Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Revisited Roles of Drosophila Female Pheromones
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
Correspondence to be sent to: Jean-François Ferveur, e-mail: jean-francois.ferveur{at}u-bourgogne.fr
Key words: co-adaptation, 7, 11-dienes, Drosophila, mate preference, sex pheromones, sexual isolation
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Introduction |
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 Top Introduction ResultsConclusionReferences |
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Chemical signals, or sex pheromones, are often required for the rapprochement of sex partners and to elicit or prevent courtship and reproduction (Wyatt, 2003
). In many invertebrate species, sex
pheromones are a part of complex mixtures because they are often associated with (or made
of) multiple components inducing different effects (Cardé and Minks, 1997). The precise pheromonal
influence of the various components of a complex bouquet is difficult to determine in
live animals because the experimental methods involved in isolating and testing are
invasive and do not parallel the ‘in vivo’ situation. Drosophila
melanogaster is a favorable species to study pheromonal communication because the
comparison of live transgenic flies producing various blends allows the evaluation of the
‘in vivo’ role of the pheromonal components that vary. Another
non-invasive method allows for the ‘perfuming’ of flies by passive transfer
of pheromones between flies of different genotypes (Coyne et al., 1994).
In D. melanogaster females of most strains (such as Canton-S = Cs),
two cuticular hydrocarbons (CHs) are quantitatively predominant [7,11-heptacosadiene
(7,11-HD = 400 ng) and 7,11-nonacosadiene (7,11-ND = 200 ng)]
(Antony and Jallon, 1982;
Antony et al., 1985).
However, females of the variant strains collected in Caribbean and sub-Saharan areas
produce much less 7,11-dienes (<100 ng;
Ferveur et al., 1996). The
genetic and molecular bases of this variation, together with its possible evolutionary
and adaptative implications, were recently revealed (Coyne et al., 1999;
Takahashi et al., 2001;
Fang et al., 2002;
Greenberg et al., 2003).
These substances may play a role in sexual isolation because they are present in
D. melanogaster and D. sechellia females, but not in females of
the two closely related species D. simulans and D. mauritiana
(Jallon and David, 1987).
Two studies carried out with the two transgenic female genotypes, hsp70 x
UAS-transformer (hs-tra) and desat1, which respectively produce no
or low amounts of 7,11-dienes (Savarit et
al., 1999;
Marcillac et al., 2004)
revealed the multiple roles that these pheromones play in inter- and intraspecific male
courtship and mating.
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Results |
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TopIntroductionResultsConclusionReferences |
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7,11-Dienes strongly prevent interspecific male courtship and mating
Flies with relatively high levels of 7,11-dienes induce no or very low courtship in
D. simulans males, indicating that these substances are involved in reproductive
isolation (Coyne et al.,
1994;
Coyne and Oyama, 1995). The strong
inhibitory role of D. melanogaster female pheromones to D. simulans and
D. mauritiana males, but not to D. sechellia males, was clearly
shown with hs-tra females that were, or were not, perfumed with dienes
(Savarit et al., 1999).
To measure the threshold of inhibition, mutant desat1 D.
melanogaster females that were, or were not, perfumed with female pheromones of the
control Cs strain were tested with males of three species (Table
1). The difference between
non-perfumed and perfumed females [with, respectively, 46 ± 5 ng (n
= 26) and 108 ± 12 ng (n = 34) of 7,11-dienes] was
apparently detected by D. mauritiana males that courted and mated more often
with non-perfumed than with perfumed desat1 females. Both frequencies of male
courtship and mating were apparently lower than those induced by totally deprived females
(hs-tra;
Savarit et al., 1999)
suggesting that D. mauritiana males are dose-dependently inhibited by quantities
of 7,11-dienes ranging between 0 and 100 ng. Conversely, D. simulans males could
be more sensitive to these substances because they were completely inhibited by
non-perfumed females.
