Journal of Insect Physiology 46 (2000) 1489–1496
www.elsevier.com/locate/jinsphys
Associations between female remating behavior, oogenesis and
oviposition in Drosophila melanogaster and Drosophila
pseudoobscura
Rhonda R. Snook *, Yee K. So
Department of Biological Sciences, 4505 S. Maryland Parkway, University of Nevada Las Vegas, Las Vegas, NV 89154-4004, USA
Received 10 January 2000; accepted 4 April 2000
Abstract
An association between female remating behavior, oogenesis and oviposition was examined in Drosophila melanogaster and
Drosophila pseudoobscura to investigate mechanisms that elicit remating. Females receptive to remating oviposited more eggs in
both species; however, the species differed in the association between remating behavior and the number and distribution of oocyte
stages. We found no differences in the number of either developing eggs of different stages or mature eggs between female D.
pseudoobscura that were either receptive or nonreceptive to remating. In contrast, D. melanogaster females that are receptive to
remating had significantly more mature eggs in the ovaries than nonreceptive females. Nonremating females had a significantly
greater number of immature, vitellogenic oocytes. These results suggest that factors associated with oogenesis are related to female
remating behavior in D. melanogaster but not in D. pseudoobscura. We discuss these results in conjunction with other evidence on
the role male ejaculatory components play in mediating female remating behavior.  2000 Elsevier Science Ltd. All rights reserved.
Keywords: Remating; Oogenesis; Oviposition; Drosophila; Ejaculate
1. Introduction
The study of insect mating systems has frequently
served to link physiological and behavioral traits in an
evolutionary context. One recurrent issue is the adaptive
significance of female remating behavior on the reproductive success of both females and males (Thornhill
and Alcock, 1983; Birkhead and Møller 1992, 1998;
Chapman et al., 1995; Rice, 1996) and the physiological
factors of both males and females that control female
remating behavior (Manning 1962, 1967; Fuchs and
Hiss, 1970; Leopold, 1970; Gromko et al., 1984; Scott,
1987; Young and Downe, 1987; Bergh et al., 1992;
Gromko and Markow, 1993; Kalb et al., 1993; Kubli,
1996; Yuval et al., 1996; Wolfner, 1997; Miyatake et
al., 1999). At least nine hypotheses have been suggested
to explain the ultimate significance of female remating
* Corresponding author. Tel.: +1-702-895-1395; fax: +1-702-8953956.
E-mail address: [email protected] (R.R. Snook).
behavior (Halliday and Arnold, 1987) and some proximate factors that mediate female remating behavior have
been identified (Kubli, 1996; Wolfner, 1997). For
example, females may benefit from remating by having
higher fecundity and, in several Drosophila species,
multiple mating by females does increase their reproductive success (Pruzan-Hotchkiss et al., 1981; Markow,
1996). This increase, however, is costly to Drosophila
melanogaster females because it results in early death.
Causes of increased mortality include exposure to males
and increased egg production as a result of mating
(Partridge et al., 1987), and male accessory gland proteins (Acps) transferred in the ejaculate (Chapman et al.,
1995). Recent work by Wolfner, Kubli and their colleagues have shown that these Acps proximately mediate
behavioral and physiological alterations in females
related to remating and oviposition (Kubli, 1996;
Wolfner, 1997).
Female remating behavior is complex and influenced
by several factors. Following mating, females in many
insects exhibit two conspicuous behavioral alterations:
decreased receptivity to mating and increased ovi-
0022-1910/00/$ - see front matter  2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 2 - 1 9 1 0 ( 0 0 ) 0 0 0 7 4 - 3
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R.R. Snook, Y.K. So / Journal of Insect Physiology 46 (2000) 1489–1496
position (Chen, 1984; Gillot, 1988; Wolfner, 1997).
