BY "T CROPS SHOWS FIELD
EVOLVED RESISTANCE IN ( ZEA BUT NOT IN
( ARMIGERA ( VIRESCENS / NUBILALIS 0 GOSSYPIELLA OR 3 NONAGRIOIDES
4ABLE AND &IG %VALUATION OF THE LARGE DATASETS FROM TWO LANDMARK
STUDIES REVEALS RESISTANCE TO #RY!C IN SOME FIELD POPULATIONS OF ( ZEA
FROM !RKANSAS AND -ISSISSIPPI &IG BUT NOT IN CONCURRENTLY TESTED POP
ULATIONS OF ( VIRESCENS FROM THE SAME REGION 4ABLE &IELD SAMPLING OF
BOTH PESTS WAS DONE FROM TO IN THE FIRST STUDY AND FROM TO
IN THE SECOND STUDY ENABLING COMPARISON OF EACH PESTS SUSCEPTIBILITY
BEFORE AND AFTER THE COMMERCIALIZATION OF "T COTTON "OTH STUDIES USED
BIOASSAYS INVOLVING TOXIN INCORPORATED IN THE DIET TO DETERMINE THE ,#
OF #RY!C FOR STRAINS DERIVED FROM FIELD POPULATIONS AND FOR LABORATORY
STRAINS THAT WERE NOT EXPOSED TO "T TOXINS 4HESE DATA ALLOW CALCULATION OF
RESISTANCE RATIOS WHICH ARE ,# VALUES OF FIELD
DERIVED STRAINS DIVIDED BY
,# VALUES OF CONSPECIFIC SUSCEPTIBLE LABORATORY STRAINS 2ESISTANCE RATIOS
ARE MOST LIKELY TO REFLECT HERITABLE DECREASES IN SUSCEPTIBILITY &OR THE
TWO PEST SPECIES IN WHICH RESISTANCE TO "T SPRAYS EVOLVED OUTSIDE OF THE
LABORATORY THE INITIAL DOCUMENTATION WAS BASED ON RESISTANCE RATIOS UP TO
FOR 0LUTELLA XYLOSTELLA FROM FIELD POPULATIONS AND FOR 4RICHOPLUSIA
NI FROM GLASSHOUSES
"IOASSAY RESULTS FOR ( ZEA SAMPLED DURING AND IN !RKANSAS
AND -ISSISSIPPI SHOW RESISTANCE RATIOS FOR #RY!C FOR SIX FIELD
DERIVED STRAINS INCLUDING RESISTANCE RATIOS FOR FOUR STRAINS AND
FOR TWO &IG AND 3UPPLEMENTARY -ETHODS ONLINE $ATA FROM
FIELD POPULATIONS SAMPLED IN AND ALSO DEMONSTRATE ( ZEA
RESISTANCE TO #RY!C YIELDING RESISTANCE RATIOS FOR SEVEN ADDI
TIONAL STRAINS FROM !RKANSAS INCLUDING TWO STRAINS WITH RESISTANCE RATIOS
REF )N CONTRAST FIELD POPULATIONS OF ( ZEA SAMPLED IN
53! #URRENT ADDRESS $EPARTMENT OF %NTOMOLOGY )OWA 3TATE 5NIVERSITY
!MES )OWA 53! #ORRESPONDENCE SHOULD BE ADDRESSED TO "%4
BRUCET AGARIZONAEDU
0UBLISHED ONLINE &EBRUARY DOINBT
.!452% ")/4%#(./,/'9 6/,5-% .5-"%2 &%"25!29
0%230%#4)6%
&IGURE &IELD
EVOLVED RESISTANCE OF (ELICOVERPA ZEA TO "T COTTON DEMONSTRATED