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7,11-Dienes are not required to induce intraspecific male courtship and mating behaviors
Early experiments performed with natural fractions of CHs extracts tested on dead
dummies suggested that 100 ng of 7,11-HD and 400 ng of 7,11-ND can induce the maximum
excitation in Cs males (Antony et al.,
1985). A study with living sex mosaic flies producing variable mixtures of
female and male predominant CHs, suggested that <30 ng 7,11-dienes can elicit the
maximal male courtship intensity (Ferveur and
Sureau, 1996).
The hypothesis that 7,11-dienes are not required to induce strong male courtship was
clear when intact hs-tra females (totally deprived of 7,11-dienes) and Cs
females induced a similarly strong excitation in Cs males (Savarit et al., 1999). However, male flies mated
less often (–25%) with intact hs-tra females and directed a weaker
courtship (–30%) to decapitated hs-tra females if compared to
control females. This suggests that the multiple sensory signals emitted by intact
females could make up for the absence of 7,11-dienes; nevertheless, these substances seem
to increase male propensity to mate.
7,11-Dienes enhance mate choice between homotypic partners, without any dose-dependent effect
To clearly assess the role on mating of female pheromones, live desat1
females were or were not perfumed (by crowding with Cs donor females) with 7,11-dienes.
In both choice and non-choice experiments (carried out, respectively, with two or one
desat1 females and one Cs male), perfumed females mated more often than
non-perfumed desat1 females. Moreover, Cs males, but not Tai males, mated faster
with perfumed than with non-perfumed females (Marcillac and Ferveur, 2004).
To measure for dose-dependent effect of 7,11-dienes, the ratio between donor Cs and receiver desat1 females was changed. Choice tests involving a Cs male with both a non-perfumed female and a perfumed female (carrying between 90 and 570 ng of 7,11-dienes) showed no dose effect for female preference and mating speed.
The presence of 7,11-dienes is correlated with increased copulation duration and decreased sex-ratio of the progeny
The transfer of Cs female’s pheromones on mutant desat1 females
increased their copulation duration with Cs and Tai males. Furthermore, the presence of
7,11-dienes and longer copulation duration were both associated with a decreased
production of female offspring in mating tests with Cs males. Perfumed females
significantly produced fewer daughters, but a similar number of sons, than non-perfumed
females. Therefore, the sex ratio in the progeny of perfumed females was biased towards
an excess of sons whereas that of non-perfumed females was close to one. Moreover,
individual females with the higher proportion of daughters showed the shorter copulation
durations (Marcillac and Ferveur,
2004). These findings suggest that female pheromones cause reciprocal effects
on the genes contributed by females and males that may have a consequence in sexual
conflict (Rice, 1996).
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Conclusion |
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TopIntroductionResultsConclusionReferences |
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The predominant cuticular hydrocarbons (CHs) of D. melanogaster female (likely 7,11-dienes) play a much more complex pheromonal role than hitherto suspected. According to their quantity, these substances play a dual role on male inter- and intraspecific mating behavior. Less than 100 ng can efficiently prevent male interspecific mating and strongly reinforce sexual isolation. More than 100 ng of 7,11-dienes are sufficient to regulate several aspects of intraspecific mating, with strain differences. If these female pheromones did not increase the overall intensity of male courtship, they enhanced both mating speed and frequency, at least in homotypic situation. The fact that a large majority of males prefered to mate first with a perfumed female can explain the selection of the factor(s) coding for these pheromones. Females of many strains produce amounts of dienes that largely exceed the threshold required for mate preference and it is not yet clear whether increasing doses of female pheromones can proportionally increase copulation duration and decrease the number of daughter in the progeny. The high level of female pheromones could also reflect the fisherian selection process of this secondary sexual character (Fisher, 1930
), or serve as a yet unknown signal during
inter-individual communication both at strain and at species levels. Finally, the
significant role played by 7,11-dienes on various sequences of reproduction that occur
before, during and after mating suggest that these pheromones help to finely adjust the
co-adaptation mechanisms between the sexes.
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References |
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TopIntroductionResultsConclusionReferences |
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Cardé, R.T. and Minks, A.K. (eds) (1997) Insect Pheromone Research: New Directions. Chapman & Hall, New York.
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Coyne, J.A., Crittenden, A.P. and Mah, K. (1994) Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science, 265, 1461–1464.
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