The Indirect Benefits of Mating
with Attractive Males
Outweigh the Direct Costs
Megan L. Head1*, John Hunt1, Michael D. Jennions2, Robert Brooks1
1 School of Biological, Earth and Environmental Sciences, the University of New South Wales, Sydney, Australia, 2 School of Botany and Zoology, The Australian National
University, Canberra, Australia
The fitness consequences of mate choice are a source of ongoing debate in evolutionary biology. Recent theory
predicts that indirect benefits of female choice due to offspring inheriting superior genes are likely to be negated when
there are direct costs associated with choice, including any costs of mating with attractive males. To estimate the
fitness consequences of mating with males of varying attractiveness, we housed female house crickets, Acheta
domesticus, with either attractive or unattractive males and measured a variety of direct and indirect fitness
components. These fitness components were combined to give relative estimates of the number of grandchildren
produced and the intrinsic rate of increase (relative net fitness). We found that females mated to attractive males incur
a substantial survival cost. However, these costs are cancelled out and may be outweighed by the benefits of having
offspring with elevated fitness. This benefit is due predominantly, but not exclusively, to the effect of an increase in
sons’ attractiveness. Our results suggest that the direct costs that females experience when mating with attractive
males can be outweighed by indirect benefits. They also reveal the value of estimating the net fitness consequences of
a mating strategy by including measures of offspring quality in estimates of fitness.
Citation: Head ML, Hunt J, Jennions MD, Brooks R (2005) The indirect benefits of mating with attractive males outweigh the direct costs. PLoS Biol 3(2): e33.
Whether mate choice can be maintained by indirect
selection when females incur direct costs by being choosy is
the subject of ongoing theoretical controversy [1,2,3,4,5]. This
is particularly true when the principal or only benefit of
mating with attractive males is that they sire attractive sons.
Weatherhead and Robertson  suggested 25 y ago that the
genetic benefits of mating with an attractive male could
outweigh the cost of reduced investment in parental care that
such a male makes. This suggestion has been opposed by
several important theoretical models [5,7,8]. More generally,
some recent theoretical work has suggested that because of
the weakness of indirect selection relative to direct selection,
genetic benefits of choice are likely to have little effect on the
evolution of costly mate choice [2,3]. This assertion has been
contested by other theoretical work .
In order to understand how mate choice evolves, it is
necessary to estimate the overall effect of mate choice on
female fitness [9,10,11,12]. The effect of mating with males of
differing attractiveness on total female fitness depends on
both positive and negative effects on a variety of fitness
components. The signs and strengths of these effects are
paramount to distinguishing between the relative importance
of various models of mate-choice evolution.
Evidence from studies that have measured one or a few
fitness components has been invoked to support direct
benefits [13,14], ‘‘viability genes’’ [15,16,17,18], ‘‘Fisherian
runaway’’ [19,20], and ‘‘sexually antagonistic coevolution’’
[21,22] models of mate-choice evolution. Similar evidence has
also been used in tests for differential allocation of
reproductive effort to offspring sired by attractive males
[14,23,24]. Understanding the relative significance of these
processes, however, requires measuring as complete a set of
fitness components as possible [12,19] and estimation of the
multigenerational effects of mate choice on fitness [11,25]
through both sons and daughters [12,26]. To date, only two
studies have compared the number of grandchildren
produced when females mate with attractive or unattractive
males [10,16]. Unfortunately, neither study accounted for the
beneficial effects of heritable male attractiveness, an im-
portant consideration in most models of mate-choice
How fitness should be estimated is controversial [27,28].
Measuring total fitness is logistically preclusive, but rate-
insensitive estimates, such as the number of grandchildren, or
rate-sensitive estimates, such as the intrinsic rate of increase,
may offer reasonable approximations [10,11,25]. The key
difference between these two estimates is that rate-sensitive
estimates take into account both the timing of reproduction
and the developmental time of offspring, whereas rate-
insensitive measures do not. To date, most empirical studies
have employed rate-insensitive estimates, whereas theoretical
models tend to focus on the intrinsic rate of increase .