These alterations have both short- and long-term physiological cues. The short-term effect, called the copulation
effect in Drosophila (Manning, 1967), is related to
decreased attractiveness to males through alterations in
pheromones (Scott, 1986; Hall, 1994), decreased locomotor response to males (Tompkins et al., 1982), and
decreased receptivity to remating through increased oviposition (Fuyama, 1995) and ejaculatory fluids (Kubli,
1996; Wolfner, 1997). In a variety of insects, molecules
in the male’s accessory fluid have been shown to temporarily reduce female receptivity and induce oviposition
(Chen, 1984; Gillot, 1988; Wolfner, 1997). For example,
both sex peptide (SP) and Acp26Aa induce oviposition
and SP also acts to decrease female receptivity to remating in D. melanogaster (Monsma and Wolfner, 1988;
Aigaki et al., 1991; Schmidt et al., 1993a,b; Herndon
and Wolfner, 1995; Soller et al. 1997, 1999).
In D. melanogaster, but not in other insects (Chapman
et al., 1998; Snook, 1998; Miyatake et al., 1999), longterm suppression of female remating has been indirectly
linked to sperm load, and termed the sperm effect
(Manning 1962, 1967; Gromko et al., 1984; Scott, 1987;
Gromko and Markow, 1993; Kubli, 1996). Female
receptivity is proximately controlled by the central nervous system (CNS) in D. melanogaster (Tompkins and
Hall, 1983) and a mechanical stimulation of the CNS
through sperm motility detected by innervation of the
sperm storage organs has been suggested to mediate the
long-term inhibition to female remating (Gromko et al.,
1984). Positive correlations between female remating
behavior and progeny production (an index of sperm use;
Trevitt et al., 1988; Gromko and Markow, 1993) have
been used to support the relationship between sperm load
and female receptivity. For example, laboratory female
D. melanogaster that oviposit more eggs or produce
more progeny remate more quickly than females ovipositing fewer eggs or producing less progeny (Trevitt
et al., 1988). In addition, field-caught D. melanogaster
and Drosophila simulans females produced fewer progeny when they were interrupted during mating (prior to
sperm transfer) compared with nonmating females randomly collected adjacent to the mating pair (Gromko and
Markow, 1993). These results suggested that remating
females had a smaller sperm load than nonremating
females (Gromko and Markow, 1993). Further indirect
evidence correlating female remating behavior with
sperm load is the positive relationships between the
number of sperm received per copulation and female
remating interval in some Drosophila species (Pitnick
and Markow, 1994a). However, no study has directly
quantified sperm loads of receptive and nonreceptive D.
melanogaster females.
Female remating behavior in the Drosophila obscura
species group also appears to be related to sperm load.
Similar to D. melanogaster, females receptive to remat-
ing oviposit more eggs than nonreceptive females, and
a positive relationship between either fecundity or productivity and female remating behavior exists (PruzanHotchkiss et al., 1981; Snook, 1998). In an effort to
directly determine if female remating behavior and
sperm load are linked, Snook (1998) quantified the number of sperm present in the sperm storage organs of Drosophila pseudoobscura females that were receptive to
remating compared with nonremating females. No difference in sperm load was found between remating and
nonremating females, although remating females did
oviposit more eggs. Instead of a dependence on sperm,
female receptivity to remating was most predictably
related to the absence of an egg in the uterus (Snook,
1998). Thus, any long-term inhibition to remating in D.
pseudoobscura has been shown to be unrelated to sperm
and at least indirectly related to oviposition. Given that
there was no association between female remating
behavior and sperm load and that female remating was
related to oviposition in D. pseudoobscura, Snook
(1998) suggested that oviposition per se mediated female
remating behavior in that species.
In support of this notion, D. pseudoobscura exhibits
rhythmic oviposition with regular alternation of periods
of egg laying and quiescent periods (Shapiro, 1932;
Dobzhansky, 1935; Donald and Lamy, 1937; Snook, personal observations). Additionally, across ovarioles, there
is a parallel synchronization of egg development
(Donald and Lamy, 1937). Donald and Lamy (1937)
noted that the “alternate” egg-laying behavior by D.
pseudoobscura depletes the ovarioles of mature eggs and
that, during quiescent periods, mature eggs accumulate.
