A set of female pheromones affects reproduction before, during and after mating in Drosophila
Unité de Recherche 5548 Associée au Centre National de la Recherche Scientifique, Faculté des Sciences, Université de Bourgogne, 6, Boulevard Gabriel, 21 000 Dijon, France
* Author for correspondence (e-mail: jean-francois.ferveur{at}u-bourgogne.fr)
Accepted 10 August 2004
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Summary |
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Key words: sex pheromone, copulation duration, pheromonal communication, Drosophila, desat1
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Introduction |
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The precise pheromonal influence of the molecular components of a complex
bouquet is difficult to measure in live animals because the experimental
methods involved in isolating and testing chemicals do not closely parallel
the in vivo situation. In Drosophila melanogaster, two
experimental in vivo approaches have been used to dissociate and
measure the behavioral influence of some of the cuticular hydrocarbons (CHs)
in the pheromonal bouquet of mature females (16 CHs) and males (12 CHs;
Jallon and David, 1987). (1)
Mutant strains with defective CHs have been induced
(Ferveur and Sureau, 1996
;
Ferveur et al., 1997
;
Savarit and Ferveur, 2002
),
and (2) flies have been covered with foreign CHs from `donor' flies of
different genotypes (Coyne et al.,
1994
). Both approaches have been used separately to measure the
influence of female and male CHs on male intra- or interspecific courtship and
mating behaviours (Ferveur and Sureau,
1996
; Coyne, 1996
;
Coyne and Charlesworth, 1997
),
or combined to produce mutant CH-depleted females perfumed with the CHs of
donor females of different species
(Savarit et al., 1999
).
Several studies revealed that 7,11-dienes in female D. melanogaster
prevent interspecific courtship and copulation
(Coyne and Oyama, 1995
;
Savarit et al., 1999
).
D. melanogaster females show a natural polymorphism for the amount
of two heptacosadiene (HD) isomers: 7,11-HD is predominant in most strains
(e.g. Canton-S=Cs), whereas 5,9-HD levels are relatively high in Caribbean and
sub-Saharan strains (e.g. Tai; Ferveur et
al., 1996). The 7,11-HD:5,9-HD ratio is entirely controlled by
desat1 and desat2, two closely linked genes on chromosome 3
(Coyne et al., 1999
;
Dallerac et al., 2000
). A
mutation in the promoter of desat2 has been correlated with variation
in HD ratio (Takahashi et al.,
2001
), and a case of incipient speciation in Zimbabwe strains
seems to be caused by variation in desat2
(Ting et al., 2001
;
Fang et al., 2002
). We
recently induced a mutation in desat1 that drastically affects the
production of all unsaturated CHs including the predominant sex pheromones in
both sexes, together with male discrimination of these signals (F. Marcillac,
Y. Grosjean and J.-F. Ferveur, unpublished observations). Moreover, the same
desat1 mutation affects the disengagement of mutant females after
copulating with mutant males. The alteration of various reproductive
characters induced by desat1 suggests that this gene may be related
to the evolution of pheromonal communication in Drosophila.
Here, we have measured the effect on reproduction of a set of female pheromones that includes 7,11-dienes. These pheromones, which are largely reduced in desat1 mutant females, were replaced by contact with control Cs females. Their effect was evaluated on mate choice of Cs males, and on both copulation latency and duration of the males of various strains. The effect of Cs female pheromones was also measured on the number and sex-ratio of their offspring. Our results indicate that these substances affect several reproductive characters that occur before, during and after mating.
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Materials and methods |
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Canton-S (Cs) is a widely used control strain of Drosophila
melanogaster. Tai is a CH-variant strain from Ivory Coast that has been
kept in the laboratory for over two decades
(Jallon and Pechiné,
1989). The desat11573-1 mutant strain was
induced by the insertion of a single PGawB (or PGal4)
transposon (Brand and Perrimon,
1993
). The gene altered by the PGal4 transposon was
mapped after cloning and sequencing of the two DNA fragments flanking the
insertion point. The comparison with the BDGP database revealed that these
fragments share a complete identity with two contiguous sequences of the
desat1 gene (Marcillac et al., in
press
). To generate derivative lines of
desat11573-1, we jumped out the PGal4 transposon
(Cooley et al., 1988
). When
these lines were stabilized, all desat11573-excision
alleles were outcrossed with the Cs strain for five generations to homogenize
genetic background and to obtain transposon-less male flies that were used in
behavioural tests. We tested five desat11573 alleles:
desat11573-1, desat11573-J2 and
desat11573-E1, which are affected for both their CH
production and male discrimination, and desat11573-N2 and
desat11573-D'1
alleles, which are totally rescued for their CH production and totally (N2) or
partly (D'1) rescued for male ability to discriminate sex pheromones (F.