Received September 7, 2004; Accepted November 22, 2004; Published
January 25, 2005
Copyright: ? 2005 Head et al. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the
original work is properly cited.
Abbreviation: rest, relative intrinsic rate of increase
Academic Editor: Paul Harvey, University of Oxford, United Kingdom
*To whom correspondence should be addressed. E-mail: megan.head@student.
PLoS Biology | www.plosbiology.orgFebruary 2005 | Volume 3 | Issue 2 | e330289
Open access, freely available online P PL Lo oS S BIOLOGY
Here, we measured both direct and indirect fitness
components of female house crickets, Acheta domesticus, mated
to either attractive or unattractive males for the term of their
adult life span. We present a female’s total fitness as both a
rate-sensitive (the intrinsic rate of increase) and a rate-
insensitive estimate of fitness (the total number of grand-
children) in interpreting our findings.
Our treatment did not affect the number of grandchildren
produced via daughters, via sons, or in total (Table 1). Thus
there was no difference in the rate-insensitive estimate of
fitness for females mated to males of differing attractiveness.
Females that mated with attractive males did, however,
experience higher relative intrinsic rates of increase (rest)
than females mated with unattractive males (Table 2).
The overall difference between the treatments on restwas
not due to any single fitness component (Table 2). When
looking at the fitness components individually, the strongest
effects were a survival cost experienced by females mated to
attractive males (Figure 1), and an indirect benefit because
sons of attractive males were more than twice as likely to
mate as those of unattractive males (see Table 1). However,
neither of these components alone can explain the significant
difference in restbetween females mated to attractive or to
unattractive males (see Table 2). Treatment differences in
other fitness components, although individually not signifi-
cant, still influenced our estimates of the overall fitness
consequences of mating with attractive males. In particular
the combined effect of sons’ attractiveness and daughters’
fecundity had a significant effect on our model (see Table 2).
When we combined a female’s egg number, egg width, and
egg length (from the first week of egg laying) into a single
index of reproductive effort, we found that females mated to
attractive males exerted greater reproductive effort in the
first week of the experiment than those mated to unattractive
males (principal component 1: attractive = 0.239 6 0.116,
unattractive =?0.233 6 0.199, randomisation test p = 0.043).
Of the constituent measures of week 1 reproductive effort,
only egg width differed significantly between treatments (egg
number: attractive = 129.07 6 15.08, unattractive = 108.17
6 18.84, p = 0.382; egg width: attractive = 0.618 6 0.008,
unattractive = 0.568 6 0.014, p = 0.005; egg length: attractive
= 2.71 6 0.017, unattractive = 2.68 6 0.025, p = 0.373).
To provide an inclusive estimate of the total fitness
consequences of mating with an attractive or unattractive
male, we quantified both the direct costs to females and the
indirect benefits to their offspring. We made two main
findings. First, the mating-associated costs borne by females
are greater when mating to attractive males throughout their
Table 1. The Effects of Mating with Either Attractive or
Unattractive Males on a Number of Fitness Components
Category Fitness ComponentAttractive,
Relative number of grandchildren
Direct fitness components
Lifetime fecundity (eggs)
Indirect fitness components via sons
Generation time (days)
Weight at maturity (mg)
Indirect fitness components via daughters
Generation time (days)
Weight at maturity (mg)
Table 2. The Sensitivity of restto Variation in Individual and
Combined Fitness Components
(? raVersus ? ru)
Excluding fitness components via sons
Generation time (a)
Number maturing (b)
Excluding fitness components via daughters
Generation time (e)
Number maturing (f)
Combined fitness components
a and b
a and c
a and d
a and e
a and f
a and g
b and c
b and d
b and e
b and f
b and g
c and d
c and e
c and f
c and g
d and e
d and f
d and g
e and f
e and g
f and g
In each reduced model individual females’ scores for the component(s) listed were replaced with experiment-wide
mean scores. ? raand ? ruare the mean restfor females mated with attractive and with unattractive males, respectively.