Hence, a large number of eggs become ready for laying
at one time. In contrast, D. melanogaster females oviposit fairly equal numbers of eggs each day (Shapiro,
1932; Dobzhansky, 1935; Donald and Lamy, 1937), and
do not exhibit synchronization of ovariole development
(Donald and Lamy, 1937). Thus, eggs are found at all
stages of development in mated females and eggs do not
ripen in batches (Donald and Lamy, 1937). The differences in oogenesis and oviposition between these two
species (synchronous and thus rhythmic, versus asynchronous and constant) support testing the hypothesis
that female remating behavior in D. pseudoobscura, but
not D. melanogaster, may be mediated by oogenesis, and
thus oviposition, per se. For example, female D. pseudoobscura may remate between deposition of successive
synchronous egg clutches, similar to some birds
(Birkhead and Møller, 1992), whereas receptivity to
remating in D. melanogaster females would have no
association with these factors.
Here we tested the hypothesis that female remating
behavior is at least indirectly mediated by the number
and stage of developing oocytes and mature eggs in D.
pseudoobscura but not in D. melanogaster. Given the
different oogenesis and oviposition patterns, we pre-
R.R. Snook, Y.K. So / Journal of Insect Physiology 46 (2000) 1489–1496
dicted that D. pseudoobscura females receptive to remating would have fewer mature eggs than nonremating
females, whereas no difference would be found between
remating and nonremating D. melanogaster females. We
found the opposite: remating D. pseudoobscura females
do not differ from nonremating females in the number
of oocytes at any stage of development, whereas remating D. melanogaster females had significantly more
mature eggs than nonremating females but significantly
fewer vitellogenic immature eggs. We discuss these
results with respect to the interaction between physiological mechanisms controlling receptivity, oogenesis
and oviposition.
2. Materials and methods
2.1. Fly maintenance
The Drosophila melanogaster culture was established
in February 1999 from multiple females collected on
fallen citrus in Tempe, Arizona (collected by T.A.
Markow). Drosophila pseudoobscura was collected in
the same manner from the same area in March 1999. All
cultures were maintained on standard cornmeal–agar–
molasses food with yeast and kept at room temperature,
22–25°C, and an approximate 12 h/12 h light/dark cycle.
We collected virgin flies, separated males and females
upon eclosion using CO2 anesthetization, and stored
each sex at 10 flies per 8 dram yeasted food vials. All
flies used were 5 days old and reproductively mature.
2.2. Remating tests
Remating tests generally followed those described in
Snook (1998). We paired two virgin males with a virgin
female in a yeasted food vial in the morning. Upon mating and the completion of copulation, males were
removed from the vial by aspiration. Forty-eight hours
later, we paired two virgin males with a previously
mated female in her vial for a maximum of 2 h. A female
was considered receptive to remating if she remated. If
females did not indicate a willingness to remate by the
end of the 2 h receptivity test, they were considered nonreceptive. In these cases, males were removed from the
vials. Remated and nonremated females were immediately dissected and processed for ovarian counts as
described below. During dissections, we noted whether
females had an egg in the uterus. We also counted the
number of eggs oviposited in vials that held females during the time between the first mating and the test for
receptivity to remating.
2.3. Scoring vitellogenic stages
Ovarian development was scored by dissecting ovaries from females and processing the ovaries for epifluo-
1491
rescence microscopy. Ether-anesthetized females were
dissected in phosphate buffered saline (PBS) and the
ovaries from a single female were placed in a microcentrifuge tube containing heptane and devitillizing membrane buffer as previously described (Cooley et al.,
1992). Ovaries were rinsed in PBS, stained with diaminophenylinidole (DAPI; Sigma) at 1 µl/ml PBST (PBS
containing 0.1% Triton X-100) for 5 min, rinsed again
in PBS, and placed on a microscope slide in mounting
media containing 80/20 (v/v) glycerol and PBS, respectively containing 1% (w/v) n-propyl gallate (Giloh and
Sedat, 1982). Ovarioles were then spread apart using
insect pins to observe all egg stages and a coverslip
placed over the sample. Oocyte stages were characterized as described in King (1970) using a Leica DMLB
microsocpe equipped with epifluorescence. Images were
visualized using the appropriate filter for DAPI fluorescence and a 40× Plan Fluotar lens (n.a.=0.70). As a
single category, we scored pre-vitellogenic stages 1–7
and early vitellogenic stage 8. Immature vitellogenic
oocytes of stages 9–13 and mature stage 14 eggs were
individually enumerated.
