Behavioral Ecology Vol. 10 No. 5: 567–571
Delayed oviposition: a female strategy to
counter infanticide by males?
Jutta M. Schneider
Mitrani Center for Desert Ecology, Jacob Blaustein Institute for Desert Research, Ben Gurion
University of the Negev, Sede Boqer 84990, Israel, and Max-Planck-Institut für Verhaltensphysiologie,
D-82319 Starnberg Seewiesen, Germany
Conflicts of interest between males and females can lead to an evolutionary arms race in which adaptations of each sex coevolve.
Intersexual conflict is extreme in the brood caring, semelparous spider Stegodyphus lineatus ; males encountering females that
have already produced their usually single egg sac attempt to remove and discard the egg sac and then remate with the female.
Females that cannot defend their eggs lose valuable time and fecundity by having to replace the clutch. Selection should favor
females that complete their suicidal maternal care as quickly as possible because of the high risk of predation. However, some
females take up to four times longer to oviposit than others. I propose that females minimize the risk of male infanticide by
postponing oviposition. Accordingly, early-maturing females, who suffer the highest risk of infanticide by males, should have a
longer interval between maturation and oviposition than late-maturing females. The date of maturation significantly predicted
the interval between maturation and oviposition and explained up to 35% of its variation in a data set from a natural population
and longer term data from a seminatural, enclosed population. Body size was predicted to have a weak effect on the timing of
oviposition and was consistently less important than maturation date. The observed facultative timing of oviposition may have
evolved as a result of intersexual conflict over mating. Key words: life-history strategy, mating system, sexual conflict, spider,
Stegodyphus. [Behav Ecol 10:567–571 (1999)]
T
he reproductive interests of males and females are not
necessarily the same, even though the sexes have to cooperate to produce common offspring. In extreme cases,
males may attempt to mate with unreceptive females (CluttonBrock and Parker, 1995), and females may vigorously protect
themselves against male force or evolve strategies to avoid
male harassment (e.g., Arnqvist and Rowe, 1995; Grinnell and
McComb, 1996). Where the mating strategy of males imposes
a high cost on females, sexual conflict theory predicts that
selection will favor the evolution of female counter strategies
that minimize their cost (Parker, 1979).
In many animals, females store sperm and thereby separate
insemination and fertilization (Alexander et al., 1997; Birkhead and Møller, 1993; Eberhard, 1985). By separating insemination and fertilization in both space and time, males may
not only lose control over which sperm the female will use to
fertilize her eggs, but also lose control over the timing of oviposition. In insects and spiders, females may enhance their
control over fertilization by morphological structures such as
spermathecae (Eberhard, 1985, 1996) or abdominal spines in
water striders (Arnquist and Rowe, 1995), which suggests that
these structures evolved as female strategies in the conflict
between the sexes. Adjusting the timing of oviposition would
allow females that may fall victim to costly male mating strategies to alter the cost–benefit equation for a specific male
behavior such as mate guarding or infanticide. If a male cannot discern when a female will oviposit, the lost opportunity
costs associated with mate guarding become unpredictable.
Plasticity in the timing of oviposition may have evolved as a
result of intersexual conflict.
J. M. Schneider is currently at the Department of Population Biology, Zoological Institute, Johannes Gutenberg University Mainz, PO
Box 3980, D-55099 Mainz, Germany. E-mail: JuttapSchneider@
t-online.de.
Received 29 June 1998; revised 31 January 1999; accepted 15 February 1999.
q 1999 International Society for Behavioral Ecology
I tested predictions derived from this idea using the eresid
spider Stegodyphus lineatus as a model species. Male and female S. lineatus actively fight each other when their interests
conflict, and each sex has a chance to win the contest (Schneider and Lubin, 1996, 1997b). S. lineatus is an annual, semelparous spider found in arid and semiarid habitats around the
Mediterranean basin (Kraus and Kraus, 1990; Ward and Lubin, 1993). Both sexes build silken tubelike nests. Males mature in their nests and then leave them permanently to search
for females. The mating season begins in early spring
(March/April) and lasts about 4 months (Schneider, 1997).