BY INCREASES IN THE MEDIAN LETHAL CONCENTRATION ,# OF THE "T TOXIN
#RY!C FOR FIELD POPULATIONS A "EFORE THE COMMERCIALIZATION OF "T COTTON
n REF NO SIGNIFICANT DIFFERENCE IN ,# VALUES EXISTED
BETWEEN FIELD
DERIVED STRAINS MEAN N AND LABORATORY STRAINS
MEAN N -ANN
7HITNEY 5
TEST 5 0 B !FTER
THE COMMERCIALIZATION OF "T COTTON n REF ,# VALUES WERE
SIGNIFICANTLY HIGHER FOR FIELD
DERIVED STRAINS MEAN N THAN FOR
LABORATORY STRAINS MEAN N 5 0 !RROWS
SHOW THE SIX FIELD
DERIVED STRAINS WITH ,# &OR THESE SIX STRAINS THE
RESISTANCE RATIOS FROM 4ABLE OF REF WERE & & &
& & & 3UPPLEMENTARY -ETHODS
&
&
%VIDENCE VERSUS THEORY
4O DETERMINE WHETHER FIELD OUTCOMES ARE CONSISTENT WITH THE THEORY
UNDERLYING THE REFUGE STRATEGY WE MODELED RESISTANCE EVOLUTION IN EACH
OF THE SIX MAJOR PESTS LISTED IN 4ABLE 7E USED THE SAME BASIC POPULA
TION GENETIC MODEL FOR ALL PESTS INCORPORATING REALISTIC ESTIMATES OF THE
KEY BIOLOGICAL PARAMETERS FOR EACH SPECIES 3UPPLEMENTARY -ETHODS AND
3UPPLEMENTARY 4ABLE ONLINE &OR EACH PEST WE USED SENSITIVITY ANALYSIS
TO ASSESS HOW RESISTANCE EVOLUTION MIGHT BE AFFECTED BY VARIATION IN THE
RELATIVE ABUNDANCE OF REFUGES OF NON
"T HOST PLANTS
4HE MODELING RESULTS ARE IN ACCORD WITH THE PATTERNS DOCUMENTED BY
MONITORING DATA SUGGESTING THAT THE PRINCIPLES OF THE REFUGE STRATEGY
APPLY IN THE FIELD FOR THIS SET OF PESTS AND "T CROPS &IG A #ONSISTENT
WITH THE MONITORING DATA THE MODELING RESULTS INDICATE THAT ( ZEA IS
EXPECTED TO EVOLVE RESISTANCE FASTER THAN THE OTHER PESTS &IG A 7ITH
REALISTIC ESTIMATES OF REFUGE ABUNDANCE INCORPORATED THE MODELING
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4ABLE 'LOBAL MONITORING OF RESISTANCE OF SIX MAJOR PESTS TO THE "T TOXINS IN TRANSGENIC CROPS
,OCATION
&IELD SAMPLE
9EARS
0ARAMETER
)NITIAL
&INAL
!USTRALIA
STRAINS
n
MAX 22
!USTRALIA
FAMILIES
n TO n
R FREQ
#HINA
STRAINS
n
SURVIVAL
#HINA !NCI
FAMILIES
n
R FREQ
#HINA 8IAJIAN
FAMILIES
n
R FREQ
53!
STRAINS
n TO n
MAX 22
.#
FAMILIES
n
R FREQ
53!
STRAINS
n TO n
MAX 22
,! AND 48
MALES
n
R FREQ
53!