Test 1 indicates the significance of the ? raversus ? rucomparison within the reduced model (based on 10,000
randomizations). Test 2 assesses the significance of the change in effect size (based on 10,000 jackknifed
pseudoestimates) between the reduced model and the full model.
PLoS Biology | www.plosbiology.orgFebruary 2005 | Volume 3 | Issue 2 | e330290
Indirect Benefits Outweigh Direct Costs
life than when they are mated to unattractive males. Second,
these costs are cancelled out (when we use the rate-insensitive
measure of the number of grandchildren) and may be
outweighed by (when we use the rate-sensitive estimate of
the intrinsic rate of increase) the benefits of having offspring
with elevated fitness (i.e., indirect benefits).
Contrary to some theoretical predictions [2,3,5], but see
[1,6], our results suggest that it may be possible for female
mate choice to evolve via indirect benefits, despite the
presence of direct costs. Whether this is the case or not will,
however, depend on the magnitude of other costs of choice
not measured here, such as the costs associated with being
choosy, as well as the accuracy of female choice .
The costs of choice, including the costs of mating with
attractive males, are of central importance to theoretic
models of mate-choice evolution [1,2,3,4,5,29]. In many
species females incur survival or fecundity costs due to being
courted or harassed by males [30,31], mating [32,33], and
allocating resources to egg laying, gestation, and/or parental
care . Female Drosophila melanogaster mated to large (and
thus presumably attractive) males incur a greater survival cost
than females mated to smaller males [21,22], and this appears
to be due to a higher mating rate with large males . A
potential criticism of such studies is that they are based on
single traits that are taken to be an indirect measure of a
male’s attractiveness. By using a direct biological measure
that incorporates all traits that contribute to a male’s ability
to induce a female to mate during short-range courtship, our
results provide the first direct evidence that females sustain
greater direct costs when mating with males that are more
attractive in this context.
While we do not know the exact mechanisms driving the
survival cost seen in our experiment, our finding that females
mated to more attractive males experience lower survival is
consistent with sexual conflict between males and females
over mating decisions [25,35], and with differential allocation
. Females mated to attractive males exerted greater
reproductive effort in the first week of the experiment. This
could be the result of male manipulation, for example,
increased mating rate , or stimulants in seminal fluids
[36,37,38] whereby more attractive males manipulate females
to invest more in their offspring than is optimal for the
females. The possibility of male manipulation is also
supported by a study by Murtaugh and Denlinger , which
shows that in A. domesticus, males pass substances in their
ejaculate that promote higher rates of short-term oviposition.
Alternatively, it may be adaptive for females to invest more in
the offspring of attractive males [34,40]. Differential alloca-
tion is only likely to be adaptive if there is an indirect fitness
benefit to allocating greater reproductive effort when mated
to attractive males . The indirect fitness benefits that we
report here, particularly the benefit of having more attractive
sons, may provide an adaptive basis for differential allocation
by females to the offspring of more attractive males.
Several studies have reported fitness benefits of mating
with attractive males. Females mated to such males have been
reported to have offspring that have greater longevity [15,41],
faster growth rate [16,17,42], increased fecundity of daughters
[16,42], and increased attractiveness of sons [19,20,42,43,44].
In our study, the net fitness benefit of mating with attractive
males is not due to any single indirect benefit but to a
combination of fitness components. This illustrates the
importance of measuring net fitness, especially if fitness
components act in opposition to each other.
A number of studies have proposed the use of an aggregate
measure of male attractiveness rather than a single morpho-
logical indicator [44,45]. Our use of time to mounting allows
us to gain a measure of male attractiveness that is based on all
traits that contribute to male mating success (hence ‘attrac-
tiveness’) during short-range courtship interactions . It is
the use of such a measure that may explain the high
correlation between fathers’ and sons’ attractiveness in this
experiment and others based on similar measures [12,44]. The
greater attractiveness of sons sired by attractive males may
also be explained by differential allocation; studies have
shown that maternal effects may enhance the heritability of
male traits . An important role for maternal effects is
unlikely in our experiment, however, because no other fitness
components of sons or daughters differ significantly between
the treatments. Regardless of whether sons’ greater attrac-
tiveness is due to additive genetic variation for attractiveness
per se or to the ability to manipulate females into allocating
more resources to the offspring, such a trait will increase a
female’s net fitness if it increases the reproductive success of
her sons sufficiently.
