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THE CONTRIBUTION OF BREEDING

TO YIELD ADVANCES IN MAIZE

(ZEA MAYS L.)

Donald N. Duvick

Iowa State UniversityAmes, Iowa 50011

I. I
ntroduction
83

Advances in Agronomy, Volume 86Copyright 2005, Elsevier Inc. All rights reserved.

0065-2113/05 $35.00

A
. M aize Yield Trends During the Past Century B . F actors Responsible for Upward Yield Trends
II. G
enetic Gains in Grain Yield of Hybrids A . P reviously Reported Genetic Yield Gains B . R ecent Estimates of Genetic Yield Gains C . E stimates of the Contribution of Breeding to Total Yield Gains D . C hanges that Have Accompanied Genetic Yield Gains in Hybrids
I
II. G enetic Gains from Population Improvement A . C omparisons with Genetic Gains in Hybrids B . R elative Contributions of Population Improvement and
Pedigree Breeding
I V. A nalysis and Conclusions
A
. P ossible Reasons for Genetic Yield Gains B . P otential Helps or Hindrances to Future Gains in Yield C . P redictions R eferences
Maize (Zea mays L.) yields have risen continually wherever hybrid maize

has been adopted, starting in the U.S. corn belt in the early 1930s. Plant

breeding and improved management practices have produced this gain joint-

ly. On average, about 50% of the increase is due to management and 50% to

breeding. The two tools interact so closely that neither of them could have

produced such progress alone. However, genetic gains may have to bear a

larger share of the load in future years. Hybrid traits have changed over the

years. Trait changes that increase resistance to a wide variety of biotic and

abiotic stresses (e.g., drought tolerance) are the most numerous, but mor-

phological and physiological changes that promote efficiency in growth,

development, and partitioning (e.g., smaller tassels) are also recorded.

Some traits have not changed over the years because breeders have intended

to hold them constant (e.g., grain maturity date in U.S. corn belt). In other

instances, they have not changed, despite breeders’ intention to change them

84 DONALD N. DUVICK

(e.g., harvest index). Although breeders have always selected for high yield,

the need to select simultaneously for overall dependability has been a driving

force in the selection of hybrids with increasingly greater stress tolerance

over the years. Newer hybrids yield more than their predecessors in unfavor-

able as well as favorable growing conditions. Improvement in the ability of

the maize plant to overcome both large and small stress bottlenecks, rather

than improvement in primary productivity, has been the primary driving

force of higher yielding ability of newer hybrid. # 2005, Elsevier Inc.

I. INTRODUCTION

A. MAIZE YIELD TRENDS DURING THE PAST CENTURY

Maize yields began to rise markedly in many countries during the past

century, first in the United States in the 1930s and then in other parts of the

world in the 1950s and 1960s. For example:

• U.S. yields, level at approximately 1.5 mg ha�1 in the first three decades

of the 20th century, started to rise significantly in the 1930s, reaching

8.5 mg ha�1 by the end of the century (USDA-NASS, 2003b). The U.S.

yield gains averaged 63 kg ha�1 year�1 from 1930–1960 and 110 kg ha�1

year�1 during the next 40 years (Troyer, 2000).

• Maize yields in Canada tripled during the period 1940–2000, increasing

from 2.5 to 7.5 mg ha�1, a linear increase of 80 kg ha�1 year�1 (Bruulsema

et al., 2000).

• Maize yields in Germany doubled in the period 1965–2000, going from

4 to 8 mg ha�1 (Frei, 2000).

• Maize yields in France quadrupled in the period 1950–1984, increasing

from 1.5 to 6.0 mg ha�1 (Derieux et al., 1987).

• In Argentina, the national mean maize yield increased “at a rate of 2.3%

per year from 1970–1992” (Eyherabide et al., 1994).

Table I summarizes yield gain data for several regions of the world during

the period 1961–2002. Globally, maize yields doubled during this time, from

1.9 to 4.3 mg ha�1, a linear increase of 61 kg ha�1 year�1. Different regions

varied in the size of annual gain, as well as in average yields at the beginning

and the end of the interval, but all showed positive and significant gains with

the exception of eastern Europe (highly variable in the past decade) and

southern Africa (minimal gain and highly variable during entire period).

Yields in south Asia did not start to rise significantly until the 1980s; annual

gains since 1985 have averaged 38 kg ha�1 year�1.

Table I

Maize Yield Trends in Selected Regions (1961–2002)a

Region1961 mean

(mg ha�1)

2002 mean

(mg ha�1)

Annual gainb

(kg ha�1 year�1) R2c

European Union (15) 2.5 9.1 169 0.98

USA 3.9 8.2 109 0.83

China 1.2 5.0 103 0.96

Canada 4.6 7.6 69 0.77

World 1.9 4.3 61 0.95

South America 1.4 3.4 48 0.87

Eastern Europe 1.8 4.2 42 0.38

South Asia 1.0 1.7 20 0.78

Southern Africa 0.7 1.3 8 0.26

aFrom FAO Statistical Databases (2004) http://apps.fao.org/default.htm.bLinear regression coefficients, calculated from annual means, 1961–2002.cCoefficient of determination.

ADVANCES IN MAIZE 85

These exampl es and other data show that maiz e y ields have increa sed

signi ficantly in man y regions of the worl d dur ing the latter half of the 20th

century , especi ally in those places wher e maiz e is gro wn as a co mmercial crop.

B. FACTORS RESPONS IBLE FOR UPWARD Y IELD TRENDS

1. Cultural Practi ces

Change s in cultura l practi ces have been respo nsible for a signifi cant

porti on of maiz e yield gains. Crop managem ent practices, such as weed

and pest con trol, timeli ness of plan ting, and increa sed effici ency of harvest

equ ipment, have impro ved over the years, especially (but not exclus ively) in

the indust rialized coun tries (e.g., Car dwell, 198 2; Edm eades and Tollenaa r,

1990 ).

Perha ps most impor tantl y, the use of synthetic nitr ogen fert ilizers

increa sed marke dly starting in the years afte r World War II when plentiful

and affor dable supp lies be came avail able, first in the ind ustrialized coun tries

and then in many (but not all) of the developi ng countri es (e.g ., Car dwell,

1982; Edmeades and Tollenaa r, 1990; Miquel, 20 01 ). Total fert ilizer app lica-

tions on all cro ps worldw ide increa sed fiv efold during the pe riod 1961–199 2.

The linea r increa se started from an average applic ation of about 20 kg ha� 1

in 1962 and reached 105 kg ha� 1 in 1992 ( USDA -ERS, 2003 ). How ever, in

some co untries, app lication amoun ts of synthetic nitr ogen fertilizer did not

fit this gen eral trend; they be gan to level off in the 1980s. Applicati on of

http://apps.fao.org/default.htm

86 DONALD N. DUVICK

commercial nitrogen fertilizer to maize plantings in the United States rose

from an average of 58 kg ha�1 in 1964 to 157 kg ha�1 in 1985, but since then

has stabilized at approximately 145–150 kg ha�1 (Daberkow et al., 2000;

USDA-ERS, 2003). It would seem, therefore, that yield gains of U.S. maize

since the mid-1980s cannot be attributed to application of increasing

amounts of nitrogen fertilizer on maize plantings.

Plant density—the number of maize plants per hectare—also increased

steadily through the years following World War II in the United States as

well as in other countries. The increase was more or less in step with increases

in application amounts of fertilizer nitrogen. In the central U.S. corn belt,

plant density averaged about 30,000 plants hectare�1 (or less) in the 1930s;

it began to increase in the late 1940s and 1950s, reaching about 40,000 plants

hectare�1 in the 1960s, 60,000 plants hectare�1 in the 1980s, and is often

at 80,000 plants hectare�1 or higher at present (Duvick, 1977, 1984a, 1992;

Duvick et al., 2004b; Paszkiewicz and Butzen, 2001; USDA, 1949–1992).

During the past 50 years, plant density in the central U.S. corn belt has

increased at an average rate of about 1000 plants hectare�1 year�1.

2. Plant Breeding

a. Farmer Breeding. Genetic improvements, as well as cultural

improvements, can contribute to an increased yield of maize. Farmer bree-

ders, beginning with the people who first domesticated maize, have selected

plants and cultivars to fit their wants and needs and, in so doing, have

developed thousands of landraces adapted to a multitude of environments,

as well as with a wide range of morphological and quality traits (e.g.,

Goodman and Brown, 1988; Grobman et al., 1961; Paterniani and Good-

man, 1977). We can assume that a higher yield, or at least an acceptable and

dependable level of yield, was always a desired trait for maize cultivars, as

well as for those of other staple grain crops.

Although long-term yield trends are not recorded for specific farmer

breeding programs, a general observation indicates that when crop varieties

are grown in a new environment (e.g., when migrants carry their favorite

cultivars to a new land), the cultivars often do not perform as well as

intended. Careful selection in the unadapted cultivars, often coupled with

hybridization to cultivars from elsewhere, then is used to develop genetically

different cultivars that are better adapted to the new environment and

therefore yield more (and more dependably) than the first introductions.

Examples in U.S. history are the 19th century development of hard red

winter wheat (Triticum aestivum L.) cultivars for Kansas (Malin, 1944) and

“Corn Belt Dent” maize open pollinated cultivars (OPCs) for U.S. corn belt

states such as Illinois and Iowa (Wallace and Brown, 1988).

Figure 1 United States maize yields, annual average, 1900–2003. FromUSDA-NASS (2003a).


Farmers developed adapted maize OPCs for the U.S. corn belt states in a

relatively short time (Hallauer and Miranda, 1988; Wallace and Brown,

1988). Within a few decades after settlement of the region in the early

years of the 19th century, maize yields and general performance of the new

“Corn Belt Dent” cultivars were at acceptable levels in most parts of the

region. However, from then on, gains in yield were small or nonexistent.

This is evidenced by the lack of gain in U.S. maize yields during the first

three decades of the 20th century (Fig. 1).

One could suppose that the lack of yield gain during those decades was

because maize-growing areas in the country changed in location and extent

over time and therefore were not always equivalent in productivity. How-

ever, in the states of Iowa and Illinois, where maize-growing areas and

cultural practices were relatively constant during this period, yields were

essentially unchanged also. Yields in those states were level at approximately

2.3 mg ha�1 during the years 1900–1930 (USDA-NASS, 2003a). It would

seem that farmer breeders in the corn belt, using selection techniques of that

time [primarily mass selection based on individual plant performance

(Sprague, 1952)], could not raise maize yields further than the levels attained

in the initial development of adapted cultivars.

New breeding methods were tried in the late 19th and early 20th centuries.

The production of varietal hybrids (first generation crosses of two maize

OPCs) was tried and abandoned because of unreliable results (e.g., Crabb,

1993; Richey, 1922). A few professional breeders in the public sector

(USDA) worked on variety improvement in the 1920s using relatively

88 DONALD N. DUVICK

unsophisticated methods of mass selection or ear-to-row breeding (Crow,

1998; Russell, 1991; Sprague, 1946, 1994). Their efforts did not increase

yields either, except when a program provided adaptation to a new environ-

ment. These breeders, working in the first decades of the 20th century, lacked

access to the present-day knowledge of experimental design, statistical anal-

ysis, and quantitative genetics. Lack of these tools must have hindered their

progress.

b. Hybrids. U.S. maize yields started to increase when maize hybrids

made from crosses of inbred lines were introduced in the early 1930s. Du-

ring the next few years the increase in maize yield was correlated with the

increase in the proportion of maize area planted to hybrids (USDA,

1944 – 1962; USDA-NASS, 2003a). Yields in Iowa increased from 2 mg

ha�1 to 3.5 mg ha�1 in the period 1933–1943, as the percentage of maize

area planted to hybrids went from 0.7 to 99%. U.S. maize yields rose from

1.5 mg ha�1 in 1933 to 2.4 mg ha�1 in 1950, as the percentage of area planted

to hybrids went from 0.1 to 78%. In either case, yield gains took place before

a significant increase in use of synthetic nitrogen fertilizers or chemical

control of weeds and insects (Cardwell, 1982; USDA, 1956), so it seems

likely that the yield gains primarily were caused by genetic improvements;

the new hybrids yielded more than the OPCs that they replaced, and succes-

sive hybrids yielded even more.

Maize yields began to rise in conjunction with the introduction of hybrids in

other countries as well (Cunha Fernandes and Franzon, 1997; Derieux et al.,

1987; Eyherabide et al., 1994; Frei, 2000; Tollenaar, 1989), although, as in the

United States, improved crop management techniques usually accompanied

the introduction of hybrid maize; plant breeding and crop management jointly

contributed to the sharp increases in maize yields. The proportion of gain

attributed to genetic improvements is treated in more detail in later sections,

with emphasis on hybrids and how sequential changes in their breeding and

genetics have contributed to increased on-farm yield.

c. Improved Populations. In the United States, the first hybrids were

made from inbreds that had been developed by selfing some of the better

OPCs of the 1920s. Breeders then worked to develop a second generation of

improved hybrids using new inbreds made by selfing the same OPCs. They

found that the second round of hybrids yielded little or no more than the

first; it seemed that breeders must have selected most of the superior geno-

types in the initial round of selfing in the OPCs. Some of the breeders

conjectured that it might be possible to make new “synthetic” OPCs, with

a potential for production of a superior second generation of inbred lines, by

intercrossing some of the best inbreds from the first round of OPC selfing

(Baker, 1990).


To this end, the breeders made several “synthetics” by intercrossing

the better inbreds of the day. Research in maize quantitative genetics

had begun by this time, and some of the populations were subjected to

various kinds of selection to make genetic improvements in the popula-

tions as such. The selection procedures were based on various assumptions

about gene action and genetic variability (Hallauer and Miranda, 1988;

Sprague, 1946, 1966). The Iowa State University Stiff Stalk Synthetic

(BSSS) (Eberhart et al., 1973; Sprague, 1946) is one of the best known of

these populations. Sprague (1946) lists the 16 progenitor inbred lines of this

synthetic.

Breeders practiced population improvement on other kinds of popu-

lations as well, such as locally adapted OPCs, exotic landraces, or compo-

sites of exotic landraces and/or inbred lines (e.g., Hallauer and Miranda,

1988; Sriwatanapongse et al., 1985). The name “recurrent selection” was

coined (Sprague, 1952) to distinguish these kinds of population improve-

ments from pedigree breeding (i.e., developing improved inbred lines from

crosses of proven inbreds). Depending on the prospective end user, breeders

intended to develop improved populations that would serve as sources of

superior inbred lines or that could be used directly as productive cultivars

per se. Results of their work are discussed in a later section.

II. GENETIC GAINS IN GRAIN YIELD OF HYBRIDS

A. PREVIOUSLY REPORTED GENETIC YIELD GAINS

Russell (1991) has summarized 16 independent estimates of genetic

yield gains of sequentially released maize hybrids. Most of the estimates

are based on comparisons of U.S. hybrids and were reported at intervals

during the 20-year period of 1971–1991. Estimates ranged from 25–92 kg

ha�1 year�1 with a mean of 57 kg ha�1 year�1. It seems likely that the wide

range in values was caused, in part, by differing growing conditions among

the several investigations and consequent differential interactions with old or

new genotypes. Other factors, as well, might explain some of the variation,

as follows:

• Breeding might have been less effective in some regions (such as those with

erratic and often severe abiotic stress) than in others.