Marcillac, Y. Grosjean and J.-F. Ferveur, unpublished observations).
Detection of cuticular hydrocarbons
Extraction of cuticular hydrocarbons (CHs), gas chromatography of the
extracts and estimation of CH quantities were performed on single 5-day-old
flies washed in hexane following a standard procedure
(Ferveur, 1991).
Quantification of CHs was carried out by using a Varian CP3380 chromatograph
(Walnut Creek, CA, USA), equipped with a Cp-sil 25 m/0.25 mm capillary column,
with hydrogen as the carrier gas. CHs were calibrated with an added standard
of hexacosane.
Transfer of hydrocarbons
Virgin mutant females were crowded in a 4 ml space in a tube with fresh
food together with Cs donor females, the day before the test. To change the
proportion of unsaturated CHs, the total number of females was kept constant
(80), and the mutant: donor female's ratio varied between 40:40 and
65:15. The ratio of unsaturated: saturated CHs was used to measure the
quantity of CHs transferred by donor Cs flies relative to the native CHs
carried by the receiver mutant females. To control the effect of this
experimental procedure, 80 desat1 females were crowded using similar
experimental conditions. Females were distinguished by wing clipping, which
was rotated between genotypes. CH extraction and analysis were performed on
some of the flies that were to be used the same day in behavioural tests.
Choice tests were carried out with 16 independent samples (with
12
N
30).
Courtship and mating tests
Most experiments were carried out with mutant
desat11573-1 females covered with exogenous CHs, either
provided by Cs, desat1 or Tai female donors. Male behaviour was
tested using two control strains (Cs and Tai), and with males homozygous for
the five desat11573 alleles described earlier. Flies were
isolated 14 h after eclosion. All males were isolated in a food vial
while females were kept in groups of five until 4 days old, and crowded 24 h
before the test. All tests took place 14 h after lights on, which is
the period during which flies are sexually more active
(Tauber et al., 2003). Tester
males were individually aspirated into an observation chamber (3.5
cm2), and after 5 min, one or two females (for non-choice or choice
experiments, respectively) were introduced. We measured the latency to
copulate (time in minutes from the introduction of the female into the chamber
until copulation) and the duration of copulation (time in minutes from the
copulation onset until disengagement), during 1 h test experiments. In choice
tests, target females were distinguished by wing-clipping, which was rotated
within treatments. Wing-clipping induced no detectable effect on the behaviour
tested here (data not shown).
The target flies used for the simultaneous discrimination test were decapitated a few minutes prior to the test. The simultaneous discrimination index (SDI) measures the difference of the courtship indices (CI1CI2) that a single subject male directed towards two different headless flies (a female and a male of the same strain) during a 5 minobservation period, under red light. CI is the cumulative amount of time in minutes that the male spends in active courtship (wing vibration, licking and attempting copulation). Experiments performed in red light with headless object flies eliminated most of visual and acoustic signals and enhanced the role of pheromones.
Measure of fertility, fecundity, sex ratio and survival
Immediately after mating, each female was transferred alone into a food
vial and allowed to lay eggs for 1 week. A female was considered fertile when
she yielded at least one viable adult offspring. To measure fecundity, male
and female viable adult offspring were counted each day for the 8 days
following the first day of adult eclosion. Same-sex flies were pooled, and the
sex ratio (female:male) was calculated. The total progeny yielded by each
female was also noted. One week after mating, isolated female flies were
transferred and pooled by groups of 810 in a fresh food vial, according
to experimental treatment. Females were transferred to a new food vial every 5
days, and the number of survivor(s) was noted at each transfer.
Statistical analysis
The homogeneity of distribution between samples was tested using a
2 test with a Yates correction. Treatments were compared using
Student's t-test or ANOVA (for one condition over three groups or two
conditions over two groups). The two-by-two comparison between the samples was
performed with a post-hoc PLSD Fisher test (significance taken as
P<0.05). A simple regression analysis was carried out to test the
significance of CH ratio and mating preference between 16 independent
groups.