Due to the nature of our experimental design we were
unable to measure all the costs and benefits associated with
choosing and mating with attractive males. First, we did not
measure sons’ ability to compete with other males for access
to females. However, in this population of A. domesticus,
fighting ability has been shown to be positively correlated
with attractiveness as we have measured it here [48,49]. Thus,
if anything we may have underestimated the fitness benefit
gained through having attractive sons. Second, we did not
measure long-range attraction of males through advertise-
ment calling. Third, our design simplifies the way mating
takes place for females paired with attractive or unattractive
males. Pairing females with a single male for 7 d at a time may
Figure 1. Female Survival in Relation to Experimental Treatment
Femaleshoused alone (black line) survived longerthan females housed
with either type of male (Cox regression Wald1= 29.636, p = 0.000).
Females mated to unattractive males (blue line) survived longer than
n = 40, 40, 40.
PLoS Biology | www.plosbiology.orgFebruary 2005 | Volume 3 | Issue 2 | e33 0291
Indirect Benefits Outweigh Direct Costs
decrease or increase the costs associated with mating with
males. For instance, costs may be increased because females
are unable to escape male harassment, or they may be
decreased because there is no male–male competition.
Despite these limitations, we believe that our estimate of
the intrinsic rate of increase offers a reasonable approxima-
tion of net fitness.
The fitness estimate of choice in empirical studies may
depend on the importance of reproductive timing in the
system in question . Brommer et al.  compared
estimates of lifetime reproductive success and intrinsic rate
of increase to real long-term data from two species of bird.
They showed that lifetime reproductive success was a better
estimate of genetic contribution to future generations.
However, their estimates did not include measures of
offspring quality, and as they point out, their results may
depend on the species life history, and the generality of their
conclusions thus remains to be tested.
There are several reasons why reproducing early and
having short maturation times is likely to be advantageous in
crickets. First, extrinsic mortality of crickets in the wild is
likely to be high. Second, females become less choosy ,
lose condition, and produce fewer eggs as they age (M. L.
Head, unpublished data). Also, individuals with shorter
generation times will contribute their genes to future
generations more rapidly .
Our research constitutes one of the first attempts to
directly and simultaneously test the combined direct and
indirect effects of mating with males that differ in attractive-
ness. Only by following the effects of mating with attractive or
unattractive males through at least two generations, and
through both sons and daughters, is it possible to observe the
combined direct effects on female lifetime fecundity and the
genetic effects on offspring fitness [11,12,25]. Although the
need to conduct such a study under laboratory conditions
may constrain our ability to definitively answer this question,
our results suggest that indirect genetic benefits have the
potential to outweigh direct costs of mating with attractive
males. Moreover, this effect comes about largely, but not
exclusively, due to the production of more attractive sons.
Materials and Methods
Study species. We obtained approximately 1,000 final-instar A.
domesticus nymphs from a commercial cricket breeder (Pisces Enter-
prises, Phoenix, Arizona, United States). Nymphs were separated into
single-sex culture tubs (4 3 80 l containers per sex) to ensure their
virginity, and reared with constant access to food (Friskies Go-Cat
senior) and water until eclosion. At eclosion, adults were maintained
in single-sex cultures for a further 10 d to ensure sexual maturity.
In the cultures from which the insects have been derived, crickets
are raised in densities ranging from 23,000–34,000 m?3and fed grain
ad libitum. In these conditions males and females mate multiply.
Males fight with other males and court females, and there is a positive
relationship between male dominance and attractiveness .
