Social experience and pheromonal perception can change malemale interactions in Drosophila melanogaster
Unité de Recherche 5548 Associée au Centre National de la Recherche Scientifique, Faculté des Sciences, Université de Bourgogne, 6, Bd Gabriel, 21 000 Dijon, France
* Author for correspondence (e-mail: jean-francois.ferveur{at}u-bourgogne.fr)
Accepted 16 December 2004
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Summary |
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Key words: social experience, homosexual courtship, aggressive behaviour, pheromonal perception, Drosophila melanogaster
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Introduction |
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Apart from sexual behaviour, Drosophila females can change their
interactions after encountering other females and show aggressive behaviour
(Kamyshev et al., 2002;
Nilsen et al., 2004
), whereas
males can display territorial and aggressive behaviours. The occurrence of
these two male behaviours overlap because territoriality often results in
aggressive interaction, and both are preferentially induced in the presence of
mated females with food (Hoffmann and
Cacoyianni, 1990
; Chen et al.,
2002
). Furthermore, during aggressive interactions, males very
often display behavioural elements similar to those observed during
heterosexual courtship (Hoffmann,
1987
; Chen et al.,
2002
). Territorial behaviour has been shown to change after
experience with conspecifics because males held in isolation act more
aggressively than males held in groups
(Hoffmann, 1990
). However, the
interpretation of these data was complicated by the presence of multiple flies
tested during an extended period of observation. Recently, the measure of
aggression was standardized with only two males allowed to fight
(Chen et al., 2002
).
Here, we tested pairs of transgenic D. melanogaster male flies
defective for one set of sensory structures potentially involved in pheromonal
perception (Xu et al., 2002).
In the absence of food and of mated females, we found that the variation of
social experience (e.g. exposure to one or several siblings) during adult life
affected the nature and strength of the behavioural interaction between two
transgenic mature males. Control males tested in similar conditions showed a
much weaker interaction.
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Materials and methods |
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Grouping procedure
After a light CO2 anesthesia, 13 h after eclosion, tester
male flies were kept either isolated or grouped with varying numbers of
same-age siblings in a fresh food vial for a controlled period of time
(x2=with one; x5=with four; x10=with nine). At the end of
the grouping period, which generally took place at 14:00 h, tester males were
individually aspirated into a fresh food vial. Males grouped until 5 days old
were isolated 1 h before the test. In Figs
1,
2,
3,
4, the `grouping period' is
shown by a black-filled bar above the histogram, and the open bar represents
the `isolation period'. To distinguish males, wing clipping equally
distributed for each treatment was performed with a small pair of iris
scissors (#14558-11; FST, Heidelberg, Germany). This operation induced no
detectable effect on male behaviour (data not shown).
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Behavioural tests
All assays were performed on 5-day-old males, 15 h after lights on
(between 9:00 h and 13:00 h). In all tests, a male was aspirated into the
observation chamber (2.8 cm diameter, 0.5 cm high). 10 min later, a second
male (for malemale interaction), or two decapitated objects (for
discrimination tests) was (were) introduced. The observation period lasted 600
s. The order in which the two intact males were introduced was randomized. We
noted the occurrence and duration of various male behaviours that included
sequences very similar to those shown during heterosexual courtship (tapping,
wing vibrating, licking and rare attempted copulation, for the two types of
tests; O'Dell, 2003) as well
as chasing and aggressive behaviours (tussling, lunging; Hoffman, 1987;
Chen, 2002
) between the two
intact males. Aggressive episodes were noted in about 5% of cases.
The total percentage of time that each male spent directing a behaviour (courtship or aggressive) is the behavioural index (BI). However, we did not take into account refusal behaviours like wing flicking and jumps that were often performed by courted intact males. For malemale interactions, we calculated the BI difference as follows: if an isolated `A' male behaved towards a grouped `B' male during a total of 120 s (BI=20), and if B acted towards A during 30 s (BI=5), the BI difference (15, in favour of A) is represented under the isolated males, between 10 and 55 (as the second bar from the left shown on Fig. 1A). When both males showed similar BIs, their BI difference was very low (or equal to `0'), and these values made up for the central bar of the histogram. For most pairs represented in the central bars of all figures (N=538), males showed either no BI (`0' for both males=67%), or very low BI (0 < BI x 10; 29%). In only 4% of the cases, at least one of the two males showed a substantial behaviour (BI>10). Males of the control Di2 and Cs strains generally showed very little physical contact, with the exception of a few brief tapping episode that occurred at the beginning of the observation period. This also explains the high central histogram bar noted for pairs of wild-type males (Fig. 4A,B). In many cases, males jumped away to avoid physical contact.