FAMILIES
n
R FREQ
3PAIN
STRAINS
n
MAX 22
!:
STRAINS
n
R FREQ
!: #!48
INSECTS
n
R FREQ
3PAIN
STRAINS
n
MAX 22
3PAIN
FAMILIES
n
R FREQ
(ELICOVERPA ARMIGERA
(ELICOVERPA ZEA
(ELIOTHIS VIRESCENS
/STRINIA NUBILALIS
0ECTINOPHORA GOSSYPIELLA
3ESAMIA NONAGRIOIDES
6/,5-% .5-"%2 &%"25!29 .!452% ")/4%#(./,/'9
0%230%#4)6%
.!452% ")/4%#(./,/'9 6/,5-% .5-"%2 &%"25!29
RESULTS ARE ALSO CONSISTENT WITH THE MONITORING
DATA SHOWING THAT FIELD
EVOLVED RESISTANCE OF
"
( ZEA TO #RY!C OCCURRED FASTER IN !RKANSAS
AND -ISSISSIPPI THAN IN .ORTH #AROLINA 4ABLE
#
'USTAFSON ET AL METICULOUSLY ESTIMATED THAT
THE EFFECTIVE REFUGE ABUNDANCE DURING EACH OF
THREE GENERATIONS WHEN ( ZEA FED ON COTTON WAS
IN !RKANSAS AND -ISSISSIPPI AND IN
.ORTH #AROLINA 7ITH THESE REFUGE SIZES ( ZEA
IS PROJECTED TO EVOLVE RESISTANCE AFTER YEARS IN
!RKANSAS AND -ISSISSIPPI "Y CONTRAST IN .ORTH
!
#AROLINA RESISTANCE EVOLUTION SHOULD TAKE
!
YEARS WITH THE EXPECTED RESISTANCE ALLELE FRE
&IGURE 3IMULATED EFFECT OF REFUGE ABUNDANCE ON PEST RESISTANCE TO "T CROPS 4HE CRITERION FOR
QUENCY STILL AFTER YEARS
RESISTANCE WAS A RESISTANCE R ALLELE FREQUENCY A 2ESISTANCE EVOLUTION IN SIX MAJOR PESTS
!LTHOUGH THE RESULTS SUGGEST THAT HIGH REF
MODELED WITH REALISTIC ESTIMATES FOR KEY BIOLOGICAL PARAMETERS 3UPPLEMENTARY 4ABLE (A (ELICOVERPA
UGE ABUNDANCE IN .ORTH #AROLINA DELAYED ARMIGERA (Z (ELICOVERPA ZEA (V (ELIOTHIS VIRESCENS /N /STRINIA NUBILALIS 0G 0ECTINOPHORA
RESISTANCE IN ( ZEA AN ALTERNATIVE HYPOTHESIS GOSSYPIELLA 3N 3ESAMIA NONAGRIOIDES &OR /N WITH A REFUGE RESISTANCE EVOLUTION REQUIRED YEARS
IS THAT INITIAL SUSCEPTIBILITY TO #RY!C WAS AND THE R ALLELE FREQUENCY WAS AFTER YEARS &OR (V WITH A REFUGE RESISTANCE EVOLVED IN
GREATER IN .ORTH #AROLINA THAN IN !RKANSAS YEARS B %FFECT OF DOMINANCE H ON RESISTANCE EVOLUTION IN A GENERIC PEST 7ITH H AND A REFUGE
RESISTANCE EVOLUTION REQUIRED YEARS AND THE R ALLELE FREQUENCY INCREASED FROM TO IN
AND -ISSISSIPPI (OWEVER MONITORING DATA YEARS
FROM AND SHOW THE OPPOSITE PATTERN
INITIAL SUSCEPTIBILITY TO #RY!C WAS GREATER IN
-ISSISSIPPI THAN IN .ORTH #AROLINA )N ADDITION THE RAPID RESPONSE TO #ONCLUSIONS AND IMPLICATIONS
LABORATORY SELECTION IN A STRAIN STARTED FROM LARVAE COLLECTED FROM /UR ANALYSIS SHOWS THAT LABORATORY BIOASSAYS OF ( ZEA DOCUMENT THE FIRST
.ORTH #AROLINA IN DEMONSTRATES THE PRESENCE OF GENETIC VARIA
CASE OF FIELD
EVOLVED RESISTANCE TO A "T TOXIN PRODUCED BY A TRANSGENIC
TION FOR RESISTANCE TO #RY!C 3ELECTION WITH #RY!C IN DIET YIELDED CROP !LTHOUGH TESTS OF SURVIVAL ON "T COTTON PLANTS FROM NEONATE TO ADULT