Despite high densities, female cooperation is needed for mating to
occur because a female must actively mount the male and align her
genitalia with his to mate. Mate choice in both culture and wild
populations of A. domesticus is generally sequential. That is, females
choose males by either mating or rejecting males one at a time, rather
than choosing between males simultaneously. We chose to work on
cultured A. domesticus because our laboratory conditions closely
resemble the culture conditions under which they have recently
evolved. This similarity maximises the evolutionary relevance of our
measures. Our experimental design, however, requires that females
be kept alone, creating an important environmental difference from
the culture conditions to which females have been adapted.
Male attractiveness. The attractiveness trials throughout our
experiment were based on latency to mounting for pairs of crickets.
While this protocol does not allow all elements of female choice to be
measured, in A. domesticus a female mounting a male is a reliable
predictor of mating success (in a previous study 46 out of 50
mountings led to successful transfer of a spermatophore ). Also,
females have been shown to produce more eggs for males that they
choose quickly (M. L. Head, unpublished data). This indicates that
latency to mounting is representative of other aspects of choice in
To obtain males that were either attractive or unattractive to
females we ran a two-round tournament. In round one, each male was
placed in a clear plastic container (7 3 7 3 5 cm) with a single
randomly assigned female, at night, under red lighting. When a
female mounted a male, but before spermatophore transfer, they
were separated. Once half of the females had mounted, all remaining
pairs were separated. Round two commenced with a new female
assigned at random to each male. The first half of first-round
mounted males to be remounted became our ‘‘attractive’’ treatment
males. The half of first-round unmounted males that remained
unmounted longest in round two became the ‘‘unattractive’’ treat-
ment males. Only males that courted females during the tournament
were used. This biological assay of male attractiveness incorporates
all traits that make a male attractive during short-range courtship,
rather than a single trait correlated with attractiveness (see
Experimental design. Forty females were randomly assigned to
each of three treatments: attractive, unattractive, and an unmated
control. Females were weighed and placed individually in a small
plastic container (as above) with food, water, and a petri dish of moist
sand for egg laying. Males from the appropriate treatment were
randomly assigned to a female. Every 7 d, or whenever a male died, a
new male from the same treatment (but from a new tournament) was
placed with the female. This allowed us to measure the fitness
consequences of the strategy of mating with attractive or unattractive
males, rather than the consequences of mating with a given individual
male. Food, water, and sand were replaced every 7 d.
Fitness measures. Female survival was monitored daily, and the
number of eggs laid was counted weekly. Hatching success was
estimated as the proportion of eggs that hatched within 14 d of the
first egg hatching in each collection. Hatchlings were collected every
3 d, and their mean weight was recorded. Each week, 50 hatchlings
per female were separated into two boxes (20 3 13 3 13 cm), each
containing 25 nymphs. We monitored offspring survival every 7 d and
recorded the time to mature and sex and body weight at eclosion.
If a female had fewer than 50 hatchlings in a given week these were
discarded. For these females, the actual number of hatchlings was
multiplied by the overall experimental mean for each subsequent
offspring fitness measure, to predict the number of grandchildren
produced. This is a conservative approach to missing values because
it reduces the difference between the treatments.
Offspring generation times were calculated from the time females
were first placed with a male until the offspring matured. This takes
into account not only the time it takes for the offspring to mature,
but also the timing of egg laying. Mature offspring were housed
individually, and their survival monitored daily. Ten days after
eclosion each son’s attractiveness was estimated by placing him with a
stock virgin female in a small plastic container for 90 min. Mounted
males were separated from females before spermatophore transfer
occurred. We used the proportion of a female’s sons that were
successful in this assay as our measure of sons’ average attractiveness
(e.g., if 8 of 16 sons were mounted, we assumed that, on average, each
son had a 50% chance of mating per encounter with a female).
Ten days after eclosion daughters were placed with a stock male
for 12 h to allow mating. Afterwards, survival of sons and daughters
was again monitored daily, and sand was collected from daughters
weekly. Eggs from daughters were counted to estimate lifetime
Statistical analysis. We calculated two estimates of female relative
net fitness when mating with either an attractive or unattractive male.
A rate-insensitive estimate, the relative number of grandchildren
produced by a female (gest), and a rate-sensitive estimate, rest.