For the discrimination test, we measured the duration of courtship
behaviour directed towards each of the two decapitated sex-objects (BI1/BI2).
Decapitation of sex objects allowed us to standardize behavioural observations
and to prevent flies producing most of their acoustic signals
(Ferveur et al., 1995). Some
observations were carried out under a red light (25 W with a Kodak Safe-light
filter no. 1) to remove visual stimuli
(Boll and Noll, 2002
).
Statistics
To test for the directionality of male interactions, the BI of the two
series of confronted males were compared using a Mann Whitney test (Statview
4.0). The BIs of the two confronted flies can be considered as independent
parameters given that each male can direct or receive a behavioural action, or
not interact. The comparison between two experimental sets (each one involving
two males) was carried out with a two-factor ANOVA to evaluate the role of
social experience, and of the number of siblings or of male genotype. The
significance of the probability shown here represents the interaction between
these two factors.
For the discrimination experiment, a Student's t-test was used to compare the intensity of behaviour directed towards each sex-object, after testing the normality of the data distribution with an F test.
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Results |
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The perception of male pheromones is altered in transgenic males
The B42 transgene contains the promoter of the CheB42a
male-specific factor, which is secreted by a small number of non-neuronal
cells associated with several chemosensory hairs carried by the male frontal
legs (Xu et al., 2002).
Because B42 is potentially involved in pheromonal perception, the
discrimination of B42/Di2 males was measured towards two decapitated
control flies a female and a male that were simultaneously
presented for 10 min (Table 1).
Discrimination experiments were performed either in red light to remove all
visual stimuli or in white light. In red light, B42/Di2 males could
not discriminate the sex of control flies (P=0.19), whereas sexual
discrimination was possible in white light (P=0.015). This contrasts
with wild-type subject males, which were able to discriminate sex-object both
in red light and in white light (P<0.001).
|
Social experience decreases malemale interaction
The aim of this study was to determine whether social experience during
adult development can influence behavioural interactions between differently
exposed male flies. Social experience with sibling male(s) clearly changed the
pattern of interaction between two hybrid male flies of similar genotype
(B42/Di2) and age (5 days old). The effect of experience is revealed
by the comparison of two extreme situations (shown on the top and bottom of
Fig. 1). Fig. 1A represents the
confrontation between a male kept isolated throughout his adult life (left)
and a second male that was held grouped during his adult life with four
same-age sibling males (right). The left two bars of the histogram indicate
that most isolated males directed an intense behaviour towards grouped males
(the reciprocal situation was not observed) during the 10 min observation
period. Isolated males frequently showed behavioural sequences similar to
those displayed during heterosexual courtship: sustained unilateral wing
vibration while chasing, and attempts to lick the genitalia. In response,
grouped males often flicked both wings simultaneously and jumped away
indicating that they refused the advance of the chaser
(Paillette et al., 1991). The
central bar of the histogram indicates the absence of a strong directional
behaviour, caused by a mutual neutralization, in 27% of the pairs (see
Material and methods). The total amount of time spent in directional behaviour
(behavioural index = BI, with its mean ± S.E.M. shown above
each treatment) indicates the high activity of isolated males (56±6)
and the absence of activity in grouped males. In this case, the difference
between the BIs of the two males was highly significant (P<0.001;
see
between treatments above the central bar). By contrast,
Fig. 1Frepresents the
confrontation between two males held in isolation during all adult development
(from eclosion to test). These naive males showed strong and reciprocal
interactions consisting of courtship elements (wing extension and flickering)
sometimes combined with sequences characteristic of aggressive behaviour
(lunging and tussling; Hoffman, 1987). In this case, the BIs shown by the two
males (31±6 and 37±6) were not significantly different
(P>0.05). No difference of directionality was detected between
males and only 19% pairs showed a mutual neutralization.