2.4. Statistical analyses
All statistical analyses were performed using Systat
(Version 5). The number of eggs oviposited between the
initial mating and the receptivity test and the total number of developing eggs found in remating and nonremating females were compared using a t-test. To analyze
differences between remating and nonremating females
(“treatment”) in the number of oocytes of different
stages and mature eggs, we performed a repeated-measures analysis of variance (ANOVA). This statistical
analysis was chosen because of the potential of the number of eggs of one stage influencing the number of eggs
in a different developmental stage within individual
females. Once again, stage 1–8 oocytes were analyzed
together, whereas vitellogenic immature stages 9–13 and
mature stage 14 eggs were considered separately.
3. Results
Remating females of both species oviposited more
eggs prior to remating than those females that were nonreceptive to remating (Fig. 1; D. pseudoobscura: df=58,
t=3.196, P=0.002; D. melanogaster: df=64, t=2.445,
P=0.017). Nonremating D. pseudoobscura females usually had an egg in the uterus whereas remating females
did not (Table 1), as was found previously (Snook,
1998). This factor predicts ca. 70% of the remating
response in D. pseudoobscura (Table 1). Nonremating
D. melanogaster females also frequently had an egg in
the uterus in contrast to remating females, and the
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R.R. Snook, Y.K. So / Journal of Insect Physiology 46 (2000) 1489–1496
Table 2
Results from a repeated-measures ANOVA on the relationship between
oocyte stages and female remating behavior in D. pseudoobscura
Source
MS
Between-subject effects (df=1, 56)
Treatment
22.564
Error
139.446
Within-subject effects (df=6, 6, 336)
Stage
19,600
Stage×Treatment
291.021
Error
197.603
Fig. 1. Total number of eggs oviposited between first remating and
receptivity test (“Eggs laid”), the number of oocytes in various developmental stages, and the total number of eggs being produced
(mean±standard error of the mean) by receptive and nonreceptive
females for D. pseudoobscura and D. melanogaster. * indicates comparisons that are statistically significantly different (see Results).
Egg present in Egg absent in
uterus
uterus
D. pseudoobscura
Nonremating
Remating
c2=43.866, df=1, P⬍0.0001, R2=0.69
D. melanogaster
Nonremating
Remating
c2=62.11, df=1, P⬍0.0001, R2=0.90
24
0
4
30
34
1
0
31
absence of an egg predicted ca. 90% of the remating
response in D. melanogaster (Table 1).
Remating and nonremating D. pseudoobscura females
did not differ in the total number of eggs being produced
P
0.162
0.689
99.1
1.473
⬍0.001
0.187
(Fig. 1; Table 2, “between-subjects” effect). Within-subject effects were found to be significant, indicating that
there was a relationship between the number of eggs of
a particular developmental stage and the number of eggs
in a different developmental stage. However, remating
and nonremating females did not differ in this response
(Table 2).
Similar to D. pseudoobscura, remating and nonremating D. melanogaster females did not differ in the total
number of eggs being produced (Fig. 1; Table 3).
