Full text of DOI:10.1111/j.0014-3820.2000.tb01259.x

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Corresponding Editor: K. Ross
Evolution, 54(6), 2000, pp. 2161–2165
COPULATING WITH MULTIPLE MATES ENHANCES FEMALE FECUNDITY BUT NOT
EGG-TO-ADULT SURVIVAL IN THE BRUCHID BEETLE
CALLOSOBRUCHUS MACULATUS
P
AUL E. EADY,1 NINA
WILSON, AND MARC JACKSON
Ecology Centre, University of Sunderland, Sunderland, SR1 3SD, United Kingdom
1
E-mail: paul.eady@sunderland.ac.uk
Abstract. Postcopulatory sexual selection theory has come a long way since the evolutionary implications of sperm
competition were first spelled out by Parker (1970). However, one of the most enduring questions remains: why do
females copulate with multiple males? Here we show that females copulating with multiple males lay more eggs than
those copulating repeatedly with the same male. We also show egg-to-adult survival to be more variable when females
copulate multiply with different males and less variable when they copulate multiply with the same male. This supports
the notion that egg-to-adult survival may depend on the genetic compatibility of males and females. However, pre-
adult survival was highest when females copulated repeatedly with the same male rather than with different males.
Thus, it would appear that polyandry in this species does not function to reduce the risk of embryo failure resulting
from fertilization by genetically incompatible sperm.
Key words. Callosobruchus maculatus, fecundity, genetic compatibility, polyandry.
Received February 16, 2000. Accepted May 18, 2000.
The recognition that copulation has costs (Keller and Reeve tion (Bateman 1948), female reproductive benefits are much
995) and that females frequently copulate with more than less obvious.
1
one male (Smith 1984; Birkhead and Møller 1998), requires
The possible benefits to females from copulating with mul-
that the function of polyandry be addressed. Whereas male tiple males fall into two broad categories: direct and indirect
reproductive success increases with each additional copula- fitness benefits. Direct benefits include fertility insurance

2
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BRIEF COMMUNICATIONS
(
Walker 1980), male parental care (Davies 1992), courtship
feeding (Thornhill and Alcock 1983), ejaculatory nutrients
Gwynne 1984), and the avoidance of infanticide (Hrdy
977). The indirect benefits include genetic diversity (Keller
and Reeve 1994), genetic compatibility (Zeh and Zeh 1996,
997), offspring viability (Olsson et al. 1994), offspring at-
Multiple Mates, Fecundity, and Offspring Survival
Twenty four hours ( 2 h) after emergence virgin females
were permitted a single copulation with 24 h ( 2 h) old virgin
males. The females were then placed in individual 25 cm
pots containing 20 black-eyed-beans and allowed to oviposit
for 48 h before being remated to either the same male or a
different male which had previously been mated once. This
controls for the potentially confounding effect of male mating
Ϯ
(
1
Ϯ
3
1
tractiveness (Kempenaers et al. 1992), and sperm fertilization
efficiency (Keller and Reeve 1995). That any one function
has universal application is unlikely due to the vast array of history. Following the second copulation females were con-
organismal life histories. However, empirical study of poly- fined to individual pots containing 15 fresh black-eyed beans
andry and its effects on female fitness will enable us to iden- on which to oviposit for a further 48 h before being remated
tify underlying patterns in its evolution.
to either the same male or a different third male, previously
Here we report on the results of two experiments designed mated twice. Following the third copulation the females were
to examine the benefits of multiple copulations with different allowed to oviposit until their natural deaths on 20 fresh
black-eyed beans. In all cases intromission was observed
Rup 1986). Elytron length, measured using an eye piece
males in the seed beetle Callosobruchus maculatus (Cole-
optera: Bruchidae), a cosmopolitan pest species of stored
legumes (Giga and Smith 1991). Under laboratory conditions
females of many strains are known to copulate with multiple
males with intercopulatory intervals of around 1–3 days
(
graticule fitted to a microscope, was recorded for all females
as this correlates well with emergence weight (Wilson and
Hill 1989). Female fecundity and egg-to-adult survival were
determined following the first, second and third copulations.