To outline the period of imaginal development during which social experience with siblings can influence homosexual interaction, tester males were held with siblings for various periods of adult development. The experiments shown on Fig. 1 always involved a male raised in total isolation (left) with a second male held grouped between eclosion and 14 days of adult development. Isolated males directed a strong directional BI towards males that were grouped at least 2 days after eclosion. The behavioural directionality and the difference of BIs increased in favour of the isolated male as a function of the duration of grouping.
The number of siblings has no effect on experience
To determine whether the frequency or intensity of social experience can
influence malemale interaction, we varied the number of siblings in the
`conditioning groups' (x2, x10;
Fig. 2AD) and compared
the effect that they induced with that of x5 groups
(Fig. 1). Isolated tester males
similarly behaved towards x2 or x5 males grouped for 5 days
(Fig. 2A and
Fig. 1A; d.f.=159;
F=0.183; P=0.67). Isolated males also behaved very similarly
towards x10 and x5 males grouped for 3 days after eclosion
(Fig. 2B and
Fig. 1C; d.f.=391;
F=0.034; P=0.86). The confrontation between x2 and
x10 males grouped for either 3 or 5 days after eclosion induced weak
malemale interaction without directionality
(Fig. 2C,D). Instead, the
frequency of mutual neutralization increased with the duration of grouping
(59% for 3 days; 91% for 5 days).
The effect of experience varies with the exposure period...
The experiment shown in Fig.
2D suggests that two males grouped with siblings until the day of
the test very frequently neutralized their mutual interactions. To measure the
effect of social exposure during the days preceding the test, one tester male
grouped x5 during all adulthood was confronted with a male grouped
x5 that was isolated either 1, 2 or 3 days before the test (respectively
shown on the right and left sides of the histograms of
Fig. 2EG). Social
experience induced significant effect during the 2 days preceding the test
because 36% males isolated 1 day before the test chased constantly grouped
males. This frequency only slightly increased, together with the BIs of the
males that were isolated earlier. In these experiments, constantly grouped
males rarely chased temporarily grouped males.
...but not with its duration
To distinguish the effect of the isolation period (the lap between
isolation and test) from the effect of experience duration, males to be
confronted were grouped at different ages but isolated on the same day
(Fig. 3AE). The
frequency of mutual neutralization increased when the isolation period
decreased: neutralization was very frequent when the isolation period was
shorter than 3 days. These data also indicate that the total duration of
grouping had no influence on the directionality of malemale
interaction. Interestingly, males held during either one or 3 days after
eclosion showed low BIs that were not significantly different even if a
tendency was noted in favour of males isolated earlier
(Fig. 3F).
The effect of experience varies with male genotype
To test the incidence of the B42 transgene on the intensity and
directionality of malemale interaction, various male genotypes were
compared. Unlike B42/Di2 males (Figs
1A,
2A), no or very little
interaction was observed between grouped and isolated males of the two
wild-type strains Canton-S (Cs) and Dijon2000 (Di2;
Fig. 4). However, a significant
effect (P=0.0018) was detected between isolated and grouped Cs males.
When wild-type males were paired, they were generally very active and strongly
avoided mutual physical contact with the exception of rare and brief tapping
episodes.
B42/Cs males (containing the B42 transgene in the Cs genetic background) showed a high behavioural directionality between isolated and grouped males. However, the directionality of this interaction was weaker than that shown by B42/Di2 males raised in the same social conditions (Figs 1A, 4C; d.f.=193; F=9.773; P=0.002). Moreover, the pairing of one naive B42/Di2 male with a naive B42/Cs male induced an interaction that was similar to that observed between two naive B42/Di2 males (Figs 1F, 4D; d.f.=175; F=2.296; P=0.131). Finally, two independent transgenic lines carrying a single copy of the B42Gal4 transgene also induced a strong directional behaviour between isolated and grouped males (data not shown).
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Discussion |
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Among the parameters that contributed to social experience, the most significant was the exposure period during adult development. The highest proportion of mutual neutralization occurred when both tester males were isolated <3 days before the test. When the two males were isolated earlier, their interactions were strong but non-directional. Malemale behaviour was directional only between (1) an isolated male towards a male grouped at least during the 3 days after eclosion, and (2) a male isolated at least 1 day before the test towards a constantly grouped male. However, the total duration of the social experience and the size of the group (210 siblings) had no effect.
