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First published online February 20, 2004
Journal of Experimental Biology 207, 1085-1091 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00865
Does she smell like a queen? Chemoreception of a cuticular hydrocarbon signal in the ant Pachycondyla inversa
1 Department of Zoology, University of Regensburg, Universitaetsstrasse 31,
93040 Regensburg, Germany
2 Institute of Organic Chemistry, University of Hamburg,
Martin-Luther-King-Platz 6, 20146 Hamburg, Germany
3 Department of Experimental Ecology, University of Ulm,
Albert-Einstein-Allee 11, 89069 Ulm, Germany
* Author for correspondence (e-mail: patrizia.dettorre{at}biologie.uni-regensburg.de)
Accepted 5 January 2004
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Key words: chemical communication, fertility signal, 3,11-dimethylheptacosane, electroantennographic detection, ant, Pachycondyla inversa
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).
Evolutionarily stable signals are supposed to be costly and to honestly
reflect the characteristics of the sender (theory of `honest signalling';
Zahavi, 1987;
Grafen, 1990; reviewed in
Johnstone, 1997). Reliability
is therefore an important characteristic of signalling systems, even though
not all signals are necessarily honest
(Krebs and Dawkins, 1984;
Dawkins and Guilford, 1991;
Maynard Smith, 1994). Most
animal societies are non-clonal and this gives rise to potential and actual
conflicts over reproduction (Ratnieks and
Reeve, 1992; Johnstone,
2000). Several studies have attempted to clarify the mechanisms of
communication underlying the regulation of reproduction in social insects
(e.g. Passera, 1984;
Fletcher and Ross, 1985;
Hölldobler and Bartz,
1985; Bourke,
1988). Pheromones produced by the queen appear to inhibit workers
from producing their own sons from unfertilised eggs. There are several
interpretations of the role of the queen's pheromone. Traditionally seen as a
manipulative agent, the queen pheromone has more recently been interpreted as
an honest signal of queen's fertility, thus workers benefit from refraining
from reproduction (Seeley,
1979; Keller and Nonacs,
1993). Signalling of queen fertility can probably not be separated
from queen recognition and is expressed as a variation in the pattern of
volatile compound composition
(Hölldobler and Michener,
1980).
The occurrence of pheromones that suppress the development of worker
ovaries has been suggested for the queens of primitively eusocial bumble bees,
such as Bombus hypnorum and the parasite B. norvegicus
(Zimma et al., 2002; B. Zimma,
personal observation). The nature of this putative primer pheromone has not
been identified and its the source is still unclear
(Bloch and Hefetz, 1999).
Nevertheless, queens and workers show caste-specific volatile patterns (Ayasse
et al., 1995,
1999) and dominant Bombus
hypnorum workers, as characterized by behaviour and well developed
ovaries, possess higher amounts of volatiles and special odour bouquets that
may have a function as a recognition signal for fertility.
In highly eusocial honey bees, the queen mandibular pheromone (QMP) elicits
several behavioural and physiological responses in workers and brood (cf.
Blum, 1992;
Winston and Slessor, 1998),
including reproductive self-restraint. Recent work showed that additional
glands might be involved in signalling the queen's presence and in the
regulation of reproduction (cf.
Katzav-Gozansky et al., 2002).
However, due to their large colony size, multiple mating of the queen and the
highly complex self-organized division of labour, honey bees are probably not
representative of the majority of eusocial insects. Ponerine ants stand on the
other side of the range of advanced eusocial structures and give the
opportunity to explore the evolution of chemical communication in such social
systems. Recent studies focusing on within-colony discrimination have
identified qualitative or quantitative differences in the profiles of
cuticular hydrocarbons that are associated with age, castes and reproductive
status. For example, in the queenless ant Dinoponera quadriceps,
workers form linear dominance hierarchies, in which only the topranking
individual (gamergate) reproduces. Reproductive and social status correlates
with chemical differences: the topranking worker has a significantly higher
amount of a single unsaturated cuticular hydrocarbon (9-C31:1) than
subordinates (Monnin et al.,
1998; Peeters et al.,
1999). Similar differences between the bouquets of reproductives
and non-reproductives have been documented for several other ponerine ants
(Liebig et al., 2000;
Cuvillier-Hot et al., 2001,
2002) and for social wasps
(Sledge et., 2001). At
present, all these studies are merely correlative (but see
Dietemann et al., 2003), and
direct proof that certain compounds communicate fertility and are detected by
the workers is still lacking. The question arises as to whether substances
found to be correlated with reproductive status are indeed recognized and, if
so, whether they are reliable signals reflecting the quality of the
sender.
Our model system is the ponerine ant Pachycondyla inversa, a
species with a clear morphological difference between queen and worker caste.
Fertile queens and, in orphaned colonies, egg-laying workers of P.
inversa are characterized by the predominance of 3,11-dimethylheptacosane
(3,11-diMeC27) on the cuticle
(Heinze et al., 2002). We used
chemical analyses, i.e. gas chromatography (GC) and GC with mass spectrometry
(GC-MS), electroanntennography (EAG), GC with electroantennographic detection
(GC-EAD) and dissection of the ovaries to clarify whether the high relative
proportion of 3,11-diMeC27 in the cuticular bouquet of P.
inversa mature queens and egg-laying workers is indeed detected by
workers and whether it serves as an honest fertility signal.
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) belong to
the subfamily Ponerinae. Colonies were collected in the field from knot