Within-subject effects were also found to be significant,
indicating a dependence of the number of eggs in one
stage on the number of eggs in another stage within an
individual (Table 3). In contrast to D. pseudoobscura,
however, this pattern differed between remating and
nonremating females (Table 3). Subsequent univariate FTable 3
Results from a repeated-measures ANOVA on the relationship between
oocyte stages and female remating behavior in D. melanogaster
Source
Table 1
Chi-square analysis of the association between the presence or absence
of an egg in the uterus and female remating behavior in D. pseudoobscura and D. melanogaster
F
MS
Between-subject effects (df=1, 64)
Treatment
0.642
Error
98.422
Within-subject effects (df=6, 6, 384)
Stage
15,900
Stage×Treatment
550.855
Error
58.216
Univariate F tests
Stages 1–8 (df=1,
330.011
64)
Error
206.127
Stage 9
41.776
Error
43.318
Stage 10
285.522
Error
49.386
Stage 11
0.243
Error
1.152
Stage 12
26.444
Error
5.611
Stage 13
8.001
Error
4.547
Stage 14
2613.776
Error
137.576
F
P
0.007
0.936
273.5
9.462
⬍0.001
⬍0.001
1.601
0.210
0.964
0.330
5.781
0.019
0.211
0.648
4.713
0.034
1.76
0.189
18.999
⬍0.001
R.R. Snook, Y.K. So / Journal of Insect Physiology 46 (2000) 1489–1496
tests indicated that the difference between remating and
nonremating females occurred at stage 10, stage 12 and
stage 14 (Table 3; Fig. 1). Nonremating females produced significantly more vitellogenic, immature stage 10
and 12 oocytes, whereas remating females produced significantly more mature stage 14 eggs.
4. Discussion
We found that remating females oviposited more eggs
than nonremating females. These results are consistent
with previous studies of D. melanogaster (Trevitt et al.,
1988) and D. pseudoobscura (Snook, 1998) using different strains than those examined here. Formerly, the
observation that remating females lay more eggs than
nonremating females has been used to infer that sperm
load mediated female remating behavior since females
that oviposited more eggs had probably used more sperm
and thus carried a smaller sperm load. However, Snook
(1998) demonstrated that, while remating D. pseudoobscura females oviposited more eggs than nonremating
females, no differences between females in sperm load
were found. Instead, females receptive to remating
tended to not have an egg in the uterus whereas nonreceptive females possessed an egg in the uterus (Snook,
1998). We therefore examined an alternative hypothesis
to explain female receptivity to remating in D. pseudoobscura: female remating behavior is at least indirectly
mediated by oogenesis and, thus, oviposition.
We found that nonremating D. pseudoobscura females
had an egg present in the uterus whereas remating
females did not, as previously seen in a different D.
pseudoobscura strain (Snook, 1998). Interestingly, D.
melanogaster females also exhibited this phenomenon.
This result has not previously been reported for this
species. However, Fuyama (1995), using homozygous
lozenge mutant females that have increased spontaneous
ovulation, found virgin females more reluctant to mate
than wild-type females. In contrast, Hihara (1981)
reported that females genetically altered so as to not oviposit had the same remating interval as ovipositing
females. Here we find that oviposition and female remating behavior in D. melanogaster are linked (through
increased egg laying and the absence of an egg in the
uterus).
Whether the observation that remating females lack
an egg in the uterus compared with nonremating females
is general to Drosophila remains to be determined, but
given the reproductive biology of this group, is intuitive.
Males transfer sperm to females in the uterus and sperm
then move into the female sperm storage organs. At the
onset of oviposition, any sperm that remain in the uterus
and have not been stored are evacuated by the act of egg
deposition due to the fact that the egg occupies the entire
space of the uterus (Scott, 1987). Males that transferred
1493
sperm to a female with an egg in the uterus would have
his sperm posterior to the egg and may lose his investment when the egg is oviposited, because the sperm may
be unable to maneuver around the egg in the female
reproductive tract and thus would be evacuated when
the female oviposits. Females may also not benefit from
remating when an egg is in the uterus because Acps may
still enter the hemolymph and cause decreased female
life span (Chapman et al., 1995) with no corresponding
benefit of additional mating (Gromko and Markow,
1993) since, as the egg is laid, recently transferred sperm
would be removed by the act of oviposition (Scott,
1987). Therefore, selection would presumably act on
males to discriminate between females with and without
an egg in the uterus if the ejaculate (Pitnick and Markow,
1994b) and/or mating were costly or limited. Selection
would act on females to avoid mating if mating is costly
(Partridge et al., 1987; Chapman et al., 1995; Rice,
1996).
