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NEWS AND COMMENTARY
Gems from the Heredity archive
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Bateman (1948): pioneer in the
measurement of sexual selection
MJ Wade and SM Shuster
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Heredity (2010) 105, 507–508; doi:10.1038/hdy.2010.8; published online 10
February 2010
Darwin (1871) identified sexual se-
lection as the process whereby the
members of one sex, generally
males, compete with one another for
reproductive access to members of the
other sex, generally females. He argued
that sexual selection should be a much
stronger evolutionary force in poly-
gamous than in monogamous mating
systems, and that, in the former, such
selection would fall primarily on mem-
bers of the male sex. Nearly 80 years
later, in his classic fruit fly study, Bate-
man (1948) reported the first empirical
demonstration that the cause of the sex
difference in intensity of selection was
variation among males in mate num-
bers. This seminal paper set the stage
for much of the modern research into
sexual selection.
Bateman’s stated goal was to identify
(p 352) ‘a fundamental cause of intra-
masculine selection, independent of
mating system and probably inherent
in the mechanics of sexual reproduc-
tion.’ He presumed that this cause
would reveal ‘why it is a general law
that the male is eager for any female,
without discrimination, whereas the
female chooses the male.’ Bateman
addressed the matter of sex differences
not in terms of behavior, as Darwin
did (with ‘arduous’ males and ‘coy’
females), but rather in terms of the
intensity of intra-sexual selection acting
within each sex. Bateman then inter-
preted his results in terms of sexual
differences in morphology, including
gamete size and tendencies to provide
parental care. Thus, Bateman’s contri-
bution simultaneously gave rise to the
two leading approaches to sexual selec-
tion and mating systems research that
exist today: (1) the conceptual and
empirical focus on sex differences in
parental investment (Williams, 1966;
Trivers, 1972; Emlen and Oring, 1977)
and (2) the theoretical and empirical
focus on measuring sexual selection itself
(Wade, 1979; Wade and Arnold, 1980;
Shuster and Wade, 2003; Jones, 2009).
In his experiments, Bateman estab-
lished 64 fly populations organized into
nine ‘series,’ each designed to explore
mating success and fitness for each sex
and to control for the effects of different
genetic markers, mating schedules, fe-
male life histories and genetic back-
grounds. Whereas modern sexual
selection researchers use microsatellites
to document paternity and maternity,
Bateman used a suite of visible single-
gene mutations to uniquely identify the
parents of each offspring in his popula-
tions. Although Bateman’s genetic mar-
kers did not have the advantage of
neutrality that microsatellites do, this
apparent constraint necessitated his
extraordinarily detailed set of experi-
mental controls, as well as the elegant
statistical methods used in analyzing his
results.
For example, to avoid inbreeding,
Bateman used different markers in
males and in females, guaranteeing that
all offspring from which matings per
parent were to be inferred would be
double heterozygotes, not homozygotes.
Bateman also emphasized that he was
measuring the actual fertility of indivi-
duals rather than their potential con-
tributions to the next generation. He
recognized how this limited his infer-
ences of the number of mating attempts:
‘the number of inseminations y
should, however, be regarded as a
minimum, for two reasons: the possibi-
lity that some matings might be ineffec-
tive, and the inability to distinguish
single and multiple inseminations in-
volving the same pair of flies.’ (p 353).
The same limitations apply to micro-
satellite estimates of parentage, but are
seldom as well recognized. Bateman
also noted that uncontrolled viability
differences among matings were more
likely to reduce rather than increase the
variance in offspring numbers within a
series, making his observed results
conservative.
Even with these constraints, Bate-
man’s results were consistent and
striking. He observed a sex difference
in the variance in fertility that was
greater for males than for females in
every series. Bateman also noted (Table 7;
p 360) ‘whereas only 4% of females
were unrepresented in progeny, 21% of
the males were unrepresented.’ Males
were five times more likely to fail in
reproductive competition than females.
Importantly, when Bateman subtracted
the sum of squares owing to the effect of
mate numbers from the total sums
of squares, he found the remainder to
be equal for the two sexes. He summar-
ized his findings in the often-repeated
quotation: ‘Variance in number of mates
is, therefore, the only important cause of
the sex difference in variance of ferti-
lity.’ These famous words were also
presented in his Figure 1 (p 362) as a
linear relationship between mate number
and offspring number for males and a
much smaller, but similar effect for
females. Such regressions today are com-
monplace and are referred to as ‘Bateman
Gradients’ (Arnold and Duvall, 1994),
consistent with Bateman’s observation
that ‘a sex difference in the variance in
fertility is therefore a measure of the sex
difference in intensity of selection.’