Egg-to-adult survival was thus determined over three clutches
for each female, enabling intraclass correlation coefficients
to be determined (Sokal and Rohlf 1981).
(
1
Credland and Wright 1989; Eady 1991; Fox 1993a; Ofuya
995; Wilson et al. 1997). Similar patterns have been reported
in other bruchid species (Huignard 1974; Boucher and Huig-
nard 1987; Wilson et al. 1999; Mbata et al. 1997). Thus, it
is likely that polyandry is a common feature of the natural
history of C. maculatus. Under conditions of sperm compe-
tition the last male to mate fertilizes approximately 80% of
the ova, although there is considerable variation about this
mean value (Eady and Tubman 1996) and females have been
shown to exert considerable influence over patterns of sperm
usage (Wilson et al. 1997). This last point is important be-
cause the hypothesis that polyandry functions to reduce the
risk of embryo failure, resulting from fertilization by genet-
ically incompatible sperm, rests on the assumption that fe-
males are capable of biasing fertilization in favor of com-
patible sperm types (Zeh and Zeh 1996, 1997).
Multiple Mates and Offspring Survival under Intense Larval
Competition
Because the effects of polyandry on offspring viability
might be detected under nonbenign conditions only, we re-
peated the above experiment with the important difference
that following the first and second copulations females were
allowed to oviposit on 10 fresh beans and following the third
copulation, females were confined to individual pots con-
taining 20 beans, which had been previously oviposited on
by different females. Therefore, upon hatching, the larvae of
the experimental females faced intense larval competition for
resources. This design was created to induce nonbenign con-
ditions for the developing larvae following the third copu-
lation. The initial oviposition was performed by black-morph
females derived from a Brazilian strain. On average these
In C. maculatus the ejaculate serves both a nutritional and
stimulatory role in females (Fox 1993a,b; Wilson et al. 1999);
thus by mating multiply females derive direct benefits. How-
ever, what has not been tested before is how polyandry (cop- females laid eight eggs per bean. Offspring from black morph
ulating with multiple males), as opposed to multiple copu- females are entirely black (Eady 1991) and can be distin-
lation per se, influences female fitness. To test this we com- guished from Niamey beetles as these are never entirely black
pared the fecundity (number of eggs laid) and offspring in our cultures. Thus, the survival of Niamey offspring could
survival of females that had copulated multiply with either be determined under conditions of intense larval competition.
Following the third copulation, fecundity, egg-to-adult sur-
vival, and mean offspring size were recorded. Fecundity of
Niamey females was determined by counting the total number
of eggs laid by black females, then recounting the eggs laid
after the Niamey females had oviposited, with the difference
between the two totals representing the fecundity of Niamey
females. Offspring size was determined by measuring the
lengths of elytra from five female offspring. Female offspring
were measured as size is a good predictor of fecundity (Fox
the same or different males. In these experiments we control
both the number of copulations and male copulatory history.
This is necessary as both copulation number and male mating
history have been shown to influence female fecundity in this
species (Savalli and Fox 1999; Wilson et al. 1999).
M
ETHODS
The beetles used in these experiments were derived from
a population in Niamey, Niger, which has been in culture at
the University of Sunderland for approximately three years
1
993a).
R
ESULTS
(
for culture details, see Wilson et al. 1997). Stock cultures
Multiple Mates, Fecundity and Offspring Survival
of C. maculatus were maintained on cowpeas (black-eyed
beans) Vigna unguiculata (L.), in a constant environment at
The proportion of females that remated to the same (30
2
6
Њ
C
Ϯ
1
Њ
C and 35% rh with a 16L:8D photoperiod.
out of 40) or different male (35 out of 40) was statistically

BRIEF COMMUNICATIONS
2163
T
ABLE 1. Fecundity and egg-to-adult survival following each copulation in the single male and multiple male treatments. Means Ϯ SE, values
in parentheses are sample sizes.
