Alastair Stutt

Dave Froman

Matt Gage

Nina Wedell

Paul Ward

Scott Pitnick

Ted Morrow

Tom Tregenza

Tracey Chapman

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TREE vol. 15, no. 3 March 2000 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(99)01798-X 85
Evolutionary biologists really got inter-ested in sperm only after the realiz-
ation that if more than one male insemi-
nates a female, their sperm will be in
competition1. At last, we had a plausible
explanation for the absurdly large num-
bers of sperm found in most species, and
an entirely new field sprang up examining
how sperm competition occurs and how
males have adapted to it. Now, nearly 
30 years later, we have progressed from
concentrating on interactions between
males to considering the roles of both
sexes, their conflicting interests and the
evolutionary consequences of everything
that goes on between copulation and ferti-
lization2. The 5th Biology of Spermatozoa
meeting* echoed the field’s broadening
horizons and its fundamental role in
understanding sexual selection.
Instead of regarding females as pas-
sive receptacles for sperm, the dominant
paradigm is now to regard interactions
between the sexes as an ongoing conflict.
Males attempt to inseminate as many
mates as possible, even if this has costs
for females, and females attempt to avoid
these costs and to control fertilization of
their eggs. A classic example of a male
trait detrimental to females is the ejacu-
late of Drosophila melanogaster, which
contains toxins that reduce female life-
span but increase sperm storage and
delay female remating3. Tracey Chapman
(University College, London, UK) and col-
laborators are now identifying specific
chemicals involved in male manipulation
of females. To achieve this, they use mu-
tant males that lack particular ejaculate
proteins and separate their effects from
those of the sperm themselves by using
spermless irradiated males. This reveals
that males who lack one glycoprotein, the
evocatively named ‘Acp36DE’, are less
able to displace the sperm of previous
males and have their own sperm stored
by the female. The magnitude of this dis-
advantage depends on whether sperm
are transferred, indicating that both ac-
cessory proteins and sperm themselves
are involved in sperm competition and
female manipulation.
A more drastic male tactic is employed
by bed bugs (Cimex lectularius). In this
species, males pierce the female body
wall and inject sperm directly into her
body cavity from where it migrates to 
the ovaries. Alastair Stutt (University of
Sheffield, UK) has found, as might be
expected, that this makes mating costly,
with females exposed to more matings
having substantially reduced lifespans.
Of course, females are not passive vic-
tims of aggressive male strategies – sexual
conflict drives coevolution between males
and females. This process can be seen 
in action in multigenerational lines of 
D. melanogaster, in which one pair of lines
has females kept with four males (poly-
andry), and the other pair has females
kept with a single male (monandry)4.
Brett Holland (University of California,
Lafayette, USA) described how, after 32
generations, males from the monandrous
line are more benign when mated to test
females and also court less readily. Simi-
larly, monandrous-line females suffered
more when mated to a test male than
polyandrous females, indicating that they
had lost some of their resistance to toxic
effects of male ejaculates. Both results
indicate that within a few generations
both sexes adapt to a reduction in sperm
competition. 
Holland has passed his selected lines
on to Scott Pitnick (University of Syracuse,
NY, USA), who is investigating differences
in sperm competitive ability between the
lines. Although this work is ongoing, it is
already apparent that males from the poly-
androus lines are more successful when
their sperm are in competition with those
of a previous male than are males from
the monandrous line. The reduction in
sperm-competition ability in monandrous
males suggests that success in sperm
competition has costs, either directly or
through reducing female fecundity.
The generality of costs of sperm 
competition to both sexes found in 
D. melanogaster could be investigated by
comparing patterns of male–female inter-
actions across populations or species of
other taxa. However, it was pointed out
by Geoff Parker (University of Liverpool,
UK) that even rare polyandry (as tends to
be found in apparently monogamous spe-
cies) theoretically is predicted to create
similar selection pressures on males as
rampant polyandry5. This suggests that
differences between completely monan-
drous and polyandrous selection lines
might not be seen between populations
differing in their degree of polyandry in
natural situations.
As well as adapting to male sperm-
competitive tactics, there is growing evi-