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Results |
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Effect of Cs female cuticular hydrocarbons on mate choice by Cs males
In each choice test, two mutant females (one perfumed and one non-perfumed)
competed for a single Cs male. Out of 250 tests, the first mating occurred
more often with a perfumed female (N=163) than with a non-perfumed
female (N=87; P<0.0001; binomial test). During the 1 h
period, a second mating occurred with a perfumed female in 66 cases and with a
non-perfumed female in 74 cases.
To test for possible doseresponse effects of Cs female CHs on mate
choice, we changed the number of `donor' Cs females relative to
desat1 mutant `receiver' females. Depending upon the donor:receiver
ratio, between 90 and 570 ng of 7,11-dienes were transferred (350 ng in
Cs females). The highest but non-significant correlation (P=0.21) was
noted when the unsaturated:saturated CH ratio was plotted against the relative
success of perfumed females in the choice test. This indicates that the
relative abundance of Cs female CHs induced no doseeffect response in
male preference.
In non-choice tests, Cs males also copulated more frequently with perfumed
(88.7%; N=283) than with non-perfumed mutant females (77.5%,
N=227; P=0.0012; 2=10.71).
Effect of Cs female cuticular hydrocarbons on male courtship of various strains
CHs from Cs females induced significant changes in the latency to copulate
of Cs males, which mated faster with perfumed (P=0.0056;
Table 1) than with non-perfumed
desat1 females. Conversely, males of the other strains (Tai, desat1
and four desat11573-excision alleles with different sex
pheromone discrimination abilities:
N2>D'1>E1>J2; see
Materials and methods) did not change their copulation latency, which was
similar to perfumed and non-perfumed females (and also to
desat1*Tai* perfumed females with Tai males;
P=n.s.; Table 2).
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We measured the quality of discrimination of sex pheromones in Tai males placed under red light and in the presence of two decapitated flies, one female and one male. Their simultaneous index of discrimination (SDI; see Materials and methods) was equally high with Cs and with Tai target flies (31.4±3.7 and 26.9±4.6, respectively; N=40). These values are close to the SDI shown by Cs males toward homotypic flies (33.9±5), indicating that both Cs and Tai males can discriminate sex-specific chemical signals, unlike mutant desat11573-1 males, which cannot discriminate the sex pheromones of Cs flies (F. Marcillac, Y. Grosjean and J.-F. Ferveur, unpublished observations).
Effect of female cuticular hydrocarbons on copulation duration
In choice experiments with a single Cs male, CHs of donor Cs females
induced a strong effect on the copulation duration (i.e. the time from the
latency to copulate until disengagement) between `first mating' females:
copulation lasted longer with perfumed than with non-perfumed females
(P=0.0003; Table 1).
Moreover, a weaker effect (although non-significant) was also detected on the
copulation duration of `second mating' females.
In the no-choice experiment, the CHs of Cs females clearly increased the duration of copulation in males of most strains. The copulation of Cs males lasted longer with perfumed female than with non-perfumed desat11573-1 females (P<0.0001; Table 1). Tai males also copulated longer with perfumed desat1*Cs* and desat1*Tai* females than with non-perfumed females (P<0.0001; Table 2). Males with the four excision alleles (N2, D'1, E1 and J2) also increased their copulation duration with perfumed females (0.0006<P<0.0001), but not desat11573-1 males (P=n.s.).
Effect of cuticular hydrocarbons from Cs females on the number and sex ratio of the progeny
Given that the CHs of Cs females increased copulation duration, we measured
the consequence of this variation on fertility and noted the number of female
and male adult offspring for each mated female, according to her CH status.
The CHs of Cs females induced no effect on the fertility of all tested
desat1 females (0.896 and 0.878, respectively measured for 365
perfumed and 337 non-perfumed females; P=n.s.). However, the
fecundity was significantly reduced in perfumed females compared to
non-perfumed females, in both non-choice and choice tests. In non-choice
tests, perfumed females produced significantly fewer daughters than
non-perfumed females (P=0.016;
Table 3) whereas male progeny
did not change. When first and second-mating females used in the choice
experiment were pooled, female CHs had a significant influence on fecundity
(P=0.0268; d.f.=388; t=2.22). These perfumed females
produced 20% fewer viable daughters and their sex ratio was significantly
lower (P=0.034; t=2.12) than in non-perfumed females
(respectively, 0.978±0.046 and 1.16±0.083). A two-way ANOVA
showed a significant interaction between the two factors (CH transfer and
mating rank) and revealed that the CH effect on female progeny was only
significant for `second-mating' females (P=0.0045; d.f.=137;
t=2.88). The difference in sex ratio between second-mating females
was only just non significant (P=0.062; d.f.=137; t=1.88),
with a tendency towards an excess of female offspring in non-perfumed females
(1.26) as compared with perfumed females (0.95).