The first egg sacs appear in April and the last as late as July
(Schneider and Lubin, 1997a). Spiderlings cannot leave the
egg sac without the help of their mother. Females guard their
single egg sac and will only produce a second clutch if the
first one is lost. After 30 days of egg development, the female
opens the egg sac to release the young, feeds them with a
liquid regurgitate (Kullmann et al., 1971), and is typically consumed by the spiderlings within a period of 14 days (Schneider, 1995).
The distribution of maturation dates of males and females
overlap broadly over a period of 80 days (Schneider, 1997),
with the first male maturing about 20 days before the first
female. Males can expect an adult life of 2–3 weeks, and the
number of males active during the mating season drops quickly. Although females usually lay eggs about 30 days after maturation, some males still search for females when up to 50%
of the females have already produced eggs (Schneider and
Lubin, 1996). The suicidal maternal care of S. lineatus means
that males encountering females with eggs cannot expect to
sire common offspring unless they force the females to re-lay.
Males can discard the egg sac fathered by an earlier male if
they win the fight with the female. The female then remates
with the infanticidal male and uses his sperm to fertilize part
of the replacement clutch (paternity of the infanticidal male
is around 50%; Schneider and Lubin, 1996). Females suffer a
constant, daily risk of predation (Schneider, 1996a), so the
additional time associated with the male infanticide translates
Behavioral Ecology Vol. 10 No. 5
568
directly to mortality costs. In addition, the size of the replacement clutch is significantly smaller. Females defend their eggs
against males because they pay a high cost if they lose them.
The combination of suicidal maternal brood care and male
infanticidal behavior produces a clear case of intersexual conflict with varying solutions.
Female S. lineatus that lose their clutch through male infanticide replace it significantly later than females that lose
their eggs from predation or fungus infestation (Schneider
and Lubin, 1997b). A delay in egg sac replacement may reduce the risk of further potentially infanticidal encounters
with males. Facultative timing of egg production may be a
female counterstrategy against egg removal by males, and, if
so, the timing of laying the first clutch should be a function
of the probability of infanticide.
The risk of infanticide is not the same for all females. Males
disappear from the population about 2 weeks after the first
females produce egg sacs (Schneider and Lubin, 1996).
Therefore, females that reproduce early in the season suffer
a higher risk of encountering infanticidal males (8% of the
females lose their clutch due to males). The difference in
prosoma (cephalothorax) width between the opponents decides the outcome of the conflict (Schneider and Lubin,
1997b). Consequently, large females suffer a lower risk of egg
loss due to infanticidal males than small females. However,
large body size of females becomes important only after a
male encounter has begun; it does not prevent conflict, and
even large females suffer a risk of injury in a fight (Schneider
and Lubin, 1997b).
I investigated whether females adjust the timing of oviposition to the risk of infanticide by males. I used data from a
field population and from 2 years of a captive population under seminatural conditions to examine whether females that
mature early in the season have a longer interval between
maturation and oviposition.
METHODS
Field population
Data on the timing of maturation and oviposition in S. lineatus were collected in March and April, 1991 on the Greek
island of Karpathos. Nests of subadult spiders were marked in
February and checked daily. At the days of molting and oviposition, prosoma width and total body length were measured
to the closest 0.1 mm (Schneider, 1997). A condition index
was calculated by dividing the body length by the width of the
prosoma (the latter is a hard structure that does not change
after maturation). Although not perfect, body length provides
an adequate indicator for body mass (r 5 .83, n 5 44, p ,
.0001).
All nests were checked daily and each molt and the exact
date of egg sac appearance was noted. It is not obvious from
the epigynum when a female is mature, so the date of maturation was inferred by back-dating from the date of oviposition
to the last molt. It is highly unlikely that a molt was missed
because the exuvia always remains in the nest. Therefore, females that mated or reproduced must have matured at the
last recorded molting. In this population, 46 females survived
from maturation to oviposition; 1 of them was not measured
at maturity, and 7 were not measured at oviposition. Therefore, sample sizes vary between 39 and 46 depending on the
variables used.
Captive population
I controlled the possible effects of size-dependent mortality,
mating frequency, and variation in foraging success by obtain-
ing a second set of data from a captive population in the
Negev Desert in Israel. Spiders were kept in a large, screened
insectary where they readily built their webs on fences erected
inside the enclosure. Spiders were fed flies, grasshoppers, and
cricket nymphs. I removed males from the insectary as soon
as they matured so that I could control all of the matings. In
1995 and in 1996, I recorded the prosoma width and total
body length and the dates of maturation and oviposition of
82 subadult females. Females were not measured at maturation, so I could not estimate a comparable measure of condition. Two males were placed with each female at different
intervals. The time interval between successive male encounters did not affect the timing of oviposition (Erez and Schneider, unpublished data).