The fact that social exposure during different developmental periods
induced a strong behavioural directionality (between B42/Di2 males)
suggests that associative and/or non-associative learning processes could be
involved. Previous studies revealed that a 30 min exposure period induced an
experience-dependent courtship modification (EDCM) that lasted for 4 h
(Gailey et al., 1982), whereas
a 5 h longassociative training induced a change that lasted >9
days(McBride et al., 1999
).
Given that with our procedure the exposure period lasted more than 24 h and
its effect was still detected 34 days later, both learning mechanisms,
as well as a remodelling of the nervous system, could be involved. We observed
that naive B42/Di2 males strongly and mutually interact during the
grouping period (data not shown). It is possible that, after at least 24 h of
this conditioning, exposed males became habituated and avoid the sensory
signals produced by sibling males. The hypothesis of a reinforced EDCM is
consistent with the fact that the frequency of mutual neutralization increased
with the age of exposure. However, the habituation process by itself cannot
explain why exposed males showed no directional interaction and relatively low
BIs, 34 days after their isolation
(Fig. 3E,F). This relatively
long from-isolation-to-test lapse of time suggests that the quality of
malemale interactions could be affected by long-term memory involving
associative learning.
Why did social exposure produce a strong effect in males carrying a copy of
the B42 transgene, but not in wild-type males? If the two naive
wild-type males confronted in a small observation chamber systematically
avoided physical contact, it is probably because they constantly exchanged
strong aversive stimuli. The moderate but significant difference detected
between the two control strains, and also between B42/Di2 and
B42/Cs males, indicates that one or several modifier gene(s) of the
background can modulate the effect of experience. We believe that
B42/Di2 males showed much stronger physical interaction probably
because of their defective perception of inhibitory male pheromones. This
interpretation is supported by the fact that the sensory structures, where
B42 is expressed, are required to detect the pheromones of
conspecific flies (Robertson,
1983; Balakireva et al.,
1998
; Xu et al.,
2002
; Bray and Amrein,
2003
). The altered behaviour of B42/Di2 males could
result from the toxic effect of Gal4, or GFP, or of both products, in the
B42Gal4-expressing cells, causing a similar effect to the
grim gene that killed the same cells. If it is true, it means that
the B42 transgene affects a function of the targeted subset of tarsal
hairs that normally allow male flies to detect inhibitory pheromones of
conspecific males (Ferveur and Sureau,
1996
). Alternatively, could the interaction between males be the
result of their pheromonal difference after the passive transfer of cuticular
hydrocarbons during conditioning? This hypothesis can be ruled out because (1)
most hydrocarbons transferred by rub-off are eliminated from the cuticle after
few hours (Scott and Jackson,
1990
), and (2) males that were either kept with one or with nine
siblings induced no behavioural difference. Therefore, if social experience
can theoretically affect all males, its effect is better measured in males
with defective sensory perception.
Male inhibitory pheromones, which strongly prevent homosexual interaction
between wild-type males, can lead to intense fighting episodes in the presence
of mated females and food (Hoffman, 1987;
Chen et al., 2002). This shows
that male inhibitory pheromones act in a context-dependent manner, and we
hypothesize that when these substances are perceived simultaneously with
chemical signals inducing rewarding effects (female pheromone, food odors),
they can elicit malemale antagonistic behaviours. Although it remains
to be shown that sensory integration of different pheromonal inputs can change
the release of substance(s) that affect neural function, certain
neuromodulators present in the central nervous system can precisely control
male courtship and aggressive behaviours
(Yellman et al., 1997
;
Neckameyer, 1998
;
Lee and Hall, 2001
;
Baier et al., 2002
). We note
that the experimental manipulation of ß-alanine changes male aggressivity
(Jacobs, 1978
), and this
effect could be partly caused by male defective visual acuity
(Baier et al., 2002
). This
makes an interesting analogy with our data because both observations suggest
that the behavioural interaction can be changed between males that are
defective for either modality of sensory perception.
In conclusion, the strong directional interaction observed between two B42 transgenic males a naive male chasing an experienced male may result from their very different experience: the naive male courts because he is not (very) inhibited by the pheromones of the exposed male who escapes because he retains a negative experience of the repulsive signals produced by sibling males.
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Acknowledgments |
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