• Choice of the time series of hybrids for comparison could have had major

effect on size of measured gain. For example, a short time series might

show less improvement than a long one if the short time series happened to

sample a period with small genetic gain.

90 DONALD N. DUVICK

• Plant density of trials could affect the results differentially; older hybrids

could have been disadvantaged if the plant density at which their yield

was measured was higher than that for which they were bred or new

hybrids could be disadvantaged if the density was below that which they

required for maximum yield.

• Harvest technology could be another source of difference; e.g., combine

harvested trials (as compared with hand-harvested trials) could under-

estimate yields of older hybrids if combines failed to pick up all downed

stalks (and ears) of older hybrids with poor standability. Conversely,

hand-harvested trials could overestimate yields of the older hybrids if a

standard shelling percentage was used to convert ear corn weight to grain

weight instead of shelling the ears and weighing the shelled grain. Use of a

standard shelling percentage could inflate estimates of grain weight on

poorly pollinated nubbins of the older hybrids.

However, these possibilities must remain conjecture. The salient fact is

that all of the experiments listed by Russell showed positive and linear

genetic yield gains, fluctuating around a mean of about 60 kg ha�1 year�1.

Additional estimates of genetic gain in hybrids have been made since

Russell’s review and are summarized in the following section.

B. RECENT ESTIMATES OF GENETIC YIELD GAINS

1. Argentina

Elite experimental maize hybrids tested in 154 regional trials in the

Argentine corn belt during the 1979–1991 period had an estimated linear

genetic gain of 105 kg ha�1 year�1 (Eyherabide et al., 1994). Estimates were

based on comparisons with a common check.

A second series of estimates extended the period (1979–1998) and showed

an estimated genetic gain of 107 kg ha�1 year�1, or 2.9% year�1. Further

analysis of these data indicated that gains were not linear during the entire

period; gains were greater in the second decade than in the first, perhaps in

part because of the introduction of single cross hybrids in the 1990s (Eyher-

abide and Damilano, 2001).

2. Brazil

Analysis of 30 years of national maize trials in Brazil (1963–1993) indi-

cates linear genetic progress of 123 kg ha�1 year�1 (Cunha Fernandes and

Franzon, 1997). Trials were grown in three locations, and estimates were

based on comparisons with a moving base of common entries.


3. United States

Duvick (1997), updating previous reports for hybrids adapted to central

Iowa in the U.S. corn belt, stated that a time series of hybrids and one OPC

representing the period from 1930–1991 showed a linear gain for grain yield

of 74 kg ha�1 year�1. The estimate was based on data from trials comparing

36 hybrids and one OPC, conducted over a period of 4 years, three locations

per year, at three plant densities per location. Yield for each hybrid was for

its “optimum density” in the trials: the plant density at which it gave its

highest mean yield.

A further update extended this time series through the year 2001; it

showed an estimated linear gain of 77 kg ha�1 year�1 (Duvick et al.,

2004b). This estimate applied “best linear unbiased predictors” (BLUPs) of

hybrid grain yield; it was based on trials of 51 hybrids and four OPCs grown

at three plant densities in the years 1991–2001, using yield of each hybrid at

its “optimum density” as described earlier.

C. ESTIMATES OF THE CONTRIBUTION OF BREEDING

TO TOTAL YIELD GAINS

Russell (1991) listed 14 estimates of genetic yield gain of hybrids as

percent of total yield gain. (Total yield gain was defined as on-farm gain

for appropriate regions during the time span of hybrids that were com-

pared.) Most of the comparisons were for the U.S. corn belt but the list

also included estimates for Ontario (Canada), France, and Yugoslavia.

Estimates of genetic gain varied from 29 to 94%, with a mean of 66%.

As noted by Russell (1991), several reasons can be advanced to show that

this broad variability could be caused by inconsistencies in planning and

executing the experiments, such as machine harvest vs hand harvest, or

whether experimental estimates of genetic gain were adjusted to on-farm

state averages. Nevertheless, all estimates agree in showing that hybrid maize

breeding (i.e., genetic improvement) has played a major part in raising

maize yields.

Among the reports of genetic gain since Russell’s summary (reviewed in

Section II.B), Cunha Fernandes and Franzon (1997) estimated that 57% of

total gain in yield in Brazil was due to genetics. The other reports did not

contain such an estimate, but further examination of data in Duvick et al.

(2004b) provides an estimate of 51% for the contribution of genetics, when

trial yields are adjusted to the equivalent of average on-farm yields for Iowa

during the period 1930–2001.

Based on these and earlier estimates, one can state that hybrid maize

breeding during the past six or seven decades has been responsible for 50 to

92 DONALD N. DUVICK

60% of the total on-farm yield gain. However, one also must acknowledge

that the interaction between breeding and management (cultural practices) is

such that neither tool could have caused the gains without aid of the other;

changes in breeding and management continually have interacted in positive

fashion.

D. CHANGES THAT HAVE ACCOMPANIED GENETIC YIELD GAINS

IN HYBRIDS

Breeders have noted that genetic gains in grain yield of hybrids may be

accompanied by changes in other traits, sometimes as a result of direct

selection, sometimes without direct intention by the breeders. And some

traits have stayed essentially unchanged over the generations. Three reviews

in the previous decade (Edmeades and Tollenaar, 1990; Russell, 1991;

Tollenaar et al., 1994) have given detailed accounts of such changes and

are recommended as sources of information and informed commentary on

the topic prior to the early 1990s. The following sections update those

accounts, as well as provide summaries and commentary for some of the

earlier research reports.

1. Plant and Ear Traits

a. Plant and Ear Height. Plant and ear height were reduced in the

second era but not thereafter in a study of single cross hybrids representing

U.S. corn belt hybrids of three eras: 1930s, 1950s, and 1970s (Meghji et al.,

1984). A study of 28 hybrids and four OPCs adapted to Iowa, representing

seven decades culminating in the 1980s, found no trend to reduction in plant

height but a continuing trend to reduction in ear height (Russell, 1984).

Plant height for a 1930–2001 time series of 51 hybrids and four OPCs

adapted to central Iowa likewise was essentially unchanged over the years,

but ear height showed a weak trend toward reduced height, approximately

�3 cm decade�1 (Duvick et al., 2004b).

b. Leaf Angle. Leaves became more upright in the 1970s era in a com-

parison of single crosses representing U.S. corn belt hybrids of three eras:

1930s, 1950s, and 1970s (Meghji et al., 1984). Leaf orientation below and

above the ear became more upright with time in a study of U.S. Midwestern

hybrids representing the decades from 1930–1970 (Crosbie, 1982; Russell,

1991). The trend to upright leaf orientationwas greatest above the ear. Russell

(1991) stated that the distinct increase in upright leaf orientation in the1970s

decade was probably because inbred B73, with upright leaves for its time, was


a parent in the set of 1970s single cross hybrids. The previously mentioned

1930–2001 time series of 51 hybrids and four OPCs for central Iowa (Duvick

et al., 2004b) showed a similar trend toward more upright leaf habit. Ratings

(as scores) in this study were for the entire plant.

c. Tassel Size. Tassel weight was least in the most recent era in com-

parisons of single cross hybrids representing U.S. corn belt hybrids of the

1930s, 1950s, and 1970s; tassel branch number decreased consistently over

the eras (Meghji et al., 1984). Tassel branch number and tassel weight

decreased over time in a 1930 to 1991 time series of hybrids for Iowa

(Duvick, 1997). Tassel branch numbers in the series averaged 2.5 fewer

branches per decade, and tassel dry weight declined, on average, 0.5 g per

decade. Reduction of tassel size continued in hybrids released during the

next 10 years, as evidenced by scores for tassel size of hybrids in the

1930–1991 time series extended to 2001 (Duvick et al., 2004b).

d. Leaf Number. Number of leaves per plant neither increased nor

decreased in a 1930–1991 time series of Iowa hybrids and OPCs (Duvick

et al., 2004b). Leaf number increased from 12.2 in the 1930s to 13.8 in the

1970s in comparisons of single cross hybrids representing U.S. corn belt

hybrids of the 1930s, 1950s, and 1970s (Meghji et al., 1984).

e. Leaf Area Index (LAI). Russell (1991) suggests that changes in LAI

“may be specific to the particular cultivars used, rather than a general

occurrence of all germplasm representative of similar eras.” This statement

is borne out by the lack of consistent trends across experiments conducted by

different researchers. LAI tended to be higher for recent hybrids than for

older ones in a time series of four hybrids grown in Ontario (Canada) from

1959 to 1989 (Dwyer et al., 1991; Tollenaar, 1991). In another investigation,

LAI increased over time in a set of eight maize hybrids that were commer-

cially important in central Ontario between 1959 and 1988 (Tollenaar, 1989).

However, a set of Iowa hybrids (20 single cross hybrids) representing the

decades of 1930–1970 showed no obvious trend (Crosbie, 1982; Russell,

1991), and a 1930–1991 time series of 36 commercial hybrids and one OPC

for Iowa also showed no change in LAI over time (Duvick, 1997).

f. Leaf Rolling. Leaf rolling of plants, especially in the vegetative stage,

is often seen when plants are subjected to drought. Leaf rolling consistently

increased in newer hybrids in a set of 18 commercial hybrids adapted to

central Iowa and representing the period 1953–2001 when the hybrids

(grown in a rain-free environment in Chile) were compared with and without

managed drought stress at various stages of development (Barker et al., 2005;

Edmeades et al., 2003). Commenting on this observation, Barker et al.

94 DONALD N. DUVICK

(2005) said “Apparently elite hybrids can reduce radiation interception and

water use by leaf rolling, while generating sufficient assimilate flux to the ear

to set adequate kernel numbers and conserving water for later in the season.”

g. Staygreen. Staygreen, also called delayed leaf senescence, or resis-

tance to premature death from unidentified causes, is consistently improved

in newer hybrids (Crosbie, 1982; Duvick et al., 2004b; Meghji et al., 1984;

Russell, 1991; Tollenaar, 1991). The improvement in each of these trials was

greatest under environmental stress such as that induced (or accentuated) by

high plant density. Staygreen improved over time in a set of 18 commercial

hybrids adapted to central Iowa and representing the period 1953–2001

when the hybrids, grown in a rain-free environment in Chile, were (a) well

watered, (b) subjected to induced drought at flowering time, or (c) subjected

to drought during the final grain-fill period (Barker et al., 2005). Genetic

gain for staygreen was greatest in the well-watered treatment and was least

under drought imposed during the grain-fill period.

h. Tillers. Number of tillers per 100 plants varied from hybrid to

hybrid, but decreased slightly on average in a 1930–1991 time series of

hybrids and OPCs for Iowa (Duvick et al., 2004b).

i. Anthesis. Date of anthesis varied among decades, but showed no

trend toward earlier or later dates in an Iowa series of four OPCs and

24 single cross hybrids representing the 1930s through 1980s (Russell,

1985). Similarly, heat units from planting to anthesis varied among hybrids

but showed no general trend toward earlier or later in a 1930–2001 time

series of 51 hybrids and four OPCs adapted to central Iowa (Duvick et al.,

2004b).

j. Silk Emergence. Silk emergence date trended toward earliness in an

Iowa series of four OPCs and 24 single cross hybrids representing the 1930s

through 1980s (Russell, 1985) and also in a 1930–1991 time series of 36

hybrids and one OPC for Iowa (Duvick, 1997). In the latter case, there was

little or no trend to an earlier silk date in absence of stress, such as at low

plant density, whereas higher plant density accentuated the trend, not be-

cause the new hybrids had earlier silking dates, but rather because the stress

of high plant density delayed silk emergence of the older hybrids.

k. Anthesis-Silking Interval (ASI). Anthesis usually precedes silk

emergence, and the interval between the two events is called the anthesis-

silking interval. (The term “silk delay” is also used.) ASI was unchanged in

hybrids representing earlier decades but was significantly shorter in hybrids


of the 1970s in a set of Iowa hybrids (20 single cross hybrids) representing

the decades of 1930–1970 (Crosbie, 1982). ASI became shorter in each

decade except the 1980s in an Iowa-adapted series of four OPCs and 24

single cross hybrids representing 1930–1980 (Russell, 1985). ASI was signifi-

cantly shorter in each interval in comparisons of single cross hybrids repre-

senting U.S. corn belt hybrids of the 1930s, 1950s, and 1970s (Meghji et al.,

1984). ASI showed a highly significant linear trend to shorter intervals in a

1930–2001 time series of 51 hybrids and four OPCs adapted to central Iowa

(Duvick et al., 2004b). The trend was greater in trials grown at higher plant

densities. ASI became shorter over time in a set of 18 commercial hybrids

adapted to central Iowa and representing the period 1953–2001 (Barker

et al., 2005; Edmeades et al., 2003). This trend was exhibited when the

hybrids were well watered and was accentuated when they were subjected

to induced drought at flowering time. The experiment was conducted in a

rain-free environment in Chile.

l. Ears per Plant. Both total and harvestable ears per plant increased

over the decades in a set of Iowa hybrids (20 single cross hybrids) representing

the decades of 1930–1970 (Crosbie, 1982). A 1930–2001 time series of 51

hybrids and four OPCs adapted to central Iowa showed a highly significant

trend toward more ears per 100 plants (+3.6 ears decade�1) (Duvick et al.,

2004b). However, ears per plant showed no change over the decades in an

Iowa-adapted series of four OPCs and 24 single cross hybrids representing

1930–1980 (Russell, 1985). The Russell experiment was planted at a single

density (51670 plants ha�1), whereas data for the other two experiments were

expressed as means of three densities in which the medium and high densities

were higher than optimum for the older hybrids and, therefore, were more

likely to cause barrenness in those hybrids. The end result would be a trend

towardmore ears per 100 plants (i.e., fewer barren plants) in the newer hybrids.

m. Grain-Filling Period. Newer hybrids had a longer period of grain

fill, calculated as time from silk emergence to black layer (physiological

maturity), in observations of four discrete time series of hybrids adapted to

the Midwestern United States (Cavalieri and Smith, 1985; Crosbie, 1982;

Meghji et al., 1984; Russell, 1985). The newer hybrids flowered at approxi-

mately the same time as the older hybrids, and although their grain-fill

periods were longer, they also exhibited a faster final dry-down rate, and

so had little or no delay in relative maturity (based on grain moisture

percentage at harvest time). The newer hybrids thus have more time to

devote to grain fill; they exhibit increased efficiency in use of the growing

season in the U.S. Midwest, which is limited on either end by average date of

last frost in spring and first frost in autumn.

96 DONALD N. DUVICK

n. Kernel Weight. Weight per 300 kernels increased in each decade

except the final one in an Iowa-adapted series of four OPCs and 24 single

cross hybrids representing seven eras from pre-1930s through the 1980s

(Russell, 1985). Kernel weight did not change significantly over the decades

except for a significant increase in the final (1970s) decade in comparisons of

20 single cross hybrids representing each decade from 1930–1970 (Crosbie,

1982). Weight per 100 kernels increased linearly in an Iowa-adapted series of

36 hybrids and one OPC representing the years 1930–1991, while number of

kernels per ear decreased slightly but not significantly (Duvick, 1997).

Weight per kernel exhibited a marked linear increase under well-watered

conditions and also under drought stress at flowering, early, and midfill

stages, but showed little or no increase under drought in late-fill and terminal

stages in a set of 18 Iowa-adapted hybrids (evaluated in Chile) representing

the period 1953–2002 (Barker et al., 2005; Edmeades et al., 2003). In ap-

praisal of the results summarized in this section: the general trend to

increased weight per kernel (and no increase in number of kernels per ear,

in the one series where this was measured) may indicate that assistance in

achieving genetic yield gain over time (and also gain in yield stability) is

given more efficiently by plants with increased kernel weight than by plants

with increased kernel number.

o. Grain Protein Percentage. Grain protein percentage declined con-

sistently in a series of 36 hybrids and one OPC for central Iowa spanning

the period 1930–1991 (Duvick, 1997). The loss averaged 0.3% protein dec-

ade�1, with a series mean of 9.8% protein.

p. Grain Starch Percentage. Grain starch percentage increased consis-

tently ina seriesof 36hybrids andoneOPCfor central Iowa spanning theperiod

1930–1991 (Duvick, 1997).The increaseaveraged0.3%starchperdecade,witha

series mean of 70.4% starch. Because production of starch requires less energy

than production of protein, selection for yield without attention to protein or

starch percentagemay have indirectly selected genotypeswith less grain protein

and more grain starch, giving a net increase in efficiency of grain production.

q. Harvest Index (HI). HI did not change consistently over time in

comparisons of single cross hybrids representing U.S. corn belt hybrids of

the 1930s, 1950s, and 1970s (Meghji et al., 1984). HI did not change consis-

tently in a set of 20 single cross hybrids representing Iowa hybrids of the

decades of the 1930s through 1970s (Crosbie, 1982) or in a series of nine

hybrids representing three decades (1959–1988) of maize production in

Ontario when hybrids were compared at optimum plant density for yield

for each hybrid (Tollenaar, 1989). HI did not change consistently over the

decades in an Iowa-adapted series of four OPCs and 24 single cross hybrids


representing 1930–1980 (Russell, 1985). HI improved on average to a small

degree in successive hybrids in a 1934–1985 time series of Iowa-adapted

hybrids (Duvick et al., 2004b) and in the same series extended to 1991

(Duvick, 1997). Higher plant density accentuated the trend. However, the

superior HI of the newer hybrids at higher plant densities was not because of

increased HI per se in the newer hybrids, but because of reduced HI in the

older hybrids—the result of barrenness induced by stress. At higher densities

the older hybrids maintained plant size but lost yield because of increased

percentages of barren or partially barren plants.

2. Resistance to Root Lodging

Hybrids improved over the years in resistance to root lodging in a series of

Iowa hybrids representing the decades 1930–1960 (Russell, 1974). However, a

later examination of a longer series of hybrids (1930–1980) showed no signifi-

cant improvement in root lodging resistance, although all hybrids were decid-

edly more resistant than the OPCs of the 1920s (Russell, 1984). Four

examinations of a successively lengthened time series of commercial hybrids

for central Iowa showed linear increases in resistance to root lodging, in each

examination (Duvick, 1977, 1984a, 1997; Duvick et al., 2004b). The four

experiments contained hybrids released in the years 1939–1971, 1934–1978,

1934–1991, and 1934–2001, respectively. However, in two other trials of this

series (for hybrids released in 1934–1989 and 1934–2000), improvement of

root strength ceased in the final decade at about the 95% nonroot-lodged level

(Duvick, 1992; Duvick et al., 2004a).

The intensity of root lodging in a given trial can influence the differentia-

tion between the older and the newer hybrids. Low levels of lodging (e.g.,

because of lack of the right combination of rain and wind or because of

insufficient plant density) will make it impossible to differentiate among the

more resistant hybrids because all will be in the range of 95 to 100% upright.

Also, from time to time new hybrids might be released with less resistance to

root lodging than intended, following which genetic improvements are

implemented in newer releases. Either of these conditions (abiotic or genetic)

could explain why apparent cessation of linear improvement in one time

series is followed by a later time series in which gains are linear.

3. Resistance to Stalk Lodging

Lodging resistance (not differentiated between root or stalk lodging)

improved significantly in a series of hybrids grown in France from

1950–1985 (Derieux et al., 1987). Higher plant densities accentuated the

difference between older and newer hybrids.

98 DONALD N. DUVICK

Stalk lodging resistance improved consistently in a time series of Iowa-

adapted hybrids representing 1930–1960 (Russell, 1974). However, in a

longer series (1930–1980), resistance to stalk lodging improved until the

1970s but did not improve in the 1980s (Russell, 1984).

Five different examinations of a successively lengthened time series of

commercial hybrids for central Iowa showed linear improvements in resis-

tance to stalk lodging (Duvick, 1977, 1984a, 1992, 1997; Duvick et al., 2004b).

The five series contained hybrids released in 1939–1971, 1934–1978,

1934–1989, 1934–1991, and 1934–2001. However, in one other trial for this

series (hybrids released from 1934–2000), improvement ceased in the final

decade at about the 95% nonstalk-lodged level (Duvick et al., 2004a).

So for both root lodging and stalk lodging, one can conclude that al-

though the overall trend is toward improved resistance to lodging, improve-

ment may seem to stop from time to time. Additional experiments involving

further extensions of the time series will be needed to test the validity of such

conclusions.

4. Tolerance to Abiotic Stress

a. High Temperatures. A 1930–1991 time series of 36 hybrids and one

OPC for Iowa exhibited a linear increase in grain yield in a low yield season

with a “hot and dry” summer, as well as in two highly favorable (exception-

ally high yield) seasons (Duvick, 1997). Weather records for the “hot and

dry” year (1991) indicate that temperatures during the flowering period were

higher than normal and precipitation was exceptionally low (Iowa State

University, 2003).

b. Low Temperatures. The aforementioned 1930–1991 time series also

exhibited a linear increase in grain yield in a “very cool and wet season”

(Fig. 2) (Duvick, 1997; Duvick et al., 2004b). Weather records for that trial

year (1993) indicate that precipitation amounts during the summer months

were at record-breaking high levels, and daytime high temperatures were

well below normal (Iowa State University, 2003).

Dwyer and Tollenaar (1989) stated that “genetic improvement in the

response to cold stress . . . has significant consequences for yield of field-

grown maize, since many Canadian seasons are subject to short seasons or

cool growing periods.” They showed (for a series of eight hybrids, released

during the years 1959–1988) that reduction in photosynthetic response to

irradiance (PRI) following a cold period during kernel fill was greater in

older than in newer hybrids. A subsequent study (Tollenaar et al., 2000)

showed similar results for a series of eight U.S. maize hybrids representing

the 1930s, 1950s, 1970s, and 1990s.

Figure 2 Grain yield per hybrid regressed on year of hybrid introduction for trials grown in

1992, 1993, and 2001. Seasons: 1992, highly favorable; 1993, cool and extremely wet; 2001, hot

and dry. Yield per hybrid is for the density giving the highest average yield. From Duvick et al.

(2004b). Copyright # 2004 by John Wiley & Sons, Inc. This material is used by permission of

John Wiley & Sons, Inc.


Frei (2000), reporting for maize production in northwestern Europe,

stated, “Breeding for adaptation to long and cool growing season has [led]

to changes in growth behavior and yield physiology. . . . There is good

evidence that low base temperature genotypes exist in northern breeding

programs. . . . Breeding for lower base-temperature or cold tolerance can

alleviate the stover versus grain antagonism.” [On a personal note, the

author has seen some short-season inbred lines from the northern U.S. and

Canada fail to make chlorophyll (white or striped seedling plants) in the cool

early summer of central Germany, while locally bred lines in the same

nursery were green and vigorous.]

c. Drought. Russell (1974) stated that in high stress drought environ-

ments, a group of commercial hybrids representing the most recent era

yielded considerably more than any other group. Hybrids and OPCs in the

trial were adapted to Iowa and represented the approximate period

1930–1970. Examination of another set of hybrids comparing decades

1930–1980 showed that the hybrids of the 1970s and 1980s had superior

100 DONALD N. DUVICK

yiel ds in all environm ents, which included two dro ught-stre ss locations an d

two high-y ieldin g en vironm ents ( Russell, 1991 ).

Com pariso n of a series of U.S. corn belt hybrids and OPC s repre-

senti ng the de cades 1930–198 0 showe d linear gains in grain yield unde r

eithe r dro ught stre ss or irrigat ed treatment s (Cas tleberry et al ., 1984 ). The

mean yield of the 1930s group was equal to 60% of the mean yield of

the 1980s grou p when both groups were subject ed to drough t stress, an d

63% of the mean y ield of the 1980s grou p when both gro ups were g iven full

irrigat ion.

In Onta rio, Canada , a ne wer hyb rid was more toleran t of sh ort dro ught

periods than an older hy brid (Dw yer et al ., 1992 ). Duri ng a dro ught period,

the ne wer hyb rid continued phot osynthes is for about 2 h longer than the

older one before star ting to decline . A furt her study indica ted that the tw o

hyb rids might adopt different mechani sms to tolerate mois ture stre ss

( Nissank a et al., 1997 ). The newer hy brid maint ained relative ly higher

rates of photo synthesis an d trans piration at a lower stem wate r potential.

Altho ugh one canno t con sider a compari son of only two hy brids as a “ time

seri es” that demonst rates trends over the years, exami nations like these

can give hints of pos sible trends and suggest profitabl e fie lds for futur e

invest igation.

Derie ux et al . (1987) , compari ng 33 maize hybrids (of three maturit y

group s) grow n in Fran ce from 1950–198 2, stat ed that modern hyb rids are

more adapted to stress, such as low temperature and drought. Regressions of

mean yield per decade of release on mean yield per location of trial consis-

tently showed that the newer the decade, the higher the yield at all locations.

Water stress limited yield in some locations, particularly for hybrids in the

semiearly category.

As not ed earlier in the sectio n “High Tem peratur es,” a 1930 to 1991 time

series of 36 hybrids and one OPC for Iowa exhibited a linear increase in

grain yield in a season (year 1991) with exceptionally low precipitation

during flowering, as well as in highly favorable seasons (Duvick, 1997).

The same series, further extended (1930–2001), showed a linear increase

in grain yield in another season (year 2000) when “heat and drought at

silking time caused reduced yields” (Duvick et al., 2004a), and also in a

third season (year 2001) when yields were low “because of a season-long

drought, especially severe at the sensitive anthesis-silking period” (Fig. 2)

(Duvick et al., 2004b). Weather records show that rainfall was well below

average during the anthesis-silking period in 2000, and also in 2001 (Iowa

State University, 2003).

A time series of 18 commercial hybrids adapted to central Iowa and

representing the period 1953–2001 showed linear gains in grain yield in

each of three different watering regimes. The hybrids (grown in a rain-free

environment in Chile) were (a) well watered, (b) subjected to drought at


flowering time, or (c) subjected to drought during the grain-fill period

(Barker et al., 2005; Edmeades et al., 2003). The hybrids in this experiment

were a subset of the series studied by Duvick et al. (2004b), discussed

previously. Gains in grain yield under optimal conditions were about twice

as large as gains when stress coincided with flowering or grain filling.

A time series of 2 OPCs and 52 hybrids adapted to central Iowa and

representing the years (for the hybrids) 1934–2001 was subjected to a man-

aged drought trial in Woodland, California (Barker et al., 2005). The

hybrids in this experiment were the same as those studied by Duvick et al.

(2004b), discussed previously. Watering regimes were similar to those de-

scribed for the experiment in Chile (described earlier). Trials were grown at

two plant densities. Both of the densities showed linear gains in grain yield

for all three watering regimes. Figure 3 shows results of the trial at high

density. Yield gain was greatest in the well-watered regime, although differ-

ences among the three regimes were not large. Annual genetic gains for all

watering regimes were greater in the trial grown at the higher density, typical

also of multidensity trials in rain-fed environments.

All of the experiments described in this section show that genetic yield

gains over time are expressed in drought as well as in favorable growing

Figure 3 Grain yield of two OPCs and 52 hybrids regressed against year of release. Hybrids

were grown in Woodland, California, at 90,000 plants ha�1 in three managed stress environ-

ments: full irrigation, flowering drought stress, or grain-filling drought stress. Adapted from

Barker et al. (2005).


seasons. On average, the newer the hybrid, the greater is its drought to-

lerance. Discussion in later sections suggests possible causes of this

improvement.

d. Excessi ve Soil Moisture. As noted ea rlier in this section (“Low Tem-

peratur es”), a 1930 to 1991 time series of Iowa hybrids showe d a linea r gain in

grain yield in a “very cool and wet season” (Duvick, 1997). That growing

season, 1993, was one of the wettest on record for the state of Iowa (precipi-

tation was two to three times normal), and soils were excessively moist (and in

some cases flooded, although not in these trials) during much of the summer

(Corrigan, 2003; Iowa State University, 2003). The linear gain in yield when

the 1930 to 1991 time series was grown in this unusually wet growing season

(see Fig. 2) indicates that although breeders had not selected directly for such

abnormally wet growing conditions, they must have done so indirectly,

perhaps through improvement in the ability of plants to set and develop

kernels in the presence of reduced photosynthesis per plant or in the ability

to tolerate a reduced uptake of key soil nutrients. One should note, however,

that yield gain was least (59 kg ha�1) in the flood year of 1993 (the lowest

yielding year) and greatest (82 kg ha�1) in the most favorable season, 1992.

e. Deficiency of Soil Nitrogen. Maize cultivars (OPCs and commercial

hybrids) typical of those grown in the U.S. corn belt in the decades 1930s

through 1980s were compared at high and low soil fertility levels (in trials

receiving approximately 200 kg ha�1 N, 90 kg ha�1 P2O5, and 150 kg ha�1

K2O versus trials in an area that, for two decades, had received no fertilizer

and was planted to continuous maize) (Castleberry et al., 1984). Yield gains

by decade were linear and positive under both of the soil fertility treatments

(high and low), although the average annual gain was greater in the high

fertility trial.

Single cross hybrids representing four decades (1940–1970) of U.S. corn

belt hybrids were compared at three levels (70, 130, and 200 kg ha�1) of

nitrogen (N) fertilizer application (Duvick, 1984a). The l970s decade gave

the highest grain yield at all N levels, and the 1960s decade produced the

second highest yield at all N levels. A second experiment, described in the

same report, compared five commercial hybrids spanning the period

1940–1978 at two treatments: high N, high plant density (215 kg N ha�1

and 54,000 plants ha�1) and low N, low plant density (70 kg N ha�1 and

35,000 plants ha�1) The two newest hybrids yielded more than the older ones

at either treatment level. In both experiments, the interaction of hybrids �N

rates was not statistically significant.

Carlone and Russell (1987) compared OPCs and a series of single cross

hybrids at three plant densities (34,445, 51,661, and 68,889 plants ha�1) and

four N fertilizer levels (0, 80, 160, and 240 kg ha�1). The single crosses were


chosen to represent hybrid genotypes of the decades 1930–1980. The trials

suffered severe moisture stress in both years of trial, 1983 and 1984. Com-

parisons used the yield of each era at its optimum plant density. Hybrids of

the older eras had their highest yield at lower densities; the newer hybrids

had their highest yield at the higher densities. The 1980s era had the highest

yield at each N level, and the 1970s era had the second highest yield at each

N level.

Carlone and Russell (1987) reported that levels of N fertilizer (0–240 kg

ha�1) interacted with plant densities and with hybrid genotype. The opti-

mum N level (level with highest yield) for hybrids of the 1940s, 1950s, and

1960s was higher than the optimum N level for hybrids of the 1970s and

1980s. However, the highest yields of the older group were lower than those

of the newer group at all N levels, so one might conclude that the newer

hybrids used N more efficiently than the older hybrids.

Carlone and Russell (1987) also showed that hybrids within an era

differed in response to densities and N levels. Two hybrids of the 1970s

group increased in yield as densities and N levels increased, but one hybrid

increased in yield significantly more than the other, such that the greatest

difference in yield between them was at the highest plant density and the

highest N level.

McCullough et al. (1994a) stated that when two hybrids were compared

in controlled environment chambers, an old hybrid (release year 1959) was

more sensitive than a new hybrid (release year 1988) to stress caused by low

soil N (0.5 mM) during early development. The new hybrid also maintained

a higher rate of leaf photosynthesis per unit of N regardless of N supply.

A second experiment (McCullough et al., 1994b) indicated that the higher

N-use efficiency of the new hybrid under low N supply “is associated with

higher N uptake and a higher leaf N per unit leaf area.” Field trials con-

firmed that the new hybrid yielded more than the old hybrid under both high

N and low N treatments (Tollenaar et al., 1994, 1997). The yield difference

between hybrids was accentuated when weeds were present, as compared

with weed-free conditions; one might conclude that the new hybrid was

also more “weed tolerant” than the old hybrid. As stated earlier, comparison

of only two hybrids representing “early” and “late” eras is not equivalent

to the study of trends in a time series of several hybrids, but the com-

parison can indicate possible changes over time and may suggest profitable

areas of future research to discover trait changes that accompany sequential

improvements in hybrid performance.

f. Unspecified Abiotic Stress—“Stress versus Nonstress” Environments.

Yield trial results can be categorized according to the average yield at

each test site. One can assume that the lower the yield at a given site

(in absence of obvious disease or insect problems), the greater the amount


of “unspecified” abiotic stress. A stability analysis of the kind proposed by

Eberhart and Russell (1966) can be used to compare yield response of

individual hybrids or of groups of hybrids such as those released in a given

decade. Yields of groups of hybrids (as in a decade) can be regressed on

mean yield at each test site (e.g., Figs. 4 and 5).

Russell (1991) cited such comparisons in several experiments. In general,

all experiments showed that the newest groups of hybrids had the highest

yields in all sites, regardless of average yield level at the site. However, linear

regressions (b), showing degree of response of each group of hybrids to

increasing site productivity, demonstrated no consistent trend of response.

In some cases, b values were similar for all eras, whereas in other cases, b

values were greater for new than for old eras, and in still other experiments,

the b values differed randomly among eras (e.g., Fig. 4). Russell concluded

that “there seems to be no distinct relationship between response and era of

the hybrids. More likely, the responses were specific for the genotypes.” He

Figure 4 Yield response, b, for open-pollinated cultivars (OPCs) and six hybrid groups of

10-year eras, 1930–1980, to eight environment indexes (four locations � 2 years). Reprinted

from Russell (1991), # 1991, with permission from Elsevier, and also with permission from W.

A. Russell and the Iowa State Journal of Research.

Figure 5 Mean grain yield of hybrids released within two-decade spans, and of three OPCs,

regressed on mean yield of all hybrids per environment. Trials were grown in a total of 13

environments during the years 1996–2000. Means of three densities per environment: 30,000,

54,000, and 79,000 plants ha�1. From Duvick et al. (2004b). Copyright# 2004 by JohnWiley &

Sons, Inc. This material is used by permission of John Wiley & Sons, Inc.


also consider ed the possibili ty that hand harvest vs machi ne harvest co uld

have intro duced a bias in some of the resul ts that he reviewed. (C ombines

might fail to ga ther ears of lodged plan ts, and because old er hybrids

tend to lodge mo re than newer hy brids, yiel ds of older hybrids woul d be

unde restima ted.)

Si nc e t he Russell (1991) report, Duvick et al. (2004b) p r e s en t e d r es ul ts f o r

42 commercial hybrids and four OPCs tested in 13 environments in central

Iowa during the years 1996–2000. They were grouped for stability analysis as

follows: OPCs, 1930s and 1940s, 1950s and 1960s, 1970s and 1980s, and 1990s

(Fig. 5). The regression for the OPCs was well below that for the hybrids,

at 0.65. Regression values were similar for all hybrid eras (b ¼ ca. 1.0), although

with a slight increase for the newest era. Thus, in this experiment the OPCs

showed markedly less response than the hybrids to higher yield environments

and the newest hybrid group gave the greatest response. However, in all cases,

the newer the era, the higher the yield in any location, low yield or high. Stress

tolerance increased significantly over the years.

In conc lusion, experi ments described in this section (“Toleran ce to

Abiot ic Stres s”) have shown that hyb rid toler ance to ab iotic stress has


increased consistently over the years. Although results are contradictory

regarding whether newer hybrids are more or less responsive than older

hybrids to higher yield environments, newer hybrids tend to be the most

responsive, sometimes strikingly so (e.g., Barker et al., 2005; Duvick, 1984a,

1992). Reasons for such variability in response are not known but probably

depend, as do most results, on interactions of genotype and environment.

5. Tolerance to Biotic Stress

a. Insects. A 1930–1991 time series of 36 hybrids and one OPC for

Iowa exhibited a linear increase in resistance to second-generation European

corn borer (Ostrinia nubilalis Hubner) (ECB2), as measured by tunnel

length following artificial infestation and by scores for evidence of natural

infestation in yield trials (Duvick, 1997). This improvement took place

even though breeders had not selected directly for resistance to ECB2.

The same series showed no improvement in resistance to first-generation

borer. Breeders and entomologists in the United States have collaboratively

produced inbreds and breeding populations with improved natural tolerance

and/or resistance to both generations of borer (see review in Russell, 1991),

but there is no record of how or if these materials were used in commer-

cial hybrids. They were not the source of increased resistance in the

aforementioned 1930–1991 time series.

In recent years (starting in 1996), seed companies have commercialized

transgenic maize hybrids that are resistant to ECB. These hybrids, common-

ly called Bt hybrids, have been genetically engineered to incorporate a gene

of Bacillus thuringiensis (Bt). Most of the first Bt hybrids contained the

gene that produces the insecticidal protein Cry1Ab. The toxic Bt protein is

effective against larvae from both first and second ECB generations

(Peferoen, 1992; Traore et al., 2000).

When subjected to artificial infestation, Bt hybrids showed significantly

less tunneling from second-generation borer than non-Bt hybrids (Traore

et al., 2000). They also had 9.7% more total plant weight in 1997 and 9.4%

more grain yield in 1998 than their non-Bt counterparts. However, the

amount of difference depended on the cultivar.

Under natural on-farm ECB infestation, Bt hybrids usually yield signifi-

cantly more than their isogenic counterparts in seasons when infestation is

relatively heavy, but not when infestation is light. In 14 yield trials in Iowa in

1997, nine Bt hybrids yielded 7% more than their near-isogenic counterparts

(Rice, 1997). Similar advantage for Bt hybrids was measured in several other

corn belt states in 1997, but in 1998 with lighter infestation the average yield

advantage was about one-fifth that of the 1997 amount (Gianessi and

Carpenter, 1999).


These data indicate that for Bt hybrids, as with other types of biotic and

abiotic stress tolerance, the amount of yield gain contributed by the benefi-

cial trait depends on the severity of the pertinent stress (in this case ECB

infestation). Thus, James (2003a) stated that global yield gains due to Bt

maize are currently estimated at 5% in the temperate maize-growing areas

and 10% in the tropical areas. The tropical areas have more and overlapping

generations of pests, leading to higher infestations and subsequently greater

yield loss, in absence of resistance contributed by Bt.

An additional restriction on potential yield gain from Bt hybrids is the

need to plant “refuge areas” (perhaps 20–30% of total) of non-Bt maize to

help prevent the development of resistance in the corn borer population

(Ostlie et al., 2002). Biologists theorize that the pest population will even-

tually develop/increase new genotypes that are not susceptible to the Bt

resistance genes, as has happened repeatedly (often in only a few seasons)

in other instances of major gene resistance [also called vertical resistance

(Simmonds, 1985; van der Plank, 1963)]. The use of refuge areas is intended

to delay such genotypic change as long as possible. The refuge areas of

course cannot provide the genetic yield advantage in the presence of corn

borer that is provided by the Bt hybrids.

More recently (in 2003), approval has been granted for use of a Bt transgene

that prevents root injury by larvae of two different species of rootworm

(Diabrotica barberi Smith & Lawrence, and Diabrotica virgifera virgifera

LeCont) (James, 2003b; Rice et al., 2003). This Bt protein is called Cry3Bb1;

it controls the rootworm larvae but not the adult beetle. As with Bt transgenic

protection against corn borer, genetic yield advantage of rootworm resistance

depends on the severity of infestation and its interaction with the environment.

“Yield trials demonstrated that under heavy rootworm pressure and moisture

stress the lack of corn rootworm larval injury in the [genetically engineered]

corn resulted in substantially higher yields than [in] cornwithout the Bt protein.

As rootworm pressure andmoisture deficits declined, the yield advantage of . . .genetically engineered corn declined.” (Rice et al., 2003).

Another similarity between the two kinds of Bt resistance is that refuge

areas will be needed to delay the development of rootworm populations that

are resistant to Cry3Bb1 (Rice et al., 2003). As with the corn borer Bt,

Cry3Bb1 imparts vertical resistance and presumably will lose its effectiveness

at some future date, thus necessitating replacement with a new genetic form

(or forms) of resistance.

b. Diseases. Frei (2000) stated that the minor presence of leaf diseases in

northern Europe allows increased emphasis on selection for yield performance

of maize hybrids for that area. This statement indirectly acknowledges that

maize breeders in other regions must select hybrids with tolerance or resis-

tance to locally prevalent diseases. The list of important diseases changes


from time to time, as new cultural methods and/or new genotypes encourage

diseases that had been absent or relatively unimportant (Dodd, 2000;

National Research Council (U.S.) Committee on Genetic Vulnerability of

Major Crops, 1972; Tatum, 1971).

Dodd (2000), speaking for maize in the United States, stated that during

the past 40 years at least 14 diseases of maize have had significant increase

in importance, although not all have endured or have proved to be wide-

spread. Their emergence as a problem is often encouraged by changes in

cultural practice, such as an increase in continuous maize growing and/or

in minimum tillage. At other times, widespread planting of a single genotype

will encourage spread of a particular disease. Breeders and farmers react

promptly to new disease problems; susceptible hybrids are dropped in favor

of resistant ones (if they are on hand) and further breeding ensures that new

releases have the needed level of resistance to the problem disease(s).

This battle will never end. Breeding for disease resistance shows its

success (and yield-enhancing contribution) most clearly when the disease is

active on susceptible hybrids (comparable to breeding for insect resistance).

It would be difficult or impossible to plot gradual gains in yield due to

gradual increases in disease resistance alone; nevertheless, the cumulative

effects of successful breeding for disease resistance surely must contribute to

the general increase in the level of on-farm yields. As Russell (1993) said,

“Selection for disease resistance has been an integral component of maize

breeding for many years, yet there are few data reflecting directly how

the success of this selection affects grain yield.” However, he does note

that “. . . improvement for stalk quality has been well documented . . . andstalk quality is highly dependent on plant health.”

One must acknowledge that interactions of disease resistance traits with

other beneficial genetic changes are perhaps the rule rather than the excep-

tion. For example, Clements et al. (2003) stated, “These results suggest that

Bt transformation events like MON810 are a useful supplement to hybrid

resistance to fumonisin contamination and fusarium [Fusarium spp.] ear

rot.” They went on to say that such benefits (reduced borer damage and

therefore less chance for disease entry) may accrue to susceptible hybrids

but not to hybrids with a relatively high level of resistance to fusarium.

The interactions of the two traits (disease resistance and insect resistance)

determine the outcome. One cannot credit either trait by itself.

6. Response to Changes in Plant Density

a. High Density. Genetic yield gain as a result of adaptation to contin-

ual increases in plant density is perhaps the most clear-cut and quantifiable

change in maize hybrids over the years. Cardwell (1982) calculated that


increased plant densities contributed 21% of the gain in maize yield in

Minnesota from 1930–1970. One must assume that not only the increase in

plant density but also the introduction of maize genotypes that could with-

stand and profit from the higher densities was essential to achieving the gain.

High plant density increases the deleterious effects of various kinds of stress

—abiotic and biotic—and so increases the need for genetic improvements in

stress tolerance (Troyer, 1996).

Several examinations of U.S. hybrids, summarized by Russell (1991),

showed that OPCs and old hybrids made their highest yields at lower

densities typical of their era, whereas the newest hybrids yielded the most

at the densities (always higher) typical of recent years. In other words, a

hybrid usually gave the highest yield when grown at the density for which it

was bred.

Similar results have been shown for late-maturing hybrids in France

and Ontario, Canada (essentially the same genotypes as grown in the

United States), but not so for early maturing hybrids in France or Ontario

(Derieux et al., 1987; Tollenaar et al., 1994). Tollenaar et al. (1994) suggested

that because newer hybrids of the early maturity group have greater leaf

area per plant as compared with the older hybrids of the same maturity,

they do not respond to (or need) higher plant density. He stated that, in

contrast, because the newer hybrids of the later maturity groups do not have

increased leaf area per plant compared with older hybrids in their maturity

group, the newer hybrids of the later maturity groups require more plants

per hectare to increase leaf area (and thereby photosynthetic surface) per

hectare.

As mentioned in Section II.D.4, optimum plant density can be affected by

the level of fertilizer N as well as by the hybrid genotype; hybrids differ

within and between eras in their response to various combinations of N level

and plant density (Carlone and Russell, 1987).

A 1930–1991 time series of 36 hybrids and one OPC for Iowa (Duvick,

1997) showed the same general trends as in earlier trials of shorter versions

of this series of hybrids (Duvick, 1977, 1984a, 1992); i.e., the older hybrids

yielded more at lower densities typical of their era, whereas the newer

hybrids yielded more at higher densities typical of their era.

However, the newest hybrids in the 1930–1991 time series made only a

very small gain in yield when planted at the highest density (79,000

plants ha�1) as compared with their performance at the intermediate density

(54,000 plants ha�1). This suggests the possibility that future yield gains

from breeding for adaptation to higher plant densities will come at a slower

pace and/or will require more breeding effort, at least with the present

breeding strategy. Breeders intending to increase genetic yield potentials

may need to modify or replace current breeding strategies and/or selection

criteria.

Figure 6 Grain yield per hybrid regressed on year of hybrid introduction at each of three

plant densities: 10,000, 30,000, and 79,000 plants ha�1. Best linear unbiased predictors (BLUPs)

for hybrid grain yield based on trials grown in the years 1991–2001, three locations per year, one

replication per density. From Duvick et al. (2004b). Copyright # 2004 by John Wiley & Sons,

Inc. This material is used by permission of John Wiley & Sons, Inc.


b. Low Density. Duvick (1997) also showed that yields of the

1930–1991 series of hybrids did not significantly increase over time when

the hybrids were planted at an extremely low plant density of 10,000 plants

ha�1. In this nearly stress-free environment, all hybrids were able to express

maximum yield potential per plant (or at least a close approach) and, under

these conditions, the older hybrids showed virtually as much yield potential

per plant as the newer hybrids. A further report, with the hybrid time series

extended to 2001 (Duvick et al., 2004b), showed essentially the same results

(Fig. 6); breeders have not significantly increased yield potential per plant,

even though they have greatly increased maize yield potential per unit area.

7. Herbicide Tolerance

An experiment designed to compare eight maize hybrids representing three

decadesof yield improvement inOntario,Canada, showed that thehybrids reacted

differentially to the herbicide bromoxynil (4-hydroxy-3,5-dibromobenzonitrile)


(Tollenaar and Mihailovic, 1991; Tollenaar et al., 1994). The hybrids in this

experiment, dating from 1959–1988, showed continuing improvement in

tolerance to bromoxynil, with a statistically significant trend of decreasing

phytotoxicity. They also showed continuing and significant improvement in

grain yield, especially at higher plant densities.

Commenting on these results, Tollenaar et al. (1994) suggested that

improved antioxidant defense mechanisms may be associated with increased

tolerance to bromoxynil and also with increased grain yield over the decades.

They also said, “The small and, in particular, gradual nature of the increased

bromoxynil tolerance suggests a highly complex, polygenic inheritance of

this particular kind of stress tolerance.”

Some maize hybrids now contain deliberately bred-in herbicide toler-

ance, primarily as transgenic resistance to broad-spectrum herbicides such

as glyphosate (e.g., Hetherington et al., 1999). Herbicide-tolerant maize

covered about 15% of the U.S. maize acreage in 2003 (ERS, 2003) and

in 2002 was planted on about 4% of all land planted to transgenic

crops globally (James, 2002). Strictly speaking, herbicide tolerance is

intended to improve the efficiency of weed management and not necessar-

ily to increase maize productivity, although better weed control could indi-

rectly result in higher yields, if weed levels were high with other kinds of

management.

In extreme cases, herbicide tolerance/resistance can increase maize yield

significantly and in strikingly large amounts. For example, initial experi-

ments in several African countries indicated that when maize is bred to be

resistant to a herbicide that normally is toxic to maize, seed coated with

that herbicide can provide effective season-long control of Striga spp.

(Kanampiu et al., 2003). Striga, a parasitic weed (sometimes called “witch-

weed”), can cause devastating crop loss in maize as well as other grain crops

in those countries. The herbicide resistance (imadazolinone resistance, “IR”)

is nontransgenic; it results from a mutation in an acetolactate synthase gene.

The specific herbicides used in these experiments were imazapyr and pyr-

ithiobac. When Striga density was high, the herbicide treatment resulted in a

three- to fourfold increase in yield. Kanampiu et al. (2003) stated, “When the

IR gene is incorporated into locally adapted varieties as in Kenya, this can

result in improvements in maize growth and hence high maize yield benefits

to small-scale farmers.”

Herbicide tolerance, indirectly, can produce undesired results and lower

yields. King and Hagood (2003) showed that postemergence control of

johnsongrass with glyphosate increased the severity of maize chlorotic

dwarf virus and maize dwarf mosaic virus in glyphosate-tolerant hybrids

that were susceptible to those diseases. They said, “The increased disease

severity resulted from greater transmission by insect vectors, which moved

from dying johnsongrass to the crop.” However, disease severity did not


increase in a virus-tolerant (and glyphosate-tolerant) hybrid subjected to

the same conditions. The authors concluded that for fields infested with

johnsongrass, the hybrid choice should be primarily for disease resistance

and secondarily for herbicide resistance.

8. Other Physiological Traits

a. Photosynthesis. As noted in earlier sections, leaf photosynthesis

seems to be more efficient in newer hybrids than in older hybrids when

they are compared in a range of stress conditions such as drought, low

temperature, or low N supply. Such an increase in efficiency could help

maize plants recover more rapidly from transient stresses such as those

induced by cold weather, overly wet soils, or drought. As summarized by

Tollenaar et al. (p. 215, 1994), “[These] findings, some of them preliminary in

nature, suggest that although hybrid differences in leaf photosynthesis under

unstressed conditions may not be indicative of actual or potential yield,

hybrid differences in response of leaf photosynthesis to stress conditions

may be a useful physiological indicator of high stable yields. To date,

selection for yield per se has apparently provided a selection pressure in

favor of stress-tolerant leaf photosynthesis.”

b. Canopy Gas Exchange, Temperature. Nissanka et al. (1997) com-

pared an old and a new hybrid (1959 vs 1988) in regard to whole plant gas

exchange and stem water potential throughout a water-deficit stress cycle

and during the subsequent recovery period upon rehydration. Under mois-

ture stress, the new hybrid maintained relatively higher rates of photosyn-

thesis and transpiration at a lower stem water potential than the old hybrid.

During the recovery day, canopy photosynthesis was 53% higher and

canopy transpiration was 31% higher in the new hybrid than in the old

hybrid. Respiration per unit CO2 fixed was lower in the new than in the

old hybrid in all conditions. The authors concluded that the new hybrid was

more tolerant to water stress and recovered faster upon rehydration than the

old hybrid. (As noted previously, comparison of only two hybrids is not

evidence of a long-term trend, but it may give useful suggestions for further

investigation.)

Canopy temperature under drought stress consistently decreased, going

from older to newer hybrids, in measurements of a set of 18 commercial

hybrids adapted to central Iowa and representing the period 1953 to 2001

(Barker et al., 2005). The hybrids were grown in a rain-free environ-

ment in Chile and were subjected to managed drought stress at various

stages of development. Barker et al. (2005) suggested that the trend to

lower canopy temperature under drought stress may result from the lower


radiation intensity on the more upright leaves of modern hybrids or on a

greater capacity by these hybrids to capture soil water.

9. Parentage and Genetic Diversity

As new hybrids replace those that preceded them, pedigrees and geno-

types change. It can be instructive to know more about the nature of these

changes. Which founder inbreds and/or OPCs remain in the pedigrees of

current hybrids and which ones disappear? Has genetic diversity decreased,

increased, or stayed about the same over the years? In a limited way some of

these questions were answered by Duvick et al. (2004a,b) with respect to the

time series of Iowa hybrids used for their studies of changes in hybrid

performance over time. For example:

• The 51 hybrids in the trials traced back to 53 founder sources: OPCs,

synthetic populations, and inbred lines. The founders came primarily from

the U.S. corn belt but a few were from the southeastern and northeastern

United States or from Latin America.

• Some families have persisted over the years and have contributed relatively

large amounts (by pedigree) to present-day hybrids, whereas others ap-

peared in pedigrees for only a few decades and then declined or disap-

peared. For example, Reid Yellow Dent, Iowa Stiff Stalk Synthetic, and

Reid Iodent have been important contributors since they first appeared in

pedigrees and they now contribute 33, 22, and 15%, respectively, to

hybrids of the 2000s. However, Maryland Yellow Dent, Boone Country

White, and the inbred Hy contributed briefly to pedigrees in the 1950s and

1960s but then disappeared completely from pedigrees of subsequent

hybrids in the time series. Krug reached a peak use of 23% in the 1940s

but declined rapidly to a steady level of about 3%, and some families

appeared late but have made significant, if not large, contributions;

for example, Argentinian Maiz Amargo appeared in the 1980s and has

contributed 4 to 5% in each of the past two decades.

• The pedigree information shows, therefore, that although certain lineages

have predominated over the years of hybrid improvement and replace-

ment, they have been supplemented significantly by additional, and di-

verse, lineages. On the whole, pedigree contributions have been broad and

volatile; the record provides strong evidence for “genetic diversity in time”

[as defined by Duvick (1984b)] in this 70-year time series of 51 hybrids for

central Iowa.Genetic diversity, including genetic diversity in time (also called

temporal genetic diversity), is widely acclaimed for its ability to provide

beneficial genetic response (timely and wide-ranging) to new and/or un-

usual kinds of biotic or abiotic stress (FAO, 1996; Gollin and Smale, 1998;


National Research Council (U.S.) Committee on Genetic Vulnerability

of Major Crops, 1972; Rosenow and Clark, 1987; Simmonds, 1962; Smale

et al., 2002).

10. Molecular Markers

Pedigree data, although informative, do not identify genetic materials in

the pedigree lineages, either qualitatively or quantitatively. Molecular mark-

er data, tracing a given DNA fragment from one generation to the next, can

enable quantification of the amount of founder germplasm that persists in

successive generations. Application of this technology to the Iowa time series

of hybrids (Duvick et al., 2004a,b) using simple sequence repeats (SSR)

showed that

• The number of alleles fluctuated from decade to decade, with about 40

to 50% of the total number of alleles present in any one decade. The

study identified 969 alleles at 100 SSR loci in the array of hybrids and

OPCs.

• The number of alleles per locus was similar for the female and male

parents of hybrids.

• Large-scale turnover of alleles took place in the first decades (1930s and

1940s) of hybrid breeding (which agrees with pedigree data), indicating

that many of the first inbred lines were not useful as parents for the next

generation of breeding. They were dropped from breeding pools, and new

and more successful breeding materials were brought in.

• The initial large-scale turnover of alleles was followed by a relatively

steady state of replacement until the 1970s (corresponding with the

changeover from double cross to single cross hybrids) when the number

of new alleles per decade again declined to what may be a new and lower

steady state of replacement.

• The alleles of the inbred parents of the modern hybrids (primarily single

crosses) could be separated (with multidimensional scaling analysis)

into two groups (called “stiff stalk” and “nonstiff stalk”), whereas alleles

of the older hybrids (primarily double crosses) sorted into an undifferenti-

ated third group (Fig. 7). This confirms the general observation that

breeders (using pedigree and experiential data) have established two breed-

ing pools to balance important traits (including those that enable use of

inbreds as either seed parent or pollen parent) and/or to maximize hetero-

sis when inbreds from the two groups are crossed with each other. The

primary goal of such divergent selection is to enable the development of

economically producible hybrids with improved on-farm yield and general

performance.

Figure 7 Scores for 94 inbreds contributing to Era hybrids on the first two dimensions of the

multidimensional scaling analysis of SSR polymorphism data for 298 SSR loci (R2 ¼ 0.45 for the

two-dimensional model). From Duvick et al. (2004b). Copyright# 2004 by John Wiley & Sons,



11. Heterosis: Hybrid and Inbred Performance

a. Heterosis for Grain Yield. The phenomenon of heterosis in maize

stimulated the initial research that led to the development and introduction

of hybrid maize (e.g., Crow, 1998; Hayes, 1952; Shull, 1952), and maize

breeders sometimes seem to have considered that breeding for higher yield is

synonymous with breeding for increased heterosis. Few researchers have

gathered data, however, to measure the degree to which the proportionate

contribution of heterosis to grain yield has changed over the years of hybrid

breeding (Duvick, 1999).

b. Absolute Heterosis. Schnell (1974) summarized data comparing sin-

gle cross yield and parental inbred yield from 17 experiments designed

for other purposes. He stated that heterosis for the decades 1920–1970

showed “only a modest increase . . . as compared to the large simulta-

neous increase in the yields of inbreds. . . .” Schnell refers here to “absolute


heterosis,” the difference between the yield of a single cross and the mean

yield of its parental inbreds (midparent yield). The amount of annual increase

in midparent yield was nearly as great as that of the single cross hybrids.

Schnell also calculated heterosis as “relative heterosis” (absolute heterosis

divided by single cross yield) and noted that it decreased from 75% in the

1920s to about 50% in the 1970s. This is because the denominator (single

cross yield) increased at a faster rate than the numerator (absolute heterosis).

Meghji et al. (1984) studied changes in heterosis for inbreds and their

single crosses representing three decades (1930s, 1950s, and 1970s) of U.S.

corn belt hybrid germplasm. Six inbreds per decade represented the 1930s

and 1950s (two inbreds, WF9 and Os420, were in both decades) and seven

inbreds represented the 1970s (four of the six single crosses for the 1970s

contained the inbred Mo17). The trials were grown in Illinois; the year(s) of

the trial is not indicated. Yields of inbreds and single crosses (averaged

across densities) increased simultaneously over the decades. Absolute heter-

osis also increased over the decades; the increase averaged 51 kg ha�1 year�1

(Experiment 1, Table II). The increase was greater at a high density typical

of the 1970s than at a low density typical of the 1930s.

Duvick (1984a) compared inbreds and single crosses representing success-

ful Iowa hybrids for the decades 1930–1970. Five unrelated inbreds for each

decade were crossed in all possible combination to give 10 single crosses

per decade; trials were grown in 3 years (1977–1979) at three densities

Table II

Contributions of Absolute Heterosis and Relative Heterosis to Grain Yield in Three Experimentsa

Experimentb Categoryc

1930s 1940s 1950s 1960s 1970s 1980s

bdkg ha�1

1 SX yield 7097 7407 9538 61

Het Abs 4112 4438 6138 51

Het (%) (58) (60) (64)

2 SX yield 4600 5300 6900 7000 7900 83

Het Abs 2700 3200 4100 3600 4300 36

Het (%) (59) (60) (59) (51) (54)

3 SX yield 5941 6371 6865 7174 7929 9164 60

Het Abs 3787 3754 4143 4188 4102 4658 13

Het (%) (64) (59) (60) (58) (52) (51)

aAdapted from Duvick (1999), with permission from American Society of Agronomy, Crop

Science Society of America, and Soil Science Society of America.bExperiment 1: Means of two densities, data from Meghji et al. (1984). Experiment 2: Means of

three densities grown in 1977–1979, data from Duvick (1984). Experiment 3: Means of three

densities grown in 1992–1993, data from Duvick (1999).cSX yield, single cross yield; Het Abs, absolute heterosis; Het (%), relative heterosis.dLinear regression coefficient (kg ha�1 year�1).


(30,000, 47,000, and 64,000 plants ha�1) representing densities of the 1930s,

1950s, and 1970s. Yields of inbreds and their single crosses (averaged across

densities) increased simultaneously in each decade. Absolute heterosis

increased in each decade, except in the 1960s. The increase averaged 36 kg

ha�1year�1 (Experiment 2, Table II).

In a second experiment, Duvick compared inbreds and single crosses

representing successful Iowa hybrids for the decades 1930–1980. Results of

the experiment are reported in Duvick (1999) and Duvick et al. (2004b).

Seven representative single crosses per decade were compared with their

parental inbreds during 2 years (1992 and 1993), at three locations per

year, and three densities (30,000, 47,000, and 64,000 plants ha�1) per loca-

tion. In 1993, a very wet year, one location was lost because of flooding.

Yields of inbreds and their single crosses (as averaged across densities

and years) increased simultaneously and by nearly the same amount

in each decade (Fig. 8). Absolute heterosis (SX–MP) increased minimally

Figure 8 Yields of single crosses (SX), their inbred parent means (MP), and heterosis (as

SX – MP). Single cross pedigrees are based on heterotic inbred combinations in Era hybrids

during the six decades, 1930–1980, 12 inbreds and six single crosses per decade. Means of

trials grown in three locations in 1992 and two locations in 1993 at three densities, 30,000,

54,000, and 79,000 plants per hectare, one replication per density. From Duvick et al. (2004b).

Copyright# 2004 by JohnWiley & Sons, Inc. This material is used by permission of JohnWiley

& Sons, Inc.


(13 kg ha�1year�1) during the six-decade period (Fig. 8 and Experiment 3,

Table II).

However, the two growing seasons gave contrasting results. Absolute

heterosis averaged over densities was constant over the decades in the 1992

trial, but it increased significantly (32 kg ha�1 year�1) in the 1993 trial

(Fig. 9). The year 1992 was an optimal growing season with very high yields;

whereas 1993 was a high-stress, low-yield year, with extremely wet and cool

growing conditions.

The trials of this experiment also exhibited contrasting outcomes when

grown at different plant densities. Absolute heterosis, averaged over the two

seasons, showed no trend over the decades at the lower density, increased

slightly but unevenly at the medium density, and increased consistently

(b ¼ 32 kg ha�1 year�1) at the higher density (Table III).

Data from this experiment show, therefore, that yielding ability under

stress has been improved to a greater degree in hybrids than in inbreds, even

though (as shown in this and in other experiments) yield under stress is

greatly improved over time for both of the categories (inbreds and hybrids).

Figure 9 Heterosis (as SX – MP) in two seasons: 1992 and 1993. Single cross pedigrees

based on heterotic inbred combinations in Era hybrids during the six decades, 1930–1980,

12 inbreds and six single crosses per decade. Trials were grown in three locations in 1992 and

two locations in 1993. Means of three densities: 30,000, 54,000, and 79,000 plants ha�1, one

replication per density. From Duvick et al. (2004b). Copyright # 2004 by John Wiley & Sons,


Table III

Interaction of Plant Density with Decadal Changes in Absolute Heterosisa

Densityb Categoryc

1930s 1940s 1950s 1960s 1970s 1980s

bdkg ha�1

Low SX 6717 6703 7099 7387 7187 8174 26

MP 2062 2373 2395 2658 3309 3875 35

Abs. Het 4655 4330 4703 4730 3877 4298 �8

Medium SX 6569 7033 7960 8171 8747 10024 64

MP 2337 3065 3174 3493 4352 4969 50

Abs. Het 4232 3968 4786 4679 4396 5055 15

High SX 5708 6648 6823 7192 9098 10492 90

MP 2308 3003 3063 3390 4463 5476 59

Abs. Het 3400 3645 3760 3802 4635 5016 32

aAdapted fromDuvick (1999), with permission fromAmericanSociety ofAgronomy,Crop Science

Society ofAmerica, and Soil Science Society ofAmerica.Data formeans of seven single crosses and

corresponding midparents per decade grown in five locations over 2 years (1992 and 1993).bPlant densities: Low, 30,000 plants ha�1; medium, 54,000 plants ha�1; and high, 79,000

plants ha�1.cSX, single cross; MP, midparent; Abs. Het, absolute heterosis.dLinear regression coefficient (kg ha�1 year�1).


These results agree with those of Meghji et al. (1984), who stated that the

increase of absolute heterosis over the decades was greater at higher than at

lower plant density.

An intriguing area of research might be to look for the genetic and physio-

logical changes that have accompanied the increases in absolute heterosis under

stressful growing conditions. Can the needed genetic combinations be present

only in heterozygous individuals or can they be gradually gathered into a single

genome? Discoveries of intraspecific violation of genetic colinearity in maize

(Fu and Dooner, 2002) may have implications for this area of investigation.

To review this section, limited data indicate that absolute heterosis for

grain yield has increased over the years to a small extent (more so under

abiotic stress) but that its annual gain is less (sometimes much less) than

total genetic gain in hybrid yield. Of course, one must recognize that one way

to increase absolute heterosis would be to reduce inbred yields without

increasing hybrid yields; this is not a desirable outcome. The current situa-

tion seems to be that yields of inbreds have increased in line with those of

their hybrids, but at a slightly slower rate such that absolute heterosis is

gradually increasing, especially when plants are grown under stress.

c. Relative Heterosis. Calculations of relative heterosis (absolute het-

erosis as percentage of single cross yield) for the aforementioned three

experiments indicate that although absolute heterosis increased over time


in most comparisons, relative heterosis did not increase in the two Iowa

experiments (Experiments 2 and 3, Table II), although it did increase in the

Illinois experiment (Experiment 1, Table II). Relative heterosis in the Iowa

experiment of 1992–1993 (Experiment 3, Table II) declined from 64% in the

1930s to 52% in the 1970s and 51% in the 1980s. Although absolute heterosis

increased minimally over the decades in this experiment, the gain in single

cross yield was greater than the gain for absolute heterosis, and so, as with

Schnell data, the proportionate contribution of heterosis to grain yield was

reduced over time. Interestingly, also, Schnell’s estimate of 50% for relative

heterosis in the 1970s corresponds closely with values of 54 and 52% for the

1970s in the two Iowa experiments.

Data summarized in this section suggest that relative heterosis for grain

yield has not increased markedly over the years; it more likely has stayed

constant or declined.

d. Heterosis for Other Traits. Plant height and flowering date exhibit

heterosis to a large degree in maize; crosses between two inbreds are always

taller and earlier than the mean of the parents. Heterosis for these traits may

(or may not) be related to some of the genetic interactions that produce

heterosis for grain yield and so it may be informative to examine changes

over time in heterosis for plant height, or other plant size measurements, and

flowering date.

Mean values for inbreeding depression in ear height and plant

height decreased over time, in comparisons made by Meghji et al. (1984).

This indicates that absolute heterosis for ear height and plant height de-

creased over time. In the same experiment, means for inbreeding depression

of tassel weight and tassel branch number increased in the 1950s but de-

creased in the 1970s to levels lower than in the 1930s. This would indicate

reduced heterosis for tassel weight and tassel branch number in the 1970s

genotypes.

Small but statistically significant trends toward reduced absolute heterosis

for plant height (�3 cm 10 year�1), ear height (�4 cm 10 year�1), and heat

units to anthesis (�11 heat units 10 year�1) were exhibited in the aforemen-

tioned comparison of inbreds and single crosses representing successful Iowa

hybrids for the decades 1930–1970 (Duvick, 1984a).

Absolute heterosis was reduced to a small degree for plant height but was

not reduced for heat units to anthesis in the aforementioned comparison of

inbreds and single crosses representing successful Iowa hybrids for the

decades 1930–1980 (Duvick et al., 2004b).

Data from these experiments indicate that, to a small degree, the size and

maturity differences between inbreds and their hybrid progeny were reduced

over time. However, the differences between the two classes remain (and

probably will remain) large. For example, reexamination of data for plant


height heterosis summarized in Duvick et al. (2004b) shows that the height

difference between the two classes was reduced from about 85 cm in the

1930s to about 70 cm in the 1980s, primarily because of a reduction in height

of the single crosses. If this rate of reduction in height difference could be

maintained (�0.3 cm year�1 or �15 cm 50 year�1), it would take about five

more 50-year cycles of selection to equalize inbred and hybrid height.

Data for changes over time in heterosis for plant size and maturity agree

in one respect with those for grain yield—neither category has exhibited

major increases (or decreases) in absolute heterosis. However, absolute

heterosis for grain yield has increased to a small degree (at least, under

stress), whereas absolute heterosis for plant size and maturity has decreased

to a small degree. Superficially, the two categories of heterosis do not seem

to answer to the same genetic stimuli.

III. GENETIC GAINS FROM POPULATIONIMPROVEMENT

A. COMPARISONS WITH GENETIC GAINS IN HYBRIDS

Although the emphasis of this review is on maize hybrids and how

successive changes in their breeding and genetics have contributed to

increased on-farm yield, recurrent selection to make improved populations

has interacted with and sometimes contributed to genetic improvements in

hybrids (e.g., via useful inbred lines bred from improved populations).

Additionally, for some farmers in some parts of the world, annual purchase

of hybrid seed is not an option. For these people, improved populations,

maintained by saving seed, are the only practical option for access to

improved cultivars. Therefore, this section briefly summarizes genetic gains

achieved by recurrent selection for population improvement in comparison

with genetic gains in hybrid performance and comments briefly on the

contribution of improved populations to hybrid maize yield.

A comparison of genetic gain for four recurrent selection experiments

with genetic gain for two time series of hybrids indicated that both methods

produced about the same annual genetic gain for grain yield: 71 kg ha�1 year�1

for recurrent selection and 68 kg ha�1 year�1 for the hybrids (Duvick, 1977).

Duvick described the two sets of experiments as follows: “Both took place

in central Iowa; both occurred in about the same time frame; both had as

a primary goal maximum improvement in yield.” For these reasons

he thought it appropriate to compare the outcomes of the two kinds of

breeding program. He also suggested, however, that selection pressure in the

recurrent selection programs might have placed less weight on nonyield


traits (e.g., root and stalk lodging) than was the case in the hybrid breed-

ing programs, thus allowing greater progress for yield per se in the recur-

rent selection programs. So the programs were not completely equivalent in

selection goals.

Duvick (1977) called for more comparisons of recurrent selection with

hybrid breeding (which typically is based on pedigree breeding), suggesting

that “Maize breeding probably could be helped by the results of quantitative

genetics studies specifically designed to compare ‘recurrent selection using

the pedigree method’ and ‘recurrent selection using the population pool

method.’ Good data, demonstrating the strong and weak points of these

two related and proven methods, would help the entire hybrid maize breed-

ing effort in its goal of producing good hybrids as quickly and efficiently as

possible.”

This request was easier to make than to grant, however, and to the

author’s knowledge, no such paired breeding programs have been designed

and executed. Even to compare estimates of genetic gain for hybrids with

estimates of genetic gain for recurrent selection is difficult because most

reports of progress in recurrent selection express yield gains in units cycle�1

rather than units year�1, and number of years per cycle usually is not stated

and must be inferred (if possible) from descriptions of the breeding cycle.

However, Edmeades and Tollenaar (1990) summarized 17 estimates of

genetic gain in temperate environments and 10 estimates of genetic gain in

tropical environments, with all estimates expressed as kg ha�1 year�1. With

one or two exceptions, the estimates for temperate environment are for time

series of commercial hybrids and the estimates for tropical environments are

for recurrent selection programs intended to produce improved populations.

Genetic gain in grain yield for the temperate programs averaged 66

kg ha�1 year�1, whereas genetic gain for the tropical programs averaged

145 kg ha�1 year�1. The average gain for the temperate experiments is iden-

tical to the average from the previously mentioned summary by Russell

(1991). This result is not too surprising because for the most part the two

lists cite the same reports, although the two lists are not identical. The list

of tropical experiments shows a broad range of estimates, from 51–310 kg

ha�1 year�1.

Edmeades and Tollenaar (1990) explained the high values for the esti-

mates of the tropical programs (primarily recurrent selection) as follows:

“The higher average rate of gain reported from the tropics is generally the

result of one, sometimes two and very occasionally three selection cycles per

year, the use of relatively unimproved germplasm with a broad genetic base,

and a selection scheme that was based on family performance.” Although it

is probably true that the first gains are the easiest in any professional

breeding program that starts with landrace materials, it also seems likely

that some of the high gains reported for the recurrent selection programs in


the tropics result from effective selection technology for important traits

such as drought tolerance (e.g., Banziger et al., 1999; Bolanos and

Edmeades, 1992), combined with rapid turnaround of breeding generations.

Edmeades and Tollenaar (1990) presented evidence for the possibility that

first gains are the easiest. They said that “. . . tropical maize . . . in its

unimproved state is tall, leafy, lodging-prone and has a harvest index of

about 0.35.” They stated that initial selection in unimproved populations in

the tropics results in shorter plants and reduced lodging, improved HI, and

reduction in barrenness.

The present review has shown that temperate hybrids have shown little or

no change over the years in plant height, leaf number, or HI when hybrids

are grown at the plant density for which they were bred. This may indicate

that farmer selectors had already changed these traits to a close approxima-

tion of “optimum” levels when they developed the corn belt OPCs that were

the basis of hybrid breeding. However, the first hybrids clearly surpassed

parent OPCs in root and stalk strength and in resistance to barrenness.

Although the stress of constantly increasing plant density continues to sort

out hybrid genotypes with increasingly greater resistance to lodging and

barrenness, these improvements are not as dramatic as those of the initial

hybrids compared with their parent OPCs. Taking into account these

changes (or lack thereof) in temperate breeding programs, one might predict

that annual yield gains of population improvement programs for tropical

materials eventually will move to lower (but nevertheless acceptable) levels,

similar to those for hybrid improvement in the temperate zones. Following

the relatively easy gains resulting from initial reductions in plant size and

lodging and from increases in HI, yield gains will need to come from more

gradual improvements in tolerance to locally important kinds of abiotic and

biotic stress.

Leaving aside comparisons between hybrid breeding and recurrent selec-

tion, numerous published reports testify clearly that recurrent selection for

grain yield and/or general performance can give positive results in temperate

as well as in tropical materials, and it can do so with acceptable investments

of time and effort (e.g., Hallauer and Miranda, 1988; Lamkey, 1992; Russell,

1991; Sriwatanapongse et al., 1985). Several methods have been tried; some

worked well and some did not (e.g., Edwards and Lamkey, 2002; Lamkey,

1992), much as has been true for various kinds of pedigree breeding applied

to hybrid development.

One difference between recurrent selection and hybrid breeding has been

that breeders sometimes have used recurrent selection primarily to intensify

expression of a single trait such as resistance to ECB or high grain oil

percentage (Klenke et al., 1986; Sprague, 1952). They often discovered that

other important traits such as grain yield or stalk digestibility could deterio-

rate, sometimes as an indirect response to strong selection for the intensified


trait or sometimes simply because of insufficient selection pressure for the

other important trait(s) (Hallauer and Miranda, 1988; Ostrander and Coors,

1997; Russell, 1991). Such populations could have only limited value as

sources of commercially useful inbred lines because inbreds (and the hybrids

they produce) must be as well balanced as possible for a full selection of

important traits. Transfer of the improved trait to useful inbred lines

may require a long-term effort or may not even be worth doing if its

intensification depends on the deterioration of another important trait.

B. RELATIVE CONTRIBUTIONS OF POPULATION IMPROVEMENT

AND PEDIGREE BREEDING

“Pedigree selection is the most widely used breeding method to develop

inbred lines for use as parents of hybrids.” . . . “Pedigree selection will always

bean important componentofmoderncorn-breedingprograms (Hallauer etal.,

1988, pp. 470–471),” “Pedigree selection was and is the most commonly used

selection method of line development (Hallauer andMiranda, 1988, p. 10).”

These statements, although in agreement with the general experience of

hybrid maize breeders, should not be construed to say that recurrent selection

for population improvement has notmade vital contributions to hybridmaize

breeding. Inbred lines such as B14, B37, and B73 have, in their time, been

parents of hybrids that dominated maize plantings in the U.S. corn belt, and

they also have been important sources of germplasm for further breeding by

pedigree selection. These inbreds are direct products of the previously de-

scribed population, BSSS (Russell, 1991). Other elite inbreds derived from

improved populations could be named as well (e.g., Hagdorn et al., 2003),

although their impact has been more limited than that of the “big three.”

Nevertheless, as stated earlier, pedigree breeding has been and remains

the backbone of hybrid maize breeding. [See Troyer (1996) for a detailed and

first-hand description of pedigree breeding in action.] Planned single crosses,

successful commercial hybrids, and crosses (or backcrosses) of an elite line to

an improved population are typical starting points for pedigree selection

to produce new inbred lines. The author knows of no detailed, data-based

exposition of the reasons for predominance and persistence of pedigree

breeding to develop inbred lines and so can only speculate about reasons

for this situation.

Perhaps one reason for the predominance of the pedigree method is that

its parental materials—inbred lines—have been very widely tested, not only

in breeders’ performance trials, but also by thousands of farmers. Breeders

typically have started selfing and pedigree selection from crosses of inbreds

(or their progeny) that were used in widely successful hybrids. Each hybrid

can be considered as a “test cross” for its parental inbreds. An unexpected


weakness in one or both parents is more likely to be discovered when a

hybrid is grown by thousands of farmers over a period of years, as compared

with growing an improved population in a relatively small number of yield

trials for one or two seasons. Conversely, one also can be more confident of

identifying genotypes that can give top performance over a wide variety

of environments if the replication number is in the thousands rather than in

the dozens (or fewer). (Commercial seed companies have a unique advantage

here in that they can gather trial data from hundreds or thousands of on-

farm “strip trial” comparisons. Although these data may be intended pri-

marily for potential use in sales promotion, they also provide the company’s

breeders with a deep mine of information about comparative performance of

a given genotype over a broad range of environments.)

A second consideration is that the odds of getting a superior inbred—with

good balance for all traits—from selfing a cross of two currently top-

performing inbreds are probably higher than the odds of getting a line of

equivalent merit from selfing an excellent but relatively heterogeneous im-

proved population, even though truly superior (and novel) genotypes may

well exist in the improved population.

This second possibility leads to further speculation that a new program

(such as some of those in the tropics) may have greater success in extracting

useful inbred lines from improved populations than has been exhibited in

mature temperate breeding programs. One reason could be that some of

today’s improved populations for the tropics are very high quality; they have

benefited from years of experience in designing and/or choosing proper

environments for performance trials and in the development of improved

designs for recurrent selection. The potential utility of such populations

(e.g., for production of stress tolerant hybrids) has been predicted by

Edmeades et al. (1997), who said “The probability of obtaining a hybrid

that yielded 40% greater than the trial mean under severe stress was 4-fold

greater when lines were extracted from a drought-tolerant source popula-

tion than from its conventional counterpart. . . . We conclude that drought-

or N-tolerant elite source populations provide a greater proportion of

drought- or N-tolerant inbred lines and hybrids.”

A second reason could be that there will be few or no truly superior

adapted inbred lines for a new breeding locality. If improved populations

(improved for the traits needed in the area where hybrids are to be grown)

are on hand, they may be the best available source of germplasm for the

development of inbred lines. They will be better than local OPCs and better

than crosses of unadapted inbreds that may be “elite” elsewhere but are not

well suited to the local environment. (This scenario contrasts with the course

of events in the U.S. corn belt, where two or three decades of pedigree

breeding had brought out many superior inbreds by the time improved

populations from recurrent selection programs were ready for use.)


In years to come, pedigree selection based on planned crosses of inbred

lines may become more competitive in new breeding localities (such as in

the tropics); however, further expertise in population improvement via

recurrent selection may enable continued development of populations that

are valuable sources of elite inbred lines for those environments.

A final speculation about the utility of improved populations is that as

expertise grows in molecular biology, breeders may learn how to “mine”

improved populations for valuable genes or gene combinations with more

precision and better odds of success than can be done with current methods

of breeding and selection. The improved populations could provide a wider

range of useful genetic diversity than can be achieved with pedigree breed-

ing and would have the diversity in much more useful forms than exist in

unadapted exotic cultivars and landraces. These latter materials are high

in genetic diversity but are also high in “useless” genetic diversity.

Remarks from Hallauer et al. (1988, pp. 531–532) make an appropriate

conclusion for this section. They said “Recurrent selection and pedigree selec-

tion . . . should not be considered in opposition to one another. Rather, the two

systems should complement each other. The goals of the two systems are

different, but the ultimate objective is the same—contribute to genetic gain.”

It seems safe to predict that as experience and technology progress,

breeders will find increasingly profitable ways to utilize recurrent selection

for development of a genetically diverse assortment of superior inbred lines

that can be parents of successful hybrids.

IV. ANALYSIS AND CONCLUSIONS

A. POSSIBLE REASONS FOR GENETIC YIELD GAINS

This review has shown that hybrid maize breeders have consistently

increased the yielding ability of hybrids during the past 70 years and that

genetic gains in grain yield are still linear. As the yielding ability of the

hybrids has increased, other traits have changed as well, in directions

that were sometimes intended and sometimes unintended or at least un-

planned. Conversely, some traits have not changed (or have changed very

little), sometimes at the intention of the breeders and sometimes despite the

breeders’ intent to make a change.

It will be instructive to categorize the various trait changes (or stabilities)

as described in Section II.D. They can be categorized as (1) trait changes that

promote the efficiency of grain production, (2) trait changes that increase

tolerance to biotic and abiotic stress, (3) intended trait stabilities, and (4)


unintended (or unplanned) trait stabilities. The various trait changes are

briefly summarized and arbitrarily sorted into these four groups as follows.

1. Trait Changes that Promote Efficiency of Grain Production

• Leaf angle has become significantly more upright, especially since about

the 1960s.

• Tassel size has been markedly reduced.

• Newer hybrids have longer period of grain fill but faster dry down;

therefore they are not later in harvest maturity and make better use of

the latter part of the growing season.

• Kernel weight is greater in newer hybrids except under drought stress at

late or terminal periods of grain fill.

• Newer hybrids have lower percentage grain protein.

• Newer hybrids have higher percentage grain starch.

• In some experiments, newer hybrids are markedly more responsive to

favorable environments (they make more efficient use of bountiful inputs),

although results are not consistent in this regard.

2. Trait Changes that Increase Tolerance (or Exhibit Evidenceof Increased Tolerance) to Biotic and Abiotic Stress

• Grain yield has increased in linear fashion; increases are greatest at

high plant density and are exhibited in high stress as well as low stress

environments, in poorly fertilized as well as in well-fertilized environments.

• Leaf rolling during drought stress is increased, perhaps because of changed

leaf orientation; potentially this can help maintain lower leaf temperature

and reduce water use.

• Staygreen (resistance to stress-induced premature death) is markedly

improved.

• Anthesis-silking interval is shortened, especially when hybrids are sub-

jected to conditions of abiotic stress such as drought or high plant density.

• Newer hybrids show increased resistance to barrenness when trials are

subjected to abiotic stress such as drought at flowering time or higher plant

density.

• Newer hybrids have higher HI than older ones if trials are subjected to

biotic stresses that induce barrenness.

• Hybrids show linear improvements in resistance to root lodging, although

some trials indicate a ceiling at about 95% nonroot-lodged plants.


• Hybrids show linear improvements in resistance to stalk lodging, although

some trials indicate a ceiling at about 95% nonstalk-lodged plants.

• Hybrids show linear improvement in yield in seasons with above-average

temperature during the growing season.

• Hybrids show linear improvement in yield in seasons with below-average

temperature during the growing season.

• Newer hybrids are more drought tolerant.

• Newer hybrids are more tolerant of excessive soil moisture (water-logged

soils).

• Newer hybrids are more tolerant of soil nitrogen deficiency.

• Newer hybrids are more tolerant of unspecified abiotic stresses (“low-

yield” sites).

• Newer hybrids are more tolerant of ECB2, and, recently, transgenic

hybrids have expressed a sharply increased level of resistance to both

generations of European corn borer and (separately) to two species of

rootworm.

• Circumstantial records show that new kinds of disease resistance are added

continually in response to new disease problems, but the contributions to

the yield of sequential changes in disease resistance are not documented.

• Newer hybrids, more tolerant of the stresses of higher plant density, enable

the use of higher plant density to maximize yield and therefore the grain

yield potential per unit area is increased.

• Newer hybrids show increased tolerance to a specific herbicide, apparently

correlated with increased antioxidant defense mechanisms; hybrids can be

bred (using conventional genetics) to be resistant to another specific her-

bicide; and in recent years transgenesis has been used to impart tolerance

to a third herbicide.

• A newer hybrid has more efficient photosynthesis than an older one,

especially under stress, and shows an improved capacity to recover the

photosynthetic rate after stress.

• A newer hybrid has more efficient canopy gas exchange, stem water

potential, transpiration, and respiration than an older hybrid when plants

are subjected to water stress.

• Canopy temperature under drought stress is decreased.

• Pedigree contributions have been diverse and are in a state of constant

change, although with a steady core of persistent lineages. The consequent

increase in genetic diversity (in time and in place) theoretically will provide

an increased stability of performance in the presence of diverse biotic and

abiotic stresses.

• Molecular marker studies validate the pedigree information and show,

further, that parent inbreds in recent years of the hybrid time series can

be divided into two genetically different groups called stiff stalk and

nonstiff stalk.


• Absolute heterosis for grain yield usually has increased to a small degree,

with the greatest increase when trials are grown under stress of high plant

density or drought.

3. Intended Trait Stabilities

• Plant and ear height have been relatively stable with a weak trend to lower

plant and ear height.

• Anthesis date is relatively unchanged.

• Date of silk emergence is unchanged over time in absence of stress, but

newer hybrids silk earlier than older hybrids when trials are subjected to

abiotic stress such as drought or high plant density; this is because silk

emergence is delayed (or fails entirely) in the older hybrids when subjected

to these kinds of abiotic stress.

• Tillering ability is rarely expressed at modern plant densities; tillering is

slightly reduced at low plant density.

4. Unintended (or Unplanned) Trait Stabilities

• Leaf number is unchanged.

• LAI is unchanged in the U.S. corn belt, but may be increased in early

maturity regions of Ontario (Canada).

• Number of ears per plant is not changed in absence of stress.

• HI of temperate hybrids is not changed if hybrids are grown at the density

for which they were bred.

• Yield potential per plant is not increased; i.e., newer hybrids do not yield

more than older hybrids at super-low plant density in absence of abiotic

stress.

• Relative heterosis for grain yield has not increased and, in some cases, is

slightly reduced.

• Absolute heterosis for plant height, ear height, and flowering date has not

increased and, in some cases, is slightly reduced.

Comparison of the categories in this summary shows that the list of

improvements in stress tolerance is by far the longest. This may indicate

that yield advances in hybrid maize depends primarily on increase in stress

tolerance—more specifically, on increased tolerance to the stresses that

typically occur in the environments where the hybrids are grown. It is true

that yields of both older and newer hybrids are reduced in the presence of

stress, either biotic or abiotic, but it also is true that the newer hybrids


always yield more than the older ones in the presence of stress and so, by this

definition, are more stress tolerant.

Changes that impart efficiency, such as smaller tassels, more upright

leaves, faster dry down of grain (to enable longer kernel-fill period), and

lower percentage grain protein, may have also enabled higher yields. These

changes were not selected directly, but they might have been selected indi-

rectly as a consequence of selection for increased grain yield per unit area

because they (presumably) improve the efficiency of transforming sunlight,

CO2, and soil nutrients into plant constituents, and so help increase yields.

The author is not surprised by the stability of maturity and plant size over

the years despite the fact that increased plant size and later maturity corre-

late positively with increased grain yield. The average date of first frost and

farmer prejudice against tall plants have automatically set the limits to which

breeders can select for harvest maturity and plant height, at least for U.S.

corn belt hybrids.

Some of the unintended (or unplanned) stabilities present surprises, or at

least do not agree with conventional wisdom. Probably the breeders’

intended constraint on plant and ear height has indirectly held leaf number

and leaf area index constant. In theory, the more leaf area per unit land area

(up to a maximum LAI of about four or five), the more photosynthesis and

consequently the higher the grain production per unit land area. However,

additional leaf area per unit land area has been achieved not by increasing

leaf area per plant, but by crowding more plants together. One could

hypothesize that shorter internodes could allow more leaves and more leaf

area per plant without increasing plant and ear height. This could substitute

for (or extend) the effect of increased plant density. However, plant archi-

tecture (e.g., leaf dimensions, shape, or angle) might need to be changed if

such an approach were used. Because leaf number usually is positively

correlated with time to flowering, it might not be possible to increase leaf

number and still hold the flowering date constant (a requirement for nearly

all temperate maize production).

Some may express surprise that HI of maize hybrids in the United States

has not increased (in absence of stress-induced barrenness) because of fre-

quent statements that an increase in HI was an important reason for the

higher yields of green revolution wheat and rice cultivars (e.g., Donald, 1968;

Peng et al., 1999; Reynolds et al., 1999; Swaminathan, 1998). However, the

first maize hybrids (as well as their parent OPCs) had about the same HI as

the initial high yield rice and wheat cultivars. It would appear that farmer

selection (at least in U.S. corn belt OPCs) had already brought maize plants

to an approximation of the 40–50% HI of initial green revolution rice and

wheat cultivars. Interestingly, rice and wheat breeders at the international

centers now suggest that an increase in biomass should receive major (per-

haps primary) emphasis as they strive to effect further increases in yield for


their crops (e.g., Peng et al., 1994, 1999; Reynolds et al., 1999). “Clearly,

there are limits to how far HI can be further increased in improved varieties

[of rice] (Peng et al., 1994).”

The lack of increase in yield potential per plant is surprising until one

reflects on the fact that up until now, the sole method of increasing yield per

unit area has been to increase plant density while maintaining constant ear

size (grain weight per plant). Although theoretically it may be possible to

raise yields per unit area by increasing yield per plant while holding popula-

tion constant (at lower densities than present norms), for one reason or other

this has not been done except in experimental studies (e.g., Fasoula and

Fasoula, 2000; Tokatlidis et al., 2001). Such a goal might be practical,

however, for hybrids suited for drought-prone environments, where planting

at lower density is prudent but the ability to utilize occasional higher rainfall

by increasing yield per plant would be desirable.

The relative lack of increase in heterosis, either absolute or relative, also

will surprise those of us who have supposed that the primary way to increase

hybrid yield is to increase heterosis for grain yield. It would appear that

comments by Hallauer (1999, p. 486) about recurrent selection can apply to

hybrids as well. He stated, “the additive effects of alleles with partial

to complete dominance were of greater importance but dominant and epi-

static effects could not be discounted.” It is also intriguing to note that

absolute heterosis for grain yield is greatest under conditions of stress, in

company with the knowledge that an increase in stress tolerance of all kinds

has strongly accompanied gains in hybrid yield over the years. Both inbreds

and hybrids are greatly improved in stress tolerance, but hybrid gains are

greater that those of their parental inbreds.

B. POTENTIAL HELPS OR HINDRANCES TO FUTURE

GAINS in YIELD

For the past 70 years, breeders have improved the yielding ability of

hybrid maize by selecting new genotypes with adaptation to the ever-increas-

ing stresses of constantly increasing plant density as well as to other kinds of

prevalent abiotic and biotic stress. They have done so by exposing these

hybrids to an increasing diversity of environments as the capacity for wide

area testing (especially in the commercial sector during the past few decades)

has been dramatically increased by investments in mechanization and infor-

mation management. Breeders consistently have selected for higher average

yield with acceptable grain moisture, improved standability, resistance to

local diseases and insect pests (that often change in kind or intensity over the

years), and tolerance to increased plant density. (Farmers continually plant

the newest hybrids at a density higher than recommended, thus forcing


breeders to continually raise the density at which they select the next round

of hybrids.) Newer hybrids have managed the stress of high plant density

(which usually accentuates other kinds of stress) in two ways: increased

stress tolerance and increased efficiency of grain production.

Efficiencies in grain production that presumably are provided by more

upright leaves, smaller tassels, and lower grain protein percentage may have

gone about as far as they can go; leaves cannot be much more vertical

without clasping the stem, tassels on some hybrids have no side branches

at all, and it is possible that livestock feeders will not be willing to accept

grain with a smaller percentage of protein than is now at hand.

Therefore, breeders will need to make even greater progress in improving

traits for stress tolerance if they are to continue the linear increase in grain

yield that has prevailed during most of the past 70 years of hybrid maize

breeding. Increased emphasis on such traits as tolerance to extremes of

temperature, to drought, to excess soil moisture, and to deficiency of soil

nitrogen (without neglecting simultaneous selection under nonstressed, high-

yield conditions) will probably be worth the effort. For each of these traits,

development and deployment of managed stress levels (such as managed

irrigation in a rain-free climate) may increase the precision and reliability of

selection for the trait.

However, widespread on-farm testing in a full range of “natural” envir-

onments, from high yield to high stress, must be the rock on which all other

selections are based. Past experience has shown that overemphasis on a

single trait may produce correlated changes in other traits, sometimes with

unintended (and unwanted) results. There is no substitute for extensive

trials, in both small plot and strip test format, of hybrids in final stages

before release (and also just after release). Although one may not be able to

identify the different kinds of stress (or nonstress) in those trials with

precision, one can be sure that such testing will subject the genotypes to a

multitude of stresses common to the area of adaptation. Some of the stresses

will be severe to catastrophic and some will be so minimal that only the

hybrids can sense them. In the end the genotypes with the broadest tolerance

to these stresses will give the highest yields in both low-yield and high-yield

environments.

C. PREDICTIONS

Mark Twain is supposed to have said, “Prophecy is a good line of

business but it is full of risks.” This caution surely applies to predictions

about prospects for future yield gains in hybrid maize, or in other kinds of

maize cultivars.


Increased grain yield per semay be less important in the future than in the

past for an increasingly large part of maize production. Specialty products

such as maize with altered or higher oil or protein content, or high extract-

able starch, or maize bred for use as a biofuel may rise in importance in

addition to or sometimes in place of commodity feed grain production (e.g.,

Lambert et al., 1998; Ng et al., 1997; Whitt et al., 2002). Conceivably, some

of these novel kinds of maize could command a premium price. Although

yield of some kind would be important for these specialty categories of

maize, grain yield per se would take second place to yield of a specified

product—yield of a specific kind of oil, protein, starch, etc.

However, despite these possible new markets for specialty types of maize,

the demand for maize as a feed grain will increase robustly if the developing

world continues to improve its economy and therefore its appetite for meat,

milk, and eggs (Rosegrant et al., 2001; Taha, 2003). Consequently, produc-

tion of maize as a commodity grain for animal feed will continue to domi-

nate commercial maize production. Increasing the on-farm grain yield of

maize hybrids will persist as a primary goal of maize breeders. Farmers will

require (and demand) hybrids that dependably produce maximum yield

with minimum inputs—a key requirement for the profitable production of

commodity maize grain.

Although the past does not necessarily predict the future, 70 years of

linear genetic yield gain in many parts of the maize-growing world would

seem to predict that similar gains will continue for at least the next few

decades. This prediction is more likely to hold for regions that have recently

adopted hybrids and complementary intensive management practices. Pro-

duction in those regions will not be as near to the theoretical maximum yield

potential (Cassman, 1999; Duvick and Cassman, 1999) as may be true for

regions with a longer period of constantly increasing yields. However, even

in regions with longer periods of yield increase such as the U.S. corn belt,

continuation of the long-standing practice of remolding adapted germplasm,

and slowly and carefully importing useful pieces of exotic germplasm, will

guarantee increased yield potential and increased stability of yield for years

to come.

On-farm yields may not always rise in line with genetic improvements,

however. In the coming decades, residents of the wealthier countries may

force their farmers to reduce (or, in some cases, eliminate) applications of

synthetic fertilizers and/or pesticides, with the intention to improve environ-

mental and human health. Such reductions could reduce maize yields. Even

though the newer hybrids would yield more than the older ones (including

the OPCs) following such a reduction of inputs, their yields could very well

be lower than before reductions were put into effect, although the amount of

loss (if any) would depend on the extent of the input reductions.


If this speculated mandatory reduction of management inputs should

come to pass, one can envision a future in which genetic yield gains will

continue but on-farm yields will stagnate or decline. In other words, the

genetic improvement of critical traits might be needed simply to maintain

yields at an even level or to minimize reductions in yield. Without genetic

improvements, yields would drop even more. This scenario highlights the

importance of breeding for resistance to disease and insect pests, tolerance to

deficiency of soil nutrients, and tolerance to other locally important kinds of

abiotic stress.

One should note, however, that breeders have already made good prog-

ress in breeding for such kinds of tolerance/resistance. As shown repeatedly

in this review, breeding for increased resistance to abiotic and biotic stress

has been the basis for 70 years of yield increase and dependability in hybrid

maize. With stimulus from farmers and the marketplace, it seems reasonable

to suppose (and predict) that breeders can and would increase the intensity

of breeding for stress tolerance, with special emphasis on specific stresses

that were amplified by the reduction of specific inputs.

For example, data reviewed in earlier sections of this report indicate that

successive hybrids have shown steady and significant genetic improvement in

the efficient use of soil nitrogen, although the selection for improvement was

indirect (and unintentional). If application of nitrogen fertilizers should be

curtailed, maize breeders could select directly for efficient use of soil nitro-

gen, and should be able to make even faster progress than in earlier years.

Such progress might enable a continued increase (or at least prevent a

decline) in on-farm yields, despite mandated reductions in fertilizer use.

Likewise, with regard to pesticides, as noted earlier, a small number

of effective aids from biotechnology for genetic improvements in disease

and insect resistance are already in place and more are contemplated

(Fernandez-Cornejo and McBride, 2002; James, 2003a; Rice et al., 2003;

Runge and Ryan, 2003). Continuation and enhancement of these transgenic

breeding efforts could incrementally and significantly increase the ability of

farmers to maintain yields without the use of pesticides. (An example of

enhancement of transgenic protection would be to progress from the con-

struction of vertical resistance genotypes to building systems of horizontal—

more durable—resistance.) Importantly, the transgenic improvements will

be most useful if they are integrated with continuing achievements in con-

ventional breeding for pest resistance (which itself will be enhanced by new

knowledge and tools, contributed by molecular biology). In time, there will

be no distinction between “biotechnology protection” and “conventional

protection.”

For some maize producers, an even more drastic reduction in inputs may

occur in future years, as water for irrigation becomes less available in regions

where irrigation is important (and sometimes essential) for maize production


(Rosegrant et al., 2002). As with breeding for tolerance to nutrient imbal-

ance or biotic stresses, breeders in regions of water shortage will need to

increase their emphasis on breeding for drought tolerance, either by moving

from indirect to direct selection or by increasing the emphasis on already

existing direct selection for drought tolerance. Past experience indicates that

this trait can be improved without sacrificing the ability to produce high

yields with favorable water balance, and evidence now accumulating indi-

cates that these breeding efforts may someday be made even more efficient

because of new insights provided by molecular biology investigations. So, as

with postulated reductions in soil nutrient and pesticide application, bree-

ders should be able to mitigate yield reductions, or even maintain on-farm

yields, in many of the areas where irrigation is reduced or eliminated.

A less optimistic prediction, based on past experience, is that the price of

successive increases in genetic yielding ability will continue to rise, just as it

has risen during the past 70 years. In the United States, for example, today’s

crew of maize breeders (broadly defined to include those who work in

biotechnology applied to plant breeding) is many times larger than the

crew that made advances during the first two or three decades of hybrid

maize breeding (Crosby et al., 1985; Duvick, 1984a; Fernandez-Cornejo,

2004; Frey, 1996), yet the genetic yield gain per year is no larger than in

past times—the gain is linear. (And therefore the expenditure per unit gain is

many times larger now than in early years.) Judging from this past experi-

ence, today’s plant breeding crew will need to be enlarged even further if

future gains are to be made at the same pace as is now achieved unless much

more efficient methods of breeding are developed and implemented.

Some have predicted that significant gains in breeding efficiency will

occur as various tools of biotechnology are employed, utilizing new genetic

discoveries and new knowledge of genes and gene action in the maize plant.

However, the current state of the art primarily is in the development of

techniques and data (e.g., Emrich et al., 2004; Jansen et al., 2003; Lawrence

et al., 2004). Biotechnology is not the primary tool for the development of

improved cultivars. Although useful new traits have been added via trans-

genesis, the number actually in use is still small (but growing) and is limited

to such defensive traits as pest resistance and/or herbicide tolerance. Bree-

ders must continue to use routine empirical breeding methods to effect

broad-scale yield improvements in the “base germplasm,” which they then

can enhance with useful transgenes. Today’s maize breeders cannot reduce

the effort devoted to “conventional plant breeding” without also reducing

the rate of progress in the development and release of higher-yielding culti-

vars, cultivars with a full and well-balanced spectrum of the important traits

that in sum govern maize yield.

Additionally, the present large investment in the testing of transgenic

products for safety adds significantly to the cost of their use for genetic


improvement. Comments by soybean breeders on the use of biotechnology

for soybean breeding are relevant to its use in maize breeding, as follows:

“Despite all the opportunities, biotech soybeans face numerous challenges.

Because of the cost of technology and regulatory clearance, it is difficult

for developers to earn sufficient returns on research investment for many

biotech traits. Gaining acceptance of crops and grain derived through bio-

technology, particularly in Europe, is yet another challenge. Although

biotechnology acceptance is increasing around the world, significant chal-

lenges will be faced by those wanting to bring new transgenic traits to market

(Soper et al., 2003).”

One hesitates to predict how much time must pass before the current

investment in biotechnology can bring about significant savings in time and

money per unit gain in maize yield, even though it is obvious that biotech-

nology research and development indeed will give significant and innovative

support to maize breeding. New techniques, based on new knowledge in

molecular biology, are increasing breeding efficiency incrementally, and with

time the number and use of such new techniques can only grow. As stated by

Runge and Ryan (2003), “Plant biotech R&D in the pipeline as of 2001

through mid-2003 indicates almost a hundred new traits in testing. Repre-

sented in these activities are about 40 universities (mainly land grants) and

about 35 private sector companies. Without question, more research

and development as measured by field tests has been devoted to biotech

traits in corn than to any other crop, attracting scores of public and private

institutions. Among the traits in testing for corn were 19 new agronomic

properties, four traits for fungal resistance, seven for herbicide tolerance,

four for insect resistance, ten trials focusing on some form of marker genes,

and over 30 for output and other end-use traits.”

This leads to the author’s final prediction, that despite the efforts of some

segments of society (e.g., Turning Point Project, 1999a,b) to stop or other-

wise hinder the use of biotechnology as an aid in food production (for

detailed description of this subject, see Charles, 2001), the tools of molecular

biology increasingly will aid maize breeders in their efforts to develop

superior hybrids. The most important and long-reaching aid will come

not so much from transgenes per se as from the use of a wide range of

biotechnology-based tools to give breeders a deeper knowledge of the genet-

ics and physiology of the maize plant; with this knowledge they will be able

to fine-tune maize genomes to achieve desired ends with much greater speed

and efficiency.

Valuable assistance will continue to come directly from some classes of

transgenes, e.g., new and more broadly effective versions of Bt transgenes

(James, 2003a; Rice et al., 2003). Breeders in the tropics and subtropics will

have particular use for transgenes that impart effective resistance to the wide

array of disease and insect problems in those regions, especially for instances


in which adequate genetic resistance cannot be found in maize itself. In

all cases, these transgenes will prevent yield loss in the presence of epi-

demics and infestations of the pest in question. In those places where

pest depredation is chronic, yield levels on average will advance. However,

as noted earlier, the use of transgenes for pest resistance must move

beyond changes that contribute vertical resistance to those that impart

more durable kinds of horizontal resistance, not an easy task but one

that will become possible as biotechnology-based knowledge and insights

accumulate.

As biologists move beyond genomics to proteomics, metabolomics,

and other related disciplines (some as yet unnamed or undiscovered), they

will help maize breeders identify key genes and gene systems/interactions in

the maize plant, and then, working together, the molecular biologists and

breeders will learn how to regulate or reconstruct them in ways that

will intensify the expression of key traits, whether for tolerance to heat

and/or drought, to chronic disease problems, or to tolerance of deficiency

of soil nutrients such as nitrogen. Breeders will learn how to mine geneti-

cally diverse exotic maize populations for improved versions of key genes or

(more likely) their regulator systems and, with aid of molecular markers, to

move them into elite germplasm with precision and efficiency (see Tuberosa

et al., 2002). (Marker-assisted selection is already used extensively in some

crops, including maize, to move useful genes or linkage groups from exotic

to adapted germplasm and/or elite cultivars.) In some cases, knowledge of

the identity and/or function of important genes in other species (such as for

tolerance to certain kinds of abiotic stress) will enable biologists to identify

their counterparts in maize, enabling breeders and molecular biologists,

collaboratively, to fine-tune the actions of the maize genes, sometimes by

using key regulatory sequences from the exotic organism (e.g., Appenzeller

et al., 2004; Shou et al., 2004).

Of course, individual genetic changes will be useful only when they

efficiently interact with the complete genetic complex in ways that improve

the overall performance of the plant according to goals set by the breeder.

Knowledge of the ways in which expression of a key gene affects the action

and products of other genes (i.e., the pleiotropic and epistatic effects), and

consequent interactions with the environment, will be critical to the success

of improving the action of any individual gene.

Finally, beyond all these conjectured advances, the maize breeders

can always hope for the Holy Grail of plant physiologists, major improve-

ment in the efficiency of the primary steps of converting intercepted solar

radiation into stored carbon, effected without disrupting the rest of the

infinitely complicated network of interacting genetic systems and ensuing

physiological processes that operate the functioning maize plant or any

other organism.


However, in the end, after all the modern tools have been employed to the

maximum degree, maize breeders will still need to walk the fields, observing

their latest creations under the widest possible range of conditions that

commonly occur in the intended region of adaptation. (One could describe

this activity as “personal perusal and evaluation of the genotype � environ-

ment interaction.”) The breeders will collate this subjective and highly

personal information with objective information obtained from widespread

performance trials, laboratory analyses, and other factual tests of perfor-

mance. In brief, maize breeders will need to practice the art as well as the

science of breeding if they are to continue the genetic progress that has been

achieved by their predecessors during the past three-quarters of a century.

“As the joy of artistic creation begins to assert itself we may expect many

interesting developments in the newer methods of corn breeding (H. A.

Wallace, 1930, unpublished manuscript).”

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