To estimate the absolute number of grandchildren each female
had (Gest), we added the number of grandchildren she had through
daughters, estimated as
Gdaughters¼ ndaughters? fecunditydaughters
to the number she had through sons, Gsons, estimated as
PLoS Biology | www.plosbiology.orgFebruary 2005 | Volume 3 | Issue 2 | e33 0292
Indirect Benefits Outweigh Direct Costs
Gsons¼ nsons? attractivenesssons? longevitysons? c:
The attractiveness of a female’s sons was estimated as the proportion
of her sons that were mounted in attractiveness trials; longevity is the
mean adult life span of a female’s sons and c is the ratio of the total
number of grandchildren through daughters in the experiment to the
total number of sons mounted in the attractiveness trials. This
correction factor converts an attractiveness score into units of the
number of grandchildren. Using this correction factor ensured that
mean son and daughter reproductive success across the entire
experiment was equal, satisfying the assumption that mean repro-
ductive success for males and females is the same in populations with
an equal sex ratio .
Gestfor each female was then divided by the experimental mean to
give the relative gest.
We estimated the absolute intrinsic rate of increase for each
where t is the generation time from parental first mating to offspring
maturity in a particular lineage. We converted our rate-sensitive
measure into a measure of relative intrinsic rate of increase (rest), by
dividing each female’s Restby the experiment-wide mean.
Due to the non-normal distributions of many fitness components,
we tested the significance of treatment differences for each fitness
component using two-tailed randomisation tests. In each random-
isation test the observed data was randomly assigned to the two
treatments 10,000 times. P-values are based on the proportion of
randomisations in which the absolute value of the estimated
difference was greater than that observed in the original data.
To explore the sensitivity of our estimates of restto variation in
each fitness component we used a model-building approach. We
removed the variance of each fitness component from our full model,
in turn, by assigning every female the overall experimental mean
value of that component. We similarly excluded every combination of
two fitness components. We then ran a randomization test (as above,
10,000 randomizations) for each reduced model to test whether the
treatment effect remained. We also obtained 10,000 jackknifed
estimates of the difference between the treatments for each reduced
model (by randomly omitting 20% of the sample in each estimate), to
test whether the reduced model resulted in a significantly different
effect size than the original full model. P-values are based on the
proportion of jackknifed estimates in which the absolute value of the
difference between the treatments was greater than the absolute
difference in the full model.
We used principal components analysis to investigate the effects of
mating with attractive or unattractive males on week 1 reproductive
effort via egg number, egg width, and egg length. All three measures
showed a strong positive loading on the first principal component,
which explained 66% of the variation in the constituent measures.
We then tested for differences in female reproductive effort between
the treatments using a randomisation test.
We thank L. Bussie `re, J. Kelley, K. Savage, J. Evans, S. Griffith, H.
Kokko, A. Lindholm, K. Monro, S. Zajitschek, F. Zajitschek, and M.
Blows for valuable discussion and comments on the manuscript. This
research was funded by an ARC grant to JH, RB, and MDJ, and an
Australian Postgraduate Award to MLH.
Competing interests. The authors have declared that no competing
Author contributions. MLH, JH, and RB conceived and designed
the experiments. MLH and JH performed the experiments. MLH,
MDJ, and RB analyzed the data. JH and RB contributed reagents/
materials/analysis tools. MLH, JH, MDJ, and RB wrote the paper.
1. Houle D, Kondrashov AS (2002) Coevolution of costly mate choice and
condition-dependent display of good genes. Proc R Soc Lond B Biol Sci
2. Kirkpatrick M (1996) Good genes and direct selection in the evolution of
mating preferences. Evolution 50: 2125–2140.
3. Kirkpatrick M, Barton NH (1997) The strength of indirect selection on
female mating preferences. Proc Natl Acad Sci U S A 94: 1282–1286.
4. Kokko H, Brooks R, McNamara JM, Houston AI (2002) The sexual selection
continuum. Proc R Soc Lond B Biol Sci 269: 1331–1340.