|
The total progeny (daughters + sons) was slightly different (P=0.0318) for second-mating females, probably because of the variation in daughter offspring.
We also measured (i) the frequency of female remating 14±1 days after the first mating, and (ii) the survival of mated females, and found no significant effect of CH transfer (data not shown).
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Discussion |
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Although the stimulatory effect of 7,11-dienes on male wing vibration was
shown more than two decades ago (Antony and
Jallon, 1982), this is the first demonstration that 7,11-dienes
can increase the frequency and rapidity of Cs males to mate. Furthermore, we
show that moderate amounts of female CHs are sufficient to elicit a maximal
mating response because no doseresponse effect was detected. This
indicates that the threshold of detection by Cs males is low. This hypothesis
is supported by the findings that a small amount (
50 ng) of 7,11-dienes
can elicit a high courtship response in another 7-T rich male (55B-Gal4;
Ferveur and Sureau, 1996
), and
that increased amounts of 7,11-dienes acquired by transfer did not increase
male courtship in 7-P-rich Tai and in 7-T-rich Ives strains
(Coyne et al., 1999
). However,
our study did not mix the CHs of two wild-type strains, or of flies of both
sexes, but instead replaced the unsaturated CHs that were quasi-absent in
mutant desat1 females.
There are several reasons why 7,11-dienes are often found in much higher
levels than necessary to stimulate courtship and mating of homotypic males.
These substances play a strong role in sexual isolation by preventing male
interspecific courtship and copulation
(Coyne and Oyama, 1995;
Savarit et al., 1999
) and also
have a role in sexual selection (this report). It is possible that large
amounts of 7,11-dienes are the result of a runaway selection process, as shown
for secondary characters as pheromones in many organisms
(Wyatt, 2003
). CHs acting as
sex pheromones that reinforce mate recognition were shown to be selected in
other Drosophila species (Higgie
et al., 2000
). Finally, the dienes present on D.
melanogaster cuticle have long carbon chain-lengths that could serve to
reduce desiccation in warmer drier environments
(Gibbs, 1998
).
Surprisingly, the same set of female pheromones acted on copulation termination: the CHs of Cs females increased the copulation duration of all males except for desat11573-1 mutants. This absence of effect indicates that the desat1 mutation can also alter male perception of sex pheromones during copulation. We do not know how the male fly perceives female pheromones during mating, but the difference between Cs and variant strains suggest that the system of perception of female pheromone(s) during copulation differs from that required during courtship. Alternatively, it is also possible that the substances perceived before and during copulation are not identical and that both sets of pheromones are absent in mutant desat1 females.
One possible consequence of the variation for copulation duration was the sex ratio effect. The presence of Cs female pheromones was correlated with decreased frequency of daughters in the progeny fathered by Cs males. A similar tendency towards a male-biased sex ratio was noted in the progeny from matings between desat1 females and Tai males (1.55±0.34 and 0.88±0.13, respectively, for non-perfumed and perfumed; P=0.034; d.f.=39; t=2.22). Moreover, when the sex ratio obtained individual desat1 mutant females mated with Cs males was plotted against the duration of copulation of each pair, the regression analysis showed a slight negative correlation (P=0.0129; d.f.=494.1; F=6.224). This indicates that the relative number of females decreased slightly in the progeny of parents with longer copulation durations.
Similar effects have been found in cockroaches. The manipulation of cues
involved in male social dominance in the cockroach Nauphoeta cinerea
allowed females to discriminate between male cues, but these females produced
fewer male progeny than randomly mated females
(Moore et al., 2001). We found
a reciprocal situation in Drosophila: the manipulation of female
pheromones increased the propensity of male mating and tended to decrease
female viable offspring. Given that in both species the homogametic sex is
female, the gender difference observed between the two sets of results could
be a consequence of the subsocial interactions that exist in cockroaches but
not in flies. Although we have no experimental evidence to explain sex ratio
variation, it is possible that a longer copulatory contact facilitates the
transfer of substances that will favour egg fertilization by the spermatozoa
carrying a Y chromosome (and yielding male offspring).