An alternative explanation for the association between
having an egg in the uterus and nonremating is that it
may be a stochastic phenomenon, perhaps related to timing of courtship by males, rather than selective. Females
may be unwilling to remate only during the time an egg
is in the uterus. As soon as an egg is deposited, unless
another egg moves immediately into the uterus, the
female may be willing to remate. The lack of remating
during the time when the uterus is empty may be a missed opportunity by the male, perhaps because he is not
near the female and not actively courting. Thus, the
association between having an egg in the uterus and a
female not remating may be spurious.
We think this is unlikely for several reasons. First,
complete sperm storage takes several hours in D. melanogaster (Markow, 1996) and over 24 h in D. pseudoobscura (Snook et al., 1994). If females were constantly
ovipositing, then males that mated with a female in
which the uterus was only temporarily unoccupied
would lose a large quantity of their investment since the
next egg oviposited would evacuate unstored sperm.
Second, dissections of young, healthy, mated D. pseudoobcura (Snook, personal observations) and D. melanogaster (S. Pitnick, personal observations) females
frequently reveal eggs in their uterus. No study has
examined either how long it takes an egg to become fertilized and subsequently oviposited, or what percentage
of time during the day males are courting females in
which the uterus is occupied by an egg. However, the
observations that females typically have an egg in the
uterus suggests that there is little opportunity of a vacant
uterus and that when a female is ovipositing and producing mature eggs, an egg probably occupies the uterus a
majority of the time.
In toto, the time it takes for sperm storage and the
observations that during bouts of oviposition the uterus
is rarely empty suggest that timing (or mistiming) of
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R.R. Snook, Y.K. So / Journal of Insect Physiology 46 (2000) 1489–1496
male courtship does not explain the association between
female nonreceptivity and the presence of an egg in the
uterus. Instead, this association is likely a real phenomenon, the proximate basis of which needs to be elucidated. Perhaps stretch receptors in the uterus cue females
as to their oviposition status and the number of mature
eggs still to be oviposited.
Another spurious relationship may be that because we
examined only one line from each species, our results
may reflect line-to-line variation as opposed to interspecies differences. We think this unlikely for several
reasons. First, in two different lines of D. pseudoobscura, both strains exhibited a significant association
between remating behavior and the absence of an egg in
the uterus (Snook, 1998; this study). Second, females
that were willing to remate had oviposited more eggs
than females unwilling to remate in both these strains
(Snook, 1998; this study). Third, we found that remating
D. melanogaster females also had oviposited more eggs
than females that did not remate, a result that has been
reported several times in the literature using different
strains (Trevitt et al., 1988, Chapman et al., 1994; Chapman and Partridge, 1996). Finally, in our D. melanogaster strain, we found that females, regardless of whether
they were willing to remate or not, had equal amounts
of stage 8 and 9 eggs, similar to previous reports (Soller
et al., 1997). In toto, these results indicate that associations between remating behavior, oviposition and oogenesis are consistent across strains for both species, and
thus our results are likely true reflections of interspecies differences.
Oviposition and oogenesis are inextricably linked. We
therefore examined the role oogenesis may play in
mediating female remating behavior by determining
whether receptivity could be predicted by the number of
eggs of any particular oocyte stage. We anticipated that
the synchronous oogenesis and, thus, rhythmic (i.e.,
clutch) oviposition found in D. pseudoobscura would
result in females remating between successive clutches,
and therefore remating females should have more immature eggs and fewer mature eggs compared with nonremating females. In contrast, we predicted that the asynchronous oogenesis (and thus constant oviposition) in D.
melanogaster would not mediate female remating
behavior. Therefore, there should be no difference
between remating and nonremating females with respect
to ovarian status. Our results did not support these predictions. No differences in ovarian status between remating and nonremating D. pseudoobscura females were
found, whereas remating D. melanogaster females had
more mature eggs and fewer stage 10 and 12 oocytes
than nonremating females (moreover, combining vitellogenic stages 10–13 still results in significant differences between remating and nonremating females).