Statistical analysis
I used general linear models to analyze the influences of different variables on the dependent variable. Significant correlations of predictor variables introduce the problem of collinearity. Although the significance of the complete regression
model is robust, the calculations of the influence of each variable may not be reliable.
The ambiguity arising from this collinearity can be avoided
by either computing partial correlation coefficients or by regressing the dependent variable on the residuals of the regression of the two independent variables. I used the first procedure when the model contained more than two predictor
variables, and the second procedure was used with two predictors.
RESULTS
Field population
The time between maturation and oviposition varied between
15 and 53 days (mean 5 28.5, SD 5 8.6, n 5 46). All spiders
increased in condition, but the increase was not a function of
time in the season (r 5 .03, p 5 .86, n 5 39), nor of the
length of the interval between maturation and oviposition (r
5 2.15, p 5 .35, n 5 39), nor of prosoma width at maturation
(r 5 2.12, p 5 .48, n 5 39). The variation in body condition
at maturation (coefficient of variation, CV 5 8.1) was similar
to the variation in condition at oviposition (CV 5 7.9), suggesting that spiders did not have to reach a certain condition
to produce eggs. Females that took longer to oviposit did not
encounter significantly more males (r 5 .151, n 5 43, p 5
.33).
There was a significant positive correlation between female
body condition at maturation and the day of maturation for
females that survived from maturation to oviposition (r 5 .4,
n 5 45, p 5 .006). Thus, late-maturing females tended to be
in a better condition than early-maturing females.
Multiple regression (n 5 39, F4,34 5 4.56, R2 5 .35, p 5
.0047) revealed that the day of maturation explains a significant proportion of the variance in the interval between maturation and oviposition (see Figure 1), whereas body condition, prosoma width, and the increase in condition were not
significant (Table 1).
Captive population
The spiders in the enclosure all experienced the same feeding
regime, two males, and an absence of predation. This ensured
no bias in the sample of females that survived from maturation to oviposition. Nevertheless, the timing of oviposition was
highly variable (14–64 days, mean 5 36, SD 5 9.6, n 5 41 in
1995 and 22–66 days, mean 5 42.2, SD 5 10.16 in 1996).
Schneider • Delayed oviposition and male infanticide
569
Table 1
Multiple regression with the time interval between maturation and
oviposition as dependent variable
Day of maturation
Prosoma width
Condition at maturation
Increase in condition until
oviposition
a
Figure 1
The interval between maturation and oviposition regressed on the
date of maturation (given as days after 1 January) in the field
population. The regression is significant (y 5 20.343x 1 70.398).
Data from 1995
Multiple regression (n 5 41, F2,38 5 4.94, R2 5 .21, p 5 .012)
revealed that maturation date was the significant predictor of
the timing of oviposition, whereas body size was not significant
(maturation date: b 5 2.49, t 5 23.07, p 5 .004; female body
size (prosoma width): b 5 2.11, t 5 20.69, p 5 .49). Prosoma
width was negatively correlated with the day of maturation (r
5 2.43, p 5 .005, n 5 41). The interval between maturation
and oviposition was regressed on the residuals of the regression of maturation date on body size (y 5 20.36x 1 36, R2 5
.20, F 5 9.52, p 5 .004, n 5 41; Figure 2 A) and of body size
on maturation date (y 5 24.64x 1 36, R2 5 .01, F 5 0.39, p
5 .53, n 5 41; Figure 2B). The results agree with the multiple
regression.
Data from 1996
There was a significant correlation between prosoma width
and maturation time (r 5 .527, p 5 .0004) for spiders in the
enclosure. A significant multiple regression model explained
the timing of oviposition (R2 5 .15, F2,38 5 3.30, p 5 .049),
with maturation date being the only significant predictor
[maturation date: b 5 -.45, t 5 22.57, p 5 .014; female body
size (prosoma width): b 5 2.25, t 5 21.45, p 5 .16]. A similar
pattern was revealed when the interval between maturation
and oviposition was regressed on the residuals of the regression of maturation date on body size (y 5 20.28x 1 42.32,
R2 5 0 .15, F 5 6.75, p 5 .013, n 5 41; Figure 2 A) and of
body size on maturation date (y 5 211.5x 1 42.32, R2 5 .05,
F 5 1.9, p 5 .17, n 5 41; Figure 2B).