The interpretation of some of the data obtained in the choice experiment is less straightforward, probably because of the interaction between the two competing females. A biological dose of 7,11-dienes transferred on mutant females highly increased their probability of mating first with a Cs male. The fact that the copulation latency with the first mating female (irrespective of her CHs) was very similar to that shown by perfumed females tested in the no-choice experiment indicates that Cs males were initially aroused by the presence of some Cs female pheromones, without distinguishing the perfumed female. Later during courtship, and before copulation, males could distinguish the pheromones of both females by gustatory contact. On the other hand, the effect of female CHs on the sex ratio of the progeny was only detected with second mating females. Given that the time interval between the two matings was relatively short (13.2±1.8 min), it is possible that the female pheromones that were perceived during the first copulation persisted long enough on male receptors or on his cuticle to influence his second mating.
Role of desat1 on the evolution of pheromonal communication
The desat1 gene may play an important role in the evolution of
Drosophila pheromonal communication because when it is mutated,
several reproductive characters are altered, including (i) the production of
female and male pheromones (Marcillac et
al., in press), (ii) male discrimination of these pheromones,
(iii) genital disengagement after copulation (F. Marcillac, Y. Grosjean and
J.-F. Ferveur, unpublished observations) and (iv) male perception of female
pheromone during copulation (this report). Given that desat1
expression can be detected in specific regions of the antenna, legs and
proboscis, which probably detect pheromones during different phases of mating
(Robertson, 1983
;
Boll and Noll, 2002
), and that
the desat11573 alleles studied here showed different
effects on the various pheromonal phenotypes (this report; F. Marcillac, Y.
Grosjean and J.-F. Ferveur, unpublished observations), it is possible that the
variable expression of desat1 in these chemosensory organs affects
specific components of male pheromonal perception. We do not know whether the
strong genetic linkage between pheromonal emission and perception is a
situation exceptional to Drosophila, but it has not yet been found in
other species such as the well-studied European corn borer moth Ostrinia
nubilalis, where the production and the perception of sex pheromones are
controlled by distinct genes (Loefstedt et
al., 1989
).
Together with abnormal male perception and discrimination of sex
pheromones, the natural variation of female pheromones could reflect
intraspecific variation for expression of the desat1 gene. This view
is partly supported by the incipient speciation process discovered in Zimbabwe
strains of D. melanogaster (Wu et
al., 1995), which seems to be related to a mutation in the
desat2 gene (Fang et al.,
2002
). Like Zimbabwe, Tai is a variant strain in which females
produce low levels of 7,11-dienes and high amounts of 5,9-dienes
(Takahashi et al., 2001
). Tai
and Cs males are already known to differ in their response to CHs (probably
7-pentacosene), and the genetic factors responsible for this polymorphism have
been mapped to limited regions of the chromosome III
(Sureau and Ferveur, 1999
;
McMahon et al., 2002
),
including some of the candidate genes that affect male discrimination and/or
responses to female signals during courtship
(Ting et al., 2001
).
In the present study, we found that Tai and Cs males responded differently
to the variation of 7,11-dienes. Tai males normally detect 7,11-dienes during
copulation with an intact female (this study) and before copulation on an
immobilized female (Sureau and Ferveur,
1999). However, the fact that they did not show a faster
copulation latency with intact perfumed female indicates that Tai males do not
perceive (or react to) 7,11-dienes as early as Cs males do, whereas their
response becomes similar during copulation. This supports the hypothesis that,
as in mutant desat1 alleles, the variation for expression of
desat1 and desat2 genes in chemosensory organs of Tai males
could change specific aspects of their response to female pheromones.
We have proposed that the desat1 gene plays a critical role in the
genetic architecture underlying some of the mechanisms involved in pheromonal
communication (Marcillac et al., in
press). Here, we show that the female pheromones coded by
desat1 can influence multiple aspects of reproduction, and cause
reciprocal effects on the genes contributed by females and males that may have
a consequence in sexual conflict (Rice,
1996
). These findings support the hypothesis that desat1
finely regulates the coevolution between the sexes in Drosophila.
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Acknowledgments |
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