FOLD RESISTANCE IN EIGHT GENERATIONS IN THE .ORTH #AROLINA STRAIN HAVE NOT BEEN REPORTED FOR FIELD
SELECTED RESISTANT STRAINS OF ( ZEA THE
SIMILAR TO THE
FOLD RESISTANCE ATTAINED IN SEVEN GENERATIONS OF SELEC
AVAILABLE EVIDENCE SUGGESTS THAT SURVIVAL ON "T COTTON IN THE FIELD IS HIGHER
TION IN A COMPOSITE STRAIN STARTED IN FROM INSECTS COLLECTED IN FOR RESISTANT POPULATIONS THAN FOR SUSCEPTIBLE POPULATIONS 3USCEPTIBLE
-ISSISSIPPI AND 4EXAS 4HESE COMPARABLE RESPONSES TO SELECTION SUGGEST STRAINS OF ( ZEA SHOW SOME SURVIVAL ON "T COTTON WHICH MEANS
THAT GENETIC VARIATION FOR RESISTANCE WAS SIMILAR IN THE TWO INDEPEN
THAT ANY DECREASE IN SUSCEPTIBILITY TO #RY!C COULD INCREASE SURVIVAL
-OREOVER IN GREENHOUSE EXPERIMENTS WITH "T COTTON PLANTS SURVIVAL
DENTLY SELECTED STRAINS
!S SEEN FOR ( ZEA IN .ORTH #AROLINA RELATIVELY HIGH REFUGE ABUNDANCES WAS FOR A LABORATORY
SELECTED STRAIN WITH
FOLD RESISTANCE TO
ARE ASSOCIATED WITH THE OBSERVED LACK OF FIELD
EVOLVED RESISTANCE TO #RY!C #RY!C COMPARED WITH FOR A FERAL STRAIN !LSO IN BIOASSAYS WITH
FOR ( ARMIGERA IN !USTRALIA AND #HINA 0 GOSSYPIELLA IN !RIZONA AND 3 NON
"T COTTON LEAVES A FIELD
DERIVED STRAIN OF ( ZEA FROM -ISSISSIPPI WITH
AGRIOIDES IN 3PAIN )N !USTRALIA "T COTTON PRODUCING #RY!C WAS LIMITED FOLD RESISTANCE TO #RY!C HAD SURVIVAL VERSUS FOR A SUSCEPTIBLE
TO OF TOTAL COTTON PLANTED PROVIDING A MINIMUM REFUGE )N STRAIN !CCORDINGLY ,UTTRELL AND !LI STATE THAT THEIR RESULTS SUGGEST
#HINA SMALL FIELDS OF "T COTTON ARE CLOSE TO FIELDS OF OTHER NON
"T CROPS THE LOW SUSCEPTIBILITY OF SOME FIELD
DERIVED STRAINS WAS hHERITABLEv AND
PROVIDING REFUGES THAT ACCOUNTED FOR n OF THE AVAILABLE HOSTS FOR hASSOCIATED WITH A MEASURABLE INCREASE IN SURVIVAL ON "T PLANT TISSUEv
( ARMIGERA IN EACH PROVINCE )N !RIZONA THE MEAN REFUGE ABUNDANCE 4HEY ALSO NOTE THAT STRAINS STARTED BY COLLECTING LARVAE SURVIVING ON "T
WAS CLOSE TO RANGING FROM TO PER COUNTY )N 3PAIN REF
COTTON PLANTS IN THE FIELD hTENDED TO HAVE REDUCED SUSCEPTIBILITY SUGGEST
UGE ABUNDANCE WAS ABOUT #ONSISTENT WITH THE MONITORING DATA ING THAT SOME COMPONENT OF THE OBSERVED FIELD CONTROL PROBLEMS MAY
( VIRESCENS AND / NUBILALIS WERE NOT PROJECTED TO EVOLVE RESISTANCE IN BE ASSOCIATED WITH THE PRESENCE OF RESISTANCE GENESv
YEARS EVEN WITH THE SMALLEST REFUGE EXAMINED
.ONETHELESS RESISTANCE OF ( ZEA TO #RY!C HAS NOT CAUSED WIDESPREAD
3UPPORTING THE THEORY UNDERLYING THE REFUGE STRATEGY DOMINANT INHERI
CONTROL FAILURES FOR SEVERAL REASONS &IRST EVEN IN THE FEW STATES WITH DOCU
TANCE OF RESISTANCE TO #RY!C APPEARS TO HAVE HASTENED THE EVOLUTION OF MENTED RESISTANCE MOST POPULATIONS TESTED WERE NOT RESISTANT TO #RY!C