Combined analysis of both years
The intervals between maturation and oviposition were significantly different between the 2 years, although the distributions overlap (Table 2). There was a significant correlation
b
t
p
Partial r a
2.58
2.23
2.19
23.66
21.15
21.03
.0009
.2575
.3112
2.531
2.194
2.174
2.17
21.21
.2357
2.203
Partial correlation coefficients were computed separately to control
for possible effects of collinearity.
between the day of maturation and prosoma width (r 5 2.48,
p , .0001).
Analysis of covariance (n 5 82, F3,78 5 8.23, R2 5 .24, p ,
.0001) revealed that maturation date explained the significant
proportion of the variance in the interval between maturation
and oviposition (Table 3). Prosoma width was a significant
covariate in the combined data set.
The relationship between the date of maturation, corrected
for prosoma width, and the interval between maturation and
oviposition was still negative and highly significant (Figure
2A). Regression of the interval between maturation and oviposition on the residuals of the regression of maturation date
on body size was also significant, but the relationship was not
strong (Figure 2B). Thus, early-maturing females delayed oviposition, and this delay was less pronounced among larger
females.
DISCUSSION
The time taken by females of the semelparous spider Stegodyphus lineatus to reach sexual maturity and oviposition varied
by a factor of four, in both natural and captive populations.
This variation is surprising because the constant, daily mortality risk ensures that females that reproduce more quickly
have a better chance of completing broodcare (Schneider,
1996a). Thus, the sooner a mother oviposits after reaching
maturation, the sooner she is consumed by her matriphagous
offspring. Why do some females take three times as long to
lay their eggs than others?
Infanticide avoidance hypothesis
A delay of oviposition reduces the risk of infanticide by males
because the presence of males in the population decreases as
the season progresses (Schneider and Lubin, 1996). Thus,
there should be a trade-off between the risk of mortality that
will select for shortening the reproductive period and the risk
of male-caused egg loss that will prolong it.
Infanticidal males inflict high costs on females, and females
may be selected to minimize the risk of encountering a male
after they oviposit. The expectation that early-maturing females, which suffer the highest risk of infanticide, also delayed
oviposition the most, was confirmed by three independent
data sets. This pattern persisted even though early-maturing
females tended to be larger and thus have a higher chance of
successfully defending their eggs against infanticidal males.
Body size was less important than maturation date in determining the timing of oviposition and only had a significant
effect on the timing of oviposition in the combined data sets
of the captive population. However, the slopes of the regression were consistently negative in all data sets. Although female body size does affect the probability of winning the fight
against the male, it does not influence the risk of encounter-
Behavioral Ecology Vol. 10 No. 5
570
Table 2
Comparison of 2 years in the enclosure (means with SDs in
parentheses)
1995
Interval (days)
Prosoma width (mm)
Day of maturation
1996
t
p
36 (9.6)
42.2 (10.2) 22.895
4.05 (0.23) 3.92 (0.23)
2.53
139.9 (12.9) 142.2 (16.5) 20.692
.005
.014
.491
ing an infanticidal male. Even females that win may suffer
injuries or other costs. Therefore, even a large female may
have a better chance of completing reproduction if she delays
oviposition. Alternatively, it may be impossible, or at least difficult, for a female to assess her own body size relative to the
distribution of male sizes in the population.
Although body size and maturation date explain a significant proportion of the variation in the timing of oviposition,
a large part of the variation remains unexplained. The unexplained variation may be a result of a mixed strategy in the
population, with a proportion of the females delaying oviposition at the cost of survival and another proportion ovipositing sooner at the risk of infanticide. The payoffs of each
strategy may vary between populations and years. Only longterm, large-scale monitoring of the costs and benefits of each
strategy will provide satisfying tests of these ideas.
Females may gauge the risk of infanticide by estimating
male activity directly in terms of male encounter rates or by
using seasonal parameters such as day length. In the captive
population, all females received two males, and the variation
in the timing of oviposition as well as the influence of the
date of maturation did not differ from the natural population.