Treatment
Following 1st copulation
Following 2nd copulation
Following 3rd copulation
Same male:
Fecundity
Egg-to-adult survival (%)
40.22 Ϯ 1.3 (40)
85 Ϯ 0.017 (40)
29.20 Ϯ 0.62 (30)
91 Ϯ 0.015 (30)
32.63 Ϯ 1.7 (27)
86 Ϯ 0.019 (27)
Different male:
Fecundity
Egg-to-adult survival (%)
40.03 Ϯ 1.1 (40)
83 Ϯ 0.017 (40)
30.86 Ϯ 0.69 (35)
89 Ϯ 0.014 (35)
32.90 Ϯ 2.0 (34)
77 Ϯ 0.036 (34)
equivalent (G-test
length was equivalent between the treatments (t
57, P 0.12). The mean number of eggs laid by females bility, then egg-to-adult survival should be less variable
ϭ
2.08, df
ϭ
1, P
ϭ
ns). Female elytra
ϭ
0.1; treatment F1,58
ϭ 7.07, P Ͻ 0.01). If egg-to-adult
ϭ
1.56, df survival is attributable, at least in part, to genetic compati-
ϭ
ϭ
in each treatment and the percentage of these eggs giving across the three clutches when females mated multiply to the
rise to adult offspring are shown in Table 1. Although it same male, compared to those mated to different males. This
would appear that fecundity is equivalent between treatments, was the case; when females were inseminated by the same
female elytron length explains a significant amount of var- male the coefficient of intraclass correlation was rI
iation in fecundity. Thus, the data were analyzed using an F30,57 2.0, P 0.012 and, when females were inseminated
0.07, F34,68 1.23, P 0.233).
ϭ 0.25,
ϭ
ϭ
analysis of covariance, using elytron length as the covariate. by different males rI
ϭ
ϭ
ϭ
When analysed this way there was a significant effect of
female size (F1,58
(
ϭ
11.99, P
Ͻ 0.001) but not treatment
Multiple Mates and Offspring Survival under Intense Larval
Competition
F1,58 ϭ 3.47, P ϭ 0.068) on female lifetime fecundity. How-
ever, if fecundity was analyzed following the second and third
copulations, which is when the effects of treatment are ex-
pected to show themselves, it was found that females cop-
ulating with multiple males laid more eggs than those cop-
Female body size was equivalent across the two treatments
(
t
ϭ
0.95, df
laid on beans by black morph females prior to the experiment
1.79, df 38, P 0.081). Following the third copulation
there was no relationship between female body size and fe-
ϭ 45, P ϭ 0.35) as was the number of eggs
(
t
ϭ
ϭ
ϭ
ulating with the same male (ANCOVA female size F1,58
ϭ
2
1
0.62, P
Ͻ 0.0001; treatment F1,58 ϭ 5.85, P Ͻ 0.02; Fig.
cundity (r
0.23, df
ϭ
ϭ
0.21, df
47, P
0.004, df
ϭ
47, P
Ͼ 0.05), offspring number (r
). An analysis of covariance on arcsine transformed survival
ϭ
Ͼ 0.05), offspring survival (arcsine trans-
data, with initial egg density the covariate, revealed egg-to-
adult survival to be equivalent between treatments following
formed data r
ϭ
ϭ
47, P
0.05). Treatment had no de-
46, P
33.2
3.1), egg-
to-adult survival (mean survival when mated to the same male
29.3% 0.043, and different males 25.1% 0.024;
ANCOVA on arcsine transformed survival data, initial egg
density F1,46 1.27, P 0.26; treatment F1,46 1.04, P
.31), nor offspring size (t 0.17, df 32, P 0.86; elytron
length of offspring from females mated to the same male
.75 0.025 mm, and different males 1.74 0.027 mm).