5.Cameron E, Day T, Rowe L (2003) Sexual conflict and indirect benefits. J
Evol Biol 16: 1055–1060.
6.Weatherhead PJ, Robertson RJ (1979) Offspring quality and the polygyny
threshold: ‘‘The sexy son hypothesis.’’ Am Nat 113: 201–208.
7.Kirkpatrick M (1985) Evolution of female choice and male parental
investment in polygynous species: The demise of the ‘‘sexy son.’’ Am Nat
8.Pomiankowski A, Iwasa Y, Nee S (1991) The evolution of costly mate
preferences I. Fisher and biased mutation. Evolution 45: 1422–1430.
9. Kirkpatrick M (1987) Sexual selection by female choice in polygynous
animals. Annu Rev Ecol Syst 18: 43–70.
10. Boake CRB (1985) Genetic consequences of mate choice: A quantitative
genetic method for testing sexual selection theory. Science 227: 1061–1063.
11. Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate
choice and mating biases. Proc R Soc Lond B Biol Sci 270: 653–664.
12. Fedorka KM, Mousseau TA (2004) Female mating bias results in conflicting
sex-specific offspring fitness. Nature 429: 65–67.
13. Alatalo RV, Lundberg A, Glynn C (1986) Female pied flycatchers choose
territory quality and not male characteristics. Nature 323: 152–153.
14. Calsbeek R, Sinervo B (2002) Uncoupling direct and indirect components
of female choice in the wild. Proc Natl Acad Sci U S A 99: 14897–14902.
15. Petrie M (1994) Improved growth and survival of offspring of peacocks with
more elaborate trains. Nature 371: 598–599.
16. Reynolds JD, Gross MR (1992) Female mate preference enhances offspring
growth and reproduction in a fish, Poecilia reticulata. Proc R Soc Lond B Biol
Sci 250: 57–62.
17. Welch AM, Semlitsch RD, Gerhardt HC (1998) Call duration as an indicator
of genetic quality in male gray tree frogs. Science 280: 1928–1930.
18. Hine E, Lachish S, Higgie M, Blows MW (2002) Positive genetic correlation
between female preference and offspring fitness. Proc R Soc Lond B Biol
Sci 692: 2215–2219.
19. Jones TM, Quinnell RJ, Balmford A (1998) Fisherian flies: Benefits of female
choice in a lekking sandfly. Proc R Soc Lond B Biol Sci 265: 1651–1657.
20. Brooks R (2000) Negative genetic correlation between male sexual
attractiveness and survival. Nature 406: 67–70.
21. Pitnick S, Garcı ´a-Gonza ´lez F (2002) Harm to females increases with male
body size in Drosophila melanogaster. Proc R Soc Lond B Biol Sci 269: 1821–
22. Friberg U, Arnqvist G (2003) Fitness effects of female mate choice:
Preferred males are detrimental for Drosophila melanogaster females. J Evol
Biol 16: 797–811.
23. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential
testosterone investment in zebra finch eggs. Science 286: 126–128.
24. Cunningham EJ, Russell AF (2000) Egg investment is influenced by male
attractiveness in the mallard. Nature 404: 74–77.
25. Pizzari T, Snook RR (2003) Sexual conflict and sexual selection: Chasing
away paradigm shifts. Evolution 57: 1223–1236.
26. Chippindale AK, Gibson JR, Rice WR (2001) Negative genetic correlation
for adult fitness between sexes reveals ontogenetic conflict in Drosophila.
Proc Natl Acad Sci U S A 98: 1671–1675.
27. Brommer JE, Gustafsson L, Pietiainen H, Merila ¨ J (2004) Single-generation
estimates of individual fitness as proxies for long-term genetic contribu-
tion. Am Nat 163: 505–517.
28. Brommer JE, Merila ¨ J, Kokko H (2002) Reproductive timing and individual
fitness. Ecol Lett 5: 802–810.