Contrary to our original prediction, female remating
in D. melanogaster is at least indirectly related to oogen-
esis and, thus, oviposition. Egg production and egg laying in D. melanogaster are tightly coupled to mating and
sperm use (Kubli, 1996; Wolfner, 1997). Acps transferred by the male during copulation stimulates oogenesis, elevates oviposition, and influences sperm storage
(Kubli, 1996; Wolfner, 1997; Neubaum and Wolfner,
1999; Tram and Wolfner, 1999). Kubli and colleagues
have defined a “control point” during oogenesis in D.
melanogaster related to mating that subsequently influences egg development (Soller et al. 1997, 1999). Mated
females and those injected with physiological amounts
of the male ejaculatory fluid, SP, had a four- to sixfold
increase in the number of stage 10 eggs compared with
unmated females and those injected with saline, but all
treatments had equal amounts of stage 8 and 9 eggs
(Soller et al., 1997). These results suggest that the progression of vitellogenic oocytes is stimulated after mating, through actions of SP on the females’ CNS that also
controls receptivity and oviposition (Soller et al., 1999).
Given these interactions, how might oviposition and
oogenesis at least indirectly mediate female remating in
D. melanogaster? One potential mechanism for the
association between oogenesis and female remating is
that SP, through the CNS, acts on nonreceptive females
at the control point of oogenesis, resulting in increased
numbers of stage 10 oocytes. The large number of stage
10 oocytes may then indicate to females that they
recently mated and to start oviposition, and thus become
nonreceptive. As the effect of SP declines (possibly
through decreased titer in the hemolymph), females may
return to a “virgin” state, that is few stage 10 eggs
(Kubli, 1996), subsequently indicating to females to
decrease oviposition and thus resulting in females
becoming receptive to remating. This response could be
either independent of or in conjunction with the sperm
effect.
Unlike D. melanogaster, oogenesis per se plays no
role in influencing female remating in D. pseudoobscura,
at least for the remating interval examined. No differences in ovarian status were found between remating and
nonreceptive females. This result suggests that there may
be different physiological influences of male ejaculatory
components, such as SP, on females of the two species.
Perhaps the half-life of SP and the cascade of female
responses triggered by SP is different, or SP does not
act on oogenesis at the same control point or in the same
fashion. To our knowledge, the physiological effects of
male ejaculatory components on female behavior,
including receptivity, oviposition and oogenesis, have
been investigated in species other than D. melanogaster
(e.g., Schmidt et al., 1993a; Imamura et al., 1998) but
not D. pseudoobscura.
Drosophila female receptivity is a complex behavior
that is influenced by several factors, including male
ejaculatory fluids and sperm (Manning 1962, 1967;
Gromko et al., 1984; Scott, 1987; Gromko and Markow,
R.R. Snook, Y.K. So / Journal of Insect Physiology 46 (2000) 1489–1496
1993; Kalb et al., 1993; Kubli, 1996; Wolfner, 1997;
Neubaum and Wolfner, 1999; Tram and Wolfner, 1999).
We have presented evidence that suggests oogenesis and
oviposition may also trigger female remating, either
alone or in concert with male effects, in one species of
Drosophila but not in another species. These results indicate new research directions to understand links between
physiological and behavioral traits affecting male and
female fitness and proximate mechanisms controlling
these processes in different species.
Acknowledgements
We thank Kathy Davidson and Cher Chang for technical support, Scott Pitnick and Steve de Belle for
reviewing an earlier version of the manuscript, and T.
Markow for reminding R.R.S. that oogenesis can be as
interesting as spermatogenesis. This research was supported in part by a grant from the National Science
Foundation to R.R.S. (DEB-9815962).
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