RESISTANCE IN ( ZEA 4HE HYBRID PROGENY PRODUCED BY MATINGS BETWEEN &IG 3ECOND INSECTICIDES HAVE BEEN USED FROM THE OUTSET TO AUGMENT
A LABORATORY
SELECTED RESISTANT STRAIN AND A SUSCEPTIBLE STRAIN OF ( ZEA CONTROL OF ( ZEA ON "T COTTON BECAUSE #RY!C ALONE IS NOT SUFFICIENT
WERE RESISTANT TO #RY!C YIELDING A DOMINANCE VALUE H OF TO CONTROL HIGH
DENSITY POPULATIONS OF THE PEST )NSECTICIDE SPRAYS
3UPPLEMENTARY 4ABLE WHERE INDICATES COMPLETELY RECESSIVE AND DECREASE ANY PROBLEMS ASSOCIATED WITH REDUCED CONTROL OF ( ZEA BY "T
COMPLETELY DOMINANT INHERITANCE /F THE FIVE OTHER MAJOR PESTS EXAMINED COTTON 4HIRD AGAINST STRAINS WITH
TO
FOLD RESISTANCE TO #RY!C
HERE ( ARMIGERA IS THE ONLY ONE WITH LABORATORY
SELECTED RESISTANCE TO "T THE #RY!C IN "T COTTON STILL CAUSED n LARVAL MORTALITY &INALLY
CROP PLANTS THAT IS NOT COMPLETELY RECESSIVE H 3UPPLEMENTARY @PYRAMIDED TRANSGENIC COTTON PRODUCING "T TOXINS #RY!B AND #RY!C
WAS REGISTERED IN $ECEMBER AND PLANTED ON MORE THAN MILLION
4ABLE
#ONSISTENT WITH THE MONITORING DATA MODELING RESULTS FOR A GENERIC HA IN THE 5NITED 3TATES IN AND REF #ONTROL OF #RY!C
PEST OF "T CROPS SHOW THAT WHILE ALL OTHER FACTORS ARE HELD CONSTANT THE RESISTANT ( ZEA BY #RY!B ALSO LIMITS PROBLEMS ASSOCIATED WITH RESISTANCE
DOMINANCE OF RESISTANCE H AND THE REFUGE ABUNDANCE GREATLY AFFECT THE TO #RY!C
RATE OF RESISTANCE EVOLUTION &IG B 7ITH COMPLETELY RECESSIVE INHERI
.EGATIVE EFFECTS OF ( ZEA RESISTANCE TO #RY!C SHOULD FURTHER DIMINISH
TANCE OF RESISTANCE TO "T CROPS H REFUGES OF r ARE EXPECTED TO AS USE OF COTTON THAT PRODUCES ONLY #RY!C DECREASES AND USE OF TWO
TOXIN
DELAY RESISTANCE YEARS IN THE GENERIC PEST /N THE OTHER HAND WITH H COTTON WITH #RY!B AND #RY!C INCREASES )N THE 53 THE AREA PLANTED
TO COTTON PRODUCING ONLY #RY!C DECLINED FROM MILLION HA IN
r REFUGES OF ARE NEEDED FOR DELAYS OF YEARS
0%230%#4)6%
TO MILLION HA IN REF !LSO -ONSANTOS 53 REGISTRATION OF
#RY!C COTTON IS SCHEDULED TO EXPIRE IN 3EPTEMBER HTTPWWWEPA
GOVOPPBPPDBIOPESTICIDESPIPSPIP?LISTHTM &OR ( VIRESCENS WHICH
HAS REMAINED SUSCEPTIBLE TO #RY!C AND IS ALSO SUSCEPTIBLE TO #RY!B
COTTON PRODUCING BOTH OF THESE TOXINS MAY GREATLY DELAY RESISTANCE &OR
#RY!C
RESISTANT POPULATIONS OF ( ZEA HOWEVER THE TWO
TOXIN COTTON
MAY ACT LIKE SINGLE
TOXIN COTTON WITH CONTROL EXERTED PRIMARILY BY #RY!B
)F SO THE POTENTIAL BENEFITS OF PYRAMIDING THESE TWO TOXINS FOR DELAYING
RESISTANCE WILL NOT BE FULLY REALIZED )N -AY 3YNGENTA APPLIED FOR
53 REGISTRATION OF TRANSGENIC COTTON WITH THE PYRAMID OF THE "T TOXINS
6IP!A AND #RY!B HTTPWWWEPAGOVFEDRGSTR%0!