This suggests that mating or encounter frequency per se does
not have a strong influence on the timing of oviposition. Intervals between male encounters did not affect oviposition
(Schneider, unpublished data). A likely factor that spiders
may use to adjust the timing of reproduction may be day
length.
Alternative explanations
Figure 2
(A) The interval between maturation and oviposition regressed on
the residuals of the date of maturation on female’s body size
(prosoma width) for both years combined (R2 5 .16, F 5 15.10, p
5 .0002, n 5 82, y 5 2.32x 1 39.159, solid regression line). (B)
The interval between maturation and oviposition regressed on the
residuals of the regression of female’s body size (prosoma width) on
the date of maturation for both years combined (R2 5 .05, F 5
4.57, p 5 .04, n 5 82, y 5 211.67x 1 39.159, solid regression line).
For panels A and B, circles and dashed regression lines represent
data from 1995 and squares and dotted regression lines represent
data from 1996 (see text for separate analyses).
Food
Body condition could determine the timing of oviposition in
two different ways: (1) females may have to achieve a certain
body condition before they can oviposit, and, for some reason,
early-maturing females take longer to reach the threshold; (2)
females may increase their fecundity by spending more time
feeding, but this is prevented by constraints on late maturing
females.
Several arguments speak against these explanations. First,
females that took longer to lay their eggs did not grow larger,
and the increase in body condition was not related with the
timing of oviposition. If females have to achieve a certain body
condition before being able to oviposit, we would expect that
the variation in body condition would be less at oviposition
than at maturation. However, this was not the case; variation
Table 3
ANCOVA with the time interval between maturation and oviposition
as dependent variable
b
Year
Day of maturation
Prosoma width
.29
2.43
2.18
t
2.86
23.85
21.50
p
.0055
.0002
.0137
Schneider • Delayed oviposition and male infanticide
in body condition was similar at both times. In a multiple
regression model, neither condition nor the increase in body
condition explained significant proportions of the variance in
the timing of oviposition. In addition, these spiders lay only a
few small eggs, clutch mass represents only 2–3% of the female’s body mass (Schneider, 1996a), and females continue
to forage during egg development. Body condition becomes
important only after the eggs hatch, about 2 months after
maturation, because the maternal resources that are available
for the young determine how large they grow before dispersal
(Schneider and Lubin, 1997a). Thus, prosoma width at maturation determines the potential to accumulate and store resources, and condition can improve substantially before the
eggs hatch. Of body length at oviposition, body weight at
hatching, and prosoma width, the latter showed the best correlation with the number of young (Schneider, 1992). Finally,
females in the enclosure had a similar and continuous supply
of food, yet still showed a large variation in the timing of their
oviposition.
Optimal time of hatching
Early-maturing females may delay oviposition if early-hatching
offspring are disadvantaged. This is unlikely because spiderlings that disperse early in spring have more time to feed and
grow before prey availability decreases, and larger juveniles
have a higher probability of surviving the winter (Schneider,
1996b). There is no reason that early reproduction has any
disadvantages for females, either. On the contrary, early-reproducing females escape the activity peak of a parasitic wasp
that is a main predator of adult females (Henschel et al.,
1996).
Mate choice
Delaying oviposition may increase the potential of multiple
mating and mate choice for females, as suggested for vertebrates (Birkhead and Møller, 1993). My data were not consistent with this idea, which predicts that early-maturing females,
who have the highest chance of male encounters, should delay the least. In addition, there was no relationship between
the interval between maturation and oviposition and the number of male encounters in the natural population.
Females that store sperm can separate fertilization from insemination and more effectively control which male’s sperm
to use for fertilization (Eberhard, 1985, 1996) and when to
use it (Birkhead and Møller, 1993). As a result, males may
have evolved counterstrategies, such as postcopulatory mate
guarding, sperm removal, and infanticide (Alexander et al.,
1997; Elgar, 1998; Schneider and Lubin, 1996, 1997b; Waage,
1981). A flexible female strategy that allows adjustments in
the time between mating and oviposition may counter these
male strategies by reducing the benefits of mate guarding,
increasing the costs associated with male mating strategies, or
regulating male encounter rates. Clearly, intersexual conflict
plays a potential role in maintaining plasticity in life-history
strategies of females.