Ͼ 0.05), or mean offspring
size (r 0.14, df
ϭ
ϭ
47, P Ͼ
the first copulation (egg density F1,77
treatment F1,77 0.18, P 0.64) and the second copulation
9.07, P 0.04; treatment F1,62 0.46,
0.5), but significantly higher in the single male treatment,
2.61, P
ϭ 27.19, P Ͻ 0.001;
tectable effect on female fecundity (t ϭ Ϫ1.22, df
0.23; fecundity when mated to the same male
.3, and when mated to different males 38.7
ϭ
ϭ
ϭ
ϭ
3
ϭ
Ϯ
(
egg density F1,62
ϭ
ϭ
ϭ
ϭ
Ϯ
P
ϭ
following the third copulation (egg density F1,58
ϭ
ϭ
Ϯ
ϭ
Ϯ
ϭ
ϭ
ϭ
ϭ
0
ϭ
ϭ
ϭ
ϭ
1
Ϯ
ϭ
Ϯ
Thus, there is no evidence to suggest that female fitness is
enhanced by mating with multiple males when offspring ex-
perience intense larval competition.
D
ISCUSSION
We have shown that by copulating with multiple males,
female C. maculatus lay more eggs than by copulating with
a single male, under laboratory conditions. This raises two
important questions. What is the mechanism? Does it serve
an important functional role?
With respect to mechanism, it is possible that between-
F
IG. 1. The effect of polyandry on female fecundity following the
second and third copulations combined. Open circles, females cop- male variation in the composition of ejaculate-derived ovi-
ulating with the same male (lower line; fecundity ϭϪ76.7
elytron length; F1,25 10.6, P 0.003); closed circles, females
copulating with multiple males (upper line; fecundity ϭϪ92.5
1.8 elytron length; F1,30 9.41, P 0.005). Lines fitted by least-
squares linear regression.
ϩ 61.8
positional stimulants produces a synergistic egg laying re-
sponse in females. Central to this argument is the existence
of intraspecific variation in male seminal products and evi-
dence that females respond to multiple chemical cues. Such
ϭ
ϭ
ϩ
7
ϭ
ϭ

2
164
BRIEF COMMUNICATIONS
variation has been found in the accessory gland proteins of Newcomer et al. (1999) would indicate this not to be the
Drosophila (Whalen and Wilson 1986, Cooke et al. 1987) case.
and in a number of species, multiple chemical cues derived
Mechanisms of post copulatory sexual selection. In Cor-
from ejaculates, stimulate oviposition (Eberhard 1996). Syn- dylochernes scorpioides and Gryllus bimaculatus, in which
ergistic effects of accessory compounds could be evoked to there appears to be genetic benefits of polyandry (Zeh 1997;
explain the results of Leahy (1973, cit. Eberhard 1996) who Tregenza and Wedell 1998), sperm mixing rather than last-
found that female grasshoppers, Schistocerca gregaria, im- male sperm precedence occurs (Simmons 1987; Zeh and Zeh
planted with the accessory glands of single males laid fewer 1994). Thus, in these species there is ample opportunity for
eggs than females implanted with the accessory glands of postcopulatory female choice of sperm types. This is im-
multiple males.
portant because the genetic incompatibility hypothesis rests
Unfortunately, control over dose in such experiments is on the foundation that females are capable of biasing fertil-
ization in favour of compatible sperm types (Zeh and Zeh
996, 1997). It could be argued that because there is last-
0.8; Eady 1991;
Eady and Tubman 1996), there is little opportunity for fe-
males to bias fertilization in favour of particular sperm types.
Thus, we might expect genetic benefits of multiple mates to
be absent in this or other species with last-male sperm pre-
cedence. The problem with such an argument is that there is
not possible. An alternative explanation for the enhanced
fecundity of polyandrous females is that males inseminate
less ejaculatory material on encountering the same female.