dence that females exercise considerable
control over inseminated sperm, and
might even actively choose to fertilize
their eggs with sperm from particular
males6. An example of such behaviour
has been studied by Tommaso Pizzari
(University of Sheffield), who showed
that female feral chickens can not only
physically eject inseminated sperm, but
that they do so more frequently when
inseminated by a lower ranking male.
However, chickens might be out-done by
female dungflies, which are equipped
with multiple sperm storage organs from
which they release sperm to fertilize
their eggs. Paul Ward (University of
Zurich, Switzerland) found that flies
reared from eggs collected from shady or
sunny areas of a cowpat differ in the fre-
quency of different forms of the enzyme
phosphoglucomutase (PGM). Because
PGM differences are associated with dif-
ferences in the effect of temperature on
larval growth, Ward suggests that multi-
ply mated females can selectively use
sperm from males differing in PGM geno-
type according to whether an egg is being
laid in a sunny or shady position7.
With growing interest in the effects of
selection on sperm characteristics has
come recognition of the need to exam-
ine their genetics and heritability. Ted
Morrow (University of Liverpool) exam-
ined 11 species from humans to insects
and found significant differences in
sperm length between males in all cases.
This supports the consensus that sperm
characteristics are controlled by the pa-
ternal genotype, rather than by sperm
themselves, because haploid expression
would predict high variation within the
ejaculate of a single male. Using field
crickets (Gryllus bimaculatus), Morrow
demonstrated that sperm length can be
artificially selected and that much vari-
ability may be carried on the X chromo-
some. If this is the case, males with long
sperm cannot pass the trait to sons, but
have daughters who pass the trait to
their own sons. So, if sperm length comes
under directional selection, this has to
act through the success of grandsons.
Although the benefits of having sperm
of a particular length are not clear, hav-
ing more mobile sperm is likely to be
advantageous. David Froman (Oregon
State University, Corvalis, USA) has
found that male chickens differ in sperm
mobility independent of differences in
body mass or overall sperm production.
Again, these differences are heritable,
with much higher measured heritability
through females (the heterogametic sex
in birds) than through males. This dif-
ference does not appear to be due to 
nongenetic maternal effects, suggesting
that variation in sperm mobility re-
flects variation in mitochondria (which
are inherited only through eggs). This 
is intriguing because Tim Birkhead’s
work (University of Sheffield) on the
NEWS & COMMENT
Evolutionarily dynamic sperm
*Biology of Spermatozoa, University of
Sheffield, UK, 28–31 October 1999.
86 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(99)01803-0 TREE vol. 15, no. 3 March 2000
same species indicates that sperm traits
might be under directional selection. Fe-
males inseminated with a mixture of
sperm from two males differing only in
sperm mobility had more of their eggs
fertilized by the male with higher mo-
bility sperm8. If mobility differences are
due to mitochondria, then selection will
not be able to act on them, because even if
males with particular mitochondrial geno-
types are more successful in fertilizing
eggs, none of their offspring will inherit this
characteristic. Therefore, mitochondrial
inheritance provides a potential expla-
nation for the maintenance of variation in
a directionally selected trait.
Overall, the meeting clearly demon-
strated that our current understanding of
the role of postcopulatory processes is
just the tip of the iceberg. To have any
hope of understanding the extravagant
world of sexual selection, we must con-
sider the world of the sperm.
Acknowledgements
Thanks to Tim Birkhead and Harry Moore
for organizing the meeting and to 
Nina Wedell, Paul Ward, Alastair Stutt,
Scott Pitnick, Ted Morrow, Matt Gage, 
Dave Froman, Tracey Chapman and 
Tim Birkhead for helpful comments on this
article. The meeting was supported by the
Association for the Study of Animal
Behaviour and the Wellcome Foundation.
Tom Tregenza
Ecology and Evolution Group, 
School of Biology, 
University of Leeds, 
Leeds, UK  LS2 9JT 
(gentbt@leeds,ac,uk)
References
1 Parker, G.A. (1970) Sperm competition and its
evolutionary consequences in the insects. Biol.
Rev. 45, 525–567
2 Birkhead, T.R. and Møller, A.P. (1998) Sperm
Competition and Sexual Selection, Academic
Press
3 Chapman, T. et al. (1995) Cost of mating in
Drosophila melanogaster females is 
mediated by male accessory-gland products.
Nature 373, 241–244
4 Holland, B. and Rice, W.R. (1999) 
Experimental removal of sexual selection
reverses intersexual antagonistic 
coevolution and removes a reproductive 