0%34-AY
$AY
PHTM WHICH WOULD PROVIDE ANOTHER OPTION FOR CONTROLLING
KEY LEPIDOPTERAN PESTS INCLUDING ( ZEA AND ( VIRESCENS -ORE GENERALLY
OPTIONS FOR PEST CONTROL WITH TRANSGENIC CROPS HAVE BEEN BROADENED BY
THE DEVELOPMENT OF CORN WITH "T TOXINS THAT KILL CORN ROOTWORMS AND MAY
BE FURTHER EXPANDED BY GENE
SILENCING TECHNOLOGY AND MODIFIED "T TOXINS
DESIGNED TO KILL RESISTANT PESTSn
4HE SUSTAINED EFFICACY OF THE FIRST GENERATION OF "T CROPS FOR A DECADE
AGAINST NEARLY ALL TARGETED PEST POPULATIONS HAS EXCEEDED THE EXPECTATIONS
OF MANY 4HE EXCEPTIONAL CASE ( ZEA RESISTANCE TO "T COTTON PRODUC
ING #RY!C IS CONSISTENT WITH THE THEORY UNDERLYING THE REFUGE STRATEGY
BECAUSE THIS RESISTANCE IS NOT RECESSIVE )N OTHER WORDS THE CONCENTRATION
OF #RY!C IN "T COTTON IS NOT HIGH ENOUGH TO KILL THE HYBRID OFFSPRING
PRODUCED BY MATINGS BETWEEN SUSCEPTIBLE AND RESISTANT ( ZEA 4HUS THE
SO
CALLED @HIGH DOSE REQUIREMENT IS NOT MET !S THE SECOND DECADE OF
TRANSGENIC CROP USE BEGINS KNOWLEDGE GAINED FROM SYSTEMATIC ANALYSES
OF MONITORING DATA FROM THE FIRST DECADE CAN HELP TO MINIMIZE THE RISKS
AND MAXIMIZE THE BENEFITS 4HE RESULTS SUMMARIZED HERE SUGGEST THAT THE
REFUGE STRATEGY CAN DELAY RESISTANCE TO "T CROPS ESPECIALLY WHEN RESISTANCE
IS RECESSIVE AND REFUGES ARE ABUNDANT
.OTE 3UPPLEMENTARY INFORMATION IS AVAILABLE ON THE .ATURE "IOTECHNOLOGY WEBSITE
!#+./7,%$'-%.43
7E ARE ESPECIALLY GRATEFUL TO 2 ,UTTRELL ! -ATHIAS 7 -OAR $ /NSTAD - 3ISTERSON
AND + 7U FOR COMMENTS AND SUGGESTIONS 4HIS WORK WAS SUPPORTED BY THE .ATIONAL
2ESEARCH )NITIATIVE THE #OOPERATIVE 3TATE 2ESEARCH %DUCATION AND %XTENSION 3ERVICE
AND 5NITED 3TATES $EPARTMENT OF !GRICULTURE GRANT
#/-0%4).'