29. Pomiankowski A (1987) The costs of choice in sexual selection. J Theor Biol
30. Clutton-Brock TH, Langley P (1997) Persistent courtship reduces male and
female longevity in captive tsetse flies Glossina morsitans morsitans Westwood
(Diptera: Glossinidae). Behav Ecol 8: 392–395.
31. Rowe L, Arnqvist G (2002) Sexually antagonistic coevolution in a mating
system: Combining experimental and comparative approaches to address
evolutionary processes. Evolution 56: 754–767.
32. Fowler K, Partridge L (1989) A cost of mating in female fruitflies. Nature
33. Crudgington H, Siva-Jothy MT (2000) Genital damage, kicking and early
death. Nature 407: 855–858.
34. Sheldon BC (2000) Differential allocation: Tests, mechanisms and implica-
tions. Trends Ecol Evol 15: 397–401.
35. Rice WR (2000) Dangerous liaisons. Proc Natl Acad Sci U S A 97: 12935–
36. Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of
mating in Drosophila melanogaster is mediated by male accessory gland
products. Nature 373: 241–244.
37. Herndon LA, Wolfner MF (1995) A drosophila seminal fluid protein,
ACP26Aa, stimulates egg laying in females for 1 day after mating. Proc Natl
Acad Sci U S A 92: 10114–10118.
38. Kalb JM, DiBenedetto AJ, Wolfner MF (1993) Probing the function of
Drosophila melanogaster accessory glands by directed cell ablation. Proc Natl
Acad Sci U S A 90: 8093–8097.
PLoS Biology | www.plosbiology.orgFebruary 2005 | Volume 3 | Issue 2 | e330293
Indirect Benefits Outweigh Direct Costs
39. Murtaugh MP, Denlinger DL (1987) Regulation of long-term oviposition in Download full-text
the house cricket, Achaeta domesticus: Roles of prostoglandin and factors
associated with sperm. Arch Insect Biochem Physiol 6: 59–72.
40. Burley N (1988) The differential-allocation hypothesis: An experimental
test. Am Nat 132: 611–628.
41. Norris KJ (1993) Heritable variation in a plumage indictor of viability in
male great tits Parus major. Nature 362: 537–539.
42. Moore AJ (1994) Genetic evidence for the ‘‘good genes’’ process of sexual
selection. Behav Ecol Sociobiol 35: 235–241.
43. Etges WJ (1996) Sexual selection operating in a wild population of
Drosophila robusta. Evolution 50: 2095–2100.
44. Wedell N, Tregenza T (1999) Successful fathers sire successful sons.
Evolution 53: 620–625.
45. Heisler IL (1985) Quantitative genetic models of female choice based on
‘‘arbitrary’’ male characters. Heredity 55: 187–198.
46. Shackleton M, Jennions MD, Hunt J (2005) Dominance and attractiveness as
predictors of male mating success in the black field cricket Teleogryllus
commudus: The effectiveness of no-choice tests. Behav Ecol Sociobiol. In
47. Kotiaho JS, Simmons LW, Hunt J, Tomkins JL (2003) Males influence
maternal effects that promote sexual selection: A quantitative genetic
experiment with dung beetles Onthophagus taurus. Am Nat 161: 852–859.
48. Gray DA (1997) Female crickets, Acheta domesticus, prefer the chirps of larger
males. Anim Behav 54: 1553–1562.
49. Savage KE, Hunt J, Jennions MD, Brooks R (2005) Male attractiveness is
positively associated with fighting ability but not confidence in the house
cricket Achaeta domesticus. Behav Ecol. In press.
50. Gray DA (1999) Intrinsic factors affecting female choice in house crickets:
Time costs, female age, nutritional condition, body size and size-relative
reproductive investment. J Insect Behav 12: 691–700.
51. Cooch EG, Cam E, Link W (2002) Occam’s shadow: Levels of analysis in
evolutionary ecology—Where to next? J Appl Stat 29: 19–48.
52. Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton (New
Jersey): Princeton University Press. 533 p.
PLoS Biology | www.plosbiology.org February 2005 | Volume 3 | Issue 2 | e330294
Indirect Benefits Outweigh Direct Costs