load. Proc. Natl. Acad. Sci. U. S. A. 96,
5083–5088
5 Parker, G.A. et al. (1997) Sperm competition
games: a prospective analysis of risk
assessment. Proc. R. Soc. London B Biol. Sci.
264, 1793–1802
6 Eberhard, W.G. (1996) Female Control: Sexual
Selection by Cryptic Female Choice, Princeton
University Press
7 Ward, P.I. (1998) A possible explanation for
cryptic female choice in the yellow dung fly,
Scathophaga stercoraria (l.). Ethology 104,
97–110
8 Birkhead, T.R. et al. (1999) Sperm mobility
determines the outcome of sperm competition
in the domestic fowl. Proc. R. Soc. London 
B Biol. Sci. 266, 1759–1764
One hundred and twenty-eight yearsafter Darwin first described the two
processes of sexual selection – male–male
competition and female choice – the lat-
ter component continues to cause con-
troversy. The main debate lies in those
cases, such as lekking species, where
females apparently obtain nothing but
semen from the male with which they
copulate. In such species, males con-
tribute no paternal care, and thus it is
assumed usually that females obtain only
indirect or genetic benefits from their
choice of partner. Consequently, female
choosiness in return for no obvious ben-
efit is referred to as the ‘lek paradox’1.
Several different types of genetic benefit
are plausible2, but the one that has
attracted the most interest is the idea of
viability genes. This ‘good genes’ hypoth-
esis has been difficult to test, but there is
now some evidence for it because several
studies have reported increased viability
of offspring fathered by attractive males3.
Researchers testing the good genes hy-
pothesis have had to be careful to avoid
the possible confounding influence of
maternal effects. For example, over ten
years ago, it was shown that within pairs
of zebra finches (Taeniopygia guttata), fe-
males paired to attractive males invested
more in offspring than females paired to
less attractive males4; this raised the possi-
bility that any increase in the viability of
offspring fathered by attractive males
could be due either to a maternal effect
(increased investment by the mother), to
the father’s ‘good genes’ or, more prob-
ably, to both (given that females are 
expected only to invest more if they in-
crease their fitness). Several studies look-
ing for good gene effects in birds have
attempted to control for maternal effects;
for example, by hatching eggs in incuba-
tors5, but, of course, this does not pre-
clude the possibility of differential mater-
nal investment before egg-laying. A new
study of zebra finches by Gil et al.6 has
shown that one maternal effect in particu-
lar – the amount of testosterone de-
posited in eggs – could have a profound
influence on a female’s offspring, in a way
that varies according to the attractive-
ness of her mate.
Gil et al. found that in captivity female
zebra finches deposit relatively more of
the androgens testosterone and 5a-dihy-
drotestosterone into their eggs when
paired to an attractive male. They were
able to demonstrate this in a particularly
elegant manner, because the attractive-
ness of male zebra finches (Fig. 1) can be
manipulated by the addition of colour-
rings – red rings render males more 
attractive and green rings reduce male
attractiveness7. Gil et al. looked at andro-
gens in the eggs of females paired to the
same males wearing red or green rings in
different clutches. Females put signifi-
cantly more androgens into their eggs
when their male social partner wore red
rings compared with when the same male
wore green rings.
In canaries, Serinus canaria, a higher
level of androgens in the egg gives chicks
of both sexes a head start in several ways
– in the nest they beg more and grow
faster, and they have higher social rank
once fledged8,9. Gil et al. assume that simi-
lar advantages would accrue in zebra
finches hatching from high androgen eggs.
With these advantages, why don’t
females put similar amounts of andro-
gens into all eggs regardless of their part-
ner’s apparent quality? Gil et al. suggest
that androgens might be costly, either to
the mother or to her offspring; for exam-
ple, by suppressing the immune system.
They propose also that only offspring
fathered by genuinely high quality males
would be able to withstand the high con-
centration of androgens. There are other
potential costs not mentioned by Gil et al.;
for example, although increased growth
might provide short-term benefits, other
studies of zebra finches indicate that it can
result in reduced subsequent survival10.
These remarkable results raise sev-
eral other questions. The zebra finch is a
socially monogamous species, but (in
common with many other passerine birds)
also engages in extra-pair copulations
(EPCs), which result in extra-pair paternity
NEWS & COMMENT
Testosterone and maternal effects –
integrating mechanisms and function


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