Against this argument is that if males could identify previous
sexual partners, then selection would favor early (precopu-
lation) rather than late (postintromission) recognition, so as
to avoid costly reinseminations (Bateman 1948). The fact that
males do copulate with the same sexual partner would suggest
that they are incapable of recognizing previous sexual part-
ners.
That females inseminated by multiple males laid more eggs
implies a function to polyandry. However, a male encoun-
tering the same female, in a receptive state, either in nature
or under culture conditions is, in our opinion, likely to be a
rare event. Thus, chance dictates that females usually remate
with different sexual partners and in C. maculatus females
remate in order to derive direct benefits from males (Fox
1
male sperm precedence in C. maculatus (P2
ϳ
a continuum of P values between zero and one, with sperm
2
selection theoretically possible when P2
Ͼ 0 and Ͻ1. In ad-
dition, females have been shown to exert considerable post-
copulatory influence over male fertilization success in C. ma-
culatus (Wilson et al. 1997), despite strong last-male sperm
precedence.
Statistical power. It is possible that our experiments were
not sufficiently powerful to detect real, but small differences
in offspring performance, between treatments. We discount
this because in both experiments egg-to-adult survival was
greatest (although not statistically significant in the second
experiment) when females copulated multiply with a single
male. Thus, it is unlikely that we would have found enhanced
offspring survival following polyandry, by increasing our
sample sizes.
1
993a; Wilson et al. 1999). This fits with the observation
that females were equally likely to remate with the same male
or a different male, although discrimination against previous
mates has been shown to be time dependent in Cordyloch-
ernes scorpioides (Zeh et al. 1998) and Dermestes maculatus
(
Archer and Elgar 1999).
Quite why polyandrous females had reduced egg-to-adult
survival remains unclear. One possibility is that seminal fluid
incapacitates nonself resident sperm lowering fertilization ef-
ficacy (Prout and Clark 2000). Another possibility is that
toxic seminal compounds (Das et al. 1980, Chapman et al.
Hypothesized genetic benefits of polyandry are many (Kel-
ler and Reeve 1995). Therefore, failure to detect one potential
benefit should not rule out the operation of others. In relation
to offspring survival, we found no evidence of indirect ben-
efits of polyandry. In fact we found the opposite; females
inseminated by multiple males had lower egg-to-adult sur-
vival. This contrasts with Madsen et al. (1992), Olsson et al.
1
995) act synergistically on females and/or their offspring
reducing egg hatch/survival, or the synergistic effects of male
accessory gland products over-stimulate oviposition resulting
in the production of immature and hence less viable eggs.
Each of these scenarios bear the hallmarks of sexual conflict,
the resolution of which is difficult to predict (Parker 1984),
which may be another explanation as to why different patterns
are found in different taxa.
(
1994); Zeh (1997), and Tregenza and Wedell (1998), in
which female promiscuity was found to increase offspring
viability. This discrepancy may be due to a number of rea-
sons:
Generality. The lack of concordance between results may
simply reflect the nonuniversal nature of the response.
Experimental design. The studies of Madsen et al. (1992)
and Olsson et al. (1994) were field based. Thus, confounding
variables could have led to an association between female
promiscuity and offspring viability (Parker 1992). Also, DNA
fingerprinting of offspring does not track exact female mating
history, thus the number of sexual partners could be under-
estimated. In addition, the studies of Madsen et al. (1992)
and Olsson et al. (1994) were conducted on small isolated
populations with low genetic variability. Therefore, promis-
cuous copulation may be a mechanism to avoid inbreeding
in inbred populations only, with the benefits of promiscuity
disappearing in outbred populations, although Zeh (1997) and
A
CKNOWLEDGMENTS
We are very grateful to M. Clephane for helping to count
eggs and to A. Cherrill, W. Arthur, S. Tubman, K. Ross, and
D. Zeh for constructive criticisms of the manuscript. Many
thanks to P. Credland for supplying the Niamey strain.
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Corresponding Editor: K. Ross