I thank M. Elgar, T. Erez, Y. Lubin, D. Reznick, T. Tregenza, P. Watson,
and N. Wedell for critically commenting on the manuscript and for
discussing ideas. T. Erez, Y. Lubin, I. Musli, and H. Weimer helped
with the data collection, and many others contributed to the construction of the spider house. I am very grateful to all of them. This is
publication 269 of the Mitrani Center for Desert Ecology.
REFERENCES
Alexander RD, Marshall DC, Cooley JR, 1997. Evolutionary perspectives on insect mating. In: The evolution of mating systems in in-
571
sects and arachnids (Choe JC, Crespi BJ, eds). Cambridge: Cambridge University Press; 4–31.
Arnqvist G, Rowe L, 1995. Sexual conflict and arms races between the
sexes: a morphological adaptation for control of mating in a female
insect. Proc R Soc Lond B 261:123–127.
Birkhead TR, Møller AP, 1993. Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles,
birds and mammals. Biol J Linn Soc 50:295–311.
Clutton-Brock TH, Parker GA, 1995. Sexual coercion in animal societies. Anim Behav 49:1345–1365.
Eberhard WG, 1985. Sexual selection and animal genitalia. Cambridge, Massachusetts: Harvard University Press.
Eberhard WG, 1996. Female control: sexual selection by cryptic female choice. Princeton, New Jersey: Princeton University Press.
Elgar MA, 1998. Sperm competition and sexual selection in spiders
and other arachnids. In: Sperm competition and sexual selection
(Birkhead TR, Moller AP, eds). London: Academic Press; 307–337.
Grinnell J, McComb K, 1996. Maternal grouping as a defense against
infanticide by males: evidence from field playback experiments on
African lions. Behav Ecol 7:55–59.
Henschel JR, Schneider JM, Meikle T,1996. Does group-living or aggregation of the spiders Stegodyphus affect parasitism by the wasp
Pseudopompilus? Bull Br Arachnol Soc 10:138–140.
Kraus O, Kraus M, 1990. The genus Stegodyphus: systematics, biogeography and sociality (Araneida, Eresidae). Acta Zool Fenn 190:
223–228.
Kullmann EJ, Sitterz H, Zimmermann W, 1971. Erster Nachweis von
Regurgitationsfütterung bei der cribellaten Spinne (Stegodyphus lineatus LATREILLE, 1871, Eresidae). Bonn zool Beitr 22:175–188.
Parker GA, 1979. Sexual selection and sexual conflict. In: Sexual selection and reproductive competition (Blum MS, Blum NA, eds).
New York: Academic Press; 123–166
Schneider JM, 1992. Die Wurzeln des Soziallebens bei der subsozialen
Spinne Stegodyphus lineatus (Eresidae) (dissertation). Munich: University of Munich.
Schneider JM, 1995. Survival and growth in groups of a subsocial
spider (Stegodyphus lineatus). Insect Soc 42:237–248.
Schneider JM, 1996a. Differential mortality and relative maternal investment in different life stages in Stegodyphus lineatus (Araneae,
Eresidae). J Arachnol 24:148–154.
Schneider JM, 1996b. Food intake, growth and relatedness in the subsocial spider, Stegodyphus lineatus (Eresidae). Ethology 102:386–
396.
Schneider JM, 1997. Timing of maturation and the mating system of
the spider, Stegodyphus lineatus: how important is body size? Biol J
Linn Soc 60:517–525.
Schneider JM, Lubin Y, 1996. Infanticidal male eresid spiders. Nature
Lond 381:655–656.
Schneider JM, Lubin Y, 1997a. Does high adult mortality explain semelparity in the spider Stegodyphus lineatus (Eresidae). Oikos 79:
92–100.
Schneider JM, Lubin Y, 1997b. Infanticide by males in a spider with
suicidal maternal care, Stegodyphus lineatus. Anim Behav 54:305–
312.
Waage JK, 1981. Sperm competition and the evolution of odonate
mating systems. In: Sperm competition and the evolution of animal
mating systems (Smith RL, ed). New York: Academic Press; 251–
290.
Ward D, Lubin Y, 1993. Habitat selection and life history of a desert
spider, Stegodyphus lineatus (Eresidae). J Anim Ecol 62: 353–363.