Several authors have claimed that
Bateman’s methods were flawed, inclu-
ding sampling problems that resulted
in unequal male and female mean
reproductive success, miscalculations
of variances, statistical pseudoreplica-
tion and selective presentation of data
(Snyder and Gowaty, 2007). These
authors imply that Bateman was
hindered in his conclusions by the
limitations of the markers he used, and
further that he was careless, even
dishonest, in how he conducted his
measurements and analyses. A careful
reading of Bateman (1948) reveals that
nothing could be further from the truth.
Bateman’s original emphasis was on
mean squares to capture the ‘gross
variability’ in fertility among males
and among females within each mating
series. In every case, even when reci-
procal matings were made between
males and females from different mar-
ker lineages, the variation in male
fertility was significantly greater than
for females. Far from an attempt to
inflate the degrees of freedom used in
his analysis, this approach accurately
measured the fitness variance for each
sex within each series, and his signifi-
cance tests of these variance ratios
showed the relationship he needed to
make his points.
Other authors (Sutherland, 1985;
Hubbell and Johnson, 1987) have sug-
gested that, because random mating can
lead to sex differences in mating suc-
cess, Bateman’s data do not show the
actual cause of sexual selection. This
Heredity (2010) 105,507–508
&
2010 Macmillan Publishers Limited All rights reserved 0018-067X/10 $32.00
www.nature.com/hdy
criticism ignores Bateman’s partitioning
of the separate variance component for
mate numbers from the total variation
in fertility, as well as the internal
consistency of the results across series,
and the layers of controls he applied.
The authors, as well as other adherents
to the notion that chance is causal in
studies of sexual selection, neglect to
acknowledge that chance is part of any
study of selection. Some individuals
survive, mate and reproduce by chance,
whereas others do not, even if preferred
or favored attributes exist within the
population. This is why the probability
of fixation of a ‘good gene’ with positive
effect on fitness, s40, is only 2sinstead
of 1.0 (Kimura, 1962).
What makes Bateman’s results defini-
tive is that certain markers appeared
disproportionately among progeny, in-
dicating that some individuals mated
and others did not. This result led to the
most enduring conclusion of his work,
the signature cause of sexual selection:
the sex difference in fertility, which
causes the positive regression of off-
spring numbers (fertility) on mate num-
bers for males. Bateman distilled his
findings to a single statement that is as
powerful today as it was in 1948 (p 364):
‘Variance in number of mates is, there-
fore, the only important cause of the sex
difference in the variance in fertility.’
Conflict of interest
The authors declare no conflict of inter-
est.
Dr MJ Wade is at the Department of Biology,
Indiana University, 1001 East 3rd Street, Bloo-
mington, IN 47405, USA and Dr SM Shuster is at
the Department of Biological Sciences, Northern
Arizona University, Flagstaff, AZ 86011-5640,
USA.
e-mail: mjwade@indiana.edu
Arnold SJ, Duvall D (1994). Animal mating
systems: a synthesis based on selection theory.
Am Nat 143: 317–348.
Bateman AJ (1948). Intra-sexual selection in
Drosophila. Heredity 2: 349–368.
Darwin CR (1871). The Descent of Man and Selection
in Relation to Sex. Appleton: New York.
Emlen ST, Oring LW (1977). Ecology, sexual
selection, and the evolution of mating systems.
Science 197: 215–223.
Hubbell S, Johnson L (1987). Environmental
variance in lifetime mating success, mate
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91–112.
Jones AG (2009). On the opportunity for sexual
selection, the Bateman Gradient and the max-
imum intensity of sexual selection. Evolution
63: 1673–1684.
Kimura M (1962). On the probability of fixation
of mutant genes in a population. Genetics 47:
713–719.
Shuster S, Wade M (2003). Mating Systems and
Strategies. Princeton University Press: Princeton,
NJ.
Snyder BF, Gowaty PA (2007). A reappraisal of
Bateman’s classic study of intrasexual selec-
tion. Evolution 63: 2457–2468.
Sutherland WJ (1985). Measures of sexual selec-
tion. Oxford Surv Evol Biol 2: 90–101.
Trivers RL (1972). Parental investment and sexual
selection. In: Campbell B (ed). Sexual Selection
and the Descent of Man. Aldine Press: Chicago,
IL, pp 136–179.
Wade MJ (1979). Sexual selection and variance in
reproductive success. Am Nat 114: 742–764.
Wade MJ, Arnold SJ (1980). The intensity of sexual
selection in relation to male sexual behaviour,
female choice, and sperm precedence. Anim
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Williams GC (1966). Adaptation and Natural Selec-
tion. Princeton University Press: Princeton, NJ.
Editor’s suggested reading
Johnston SE, Beraldi D, McRae AF, Pemberton JM,
Slate J (2010). Horn type and horn length genes
map to the same chromosomal region in Soay
sheep. Heredity 104: 196–205.
Dobler R, Hosken DJ (2010). Response to selection
and realized heritability of sperm length in
the yellow dung fly (Scathophaga stercoraria).
Heredity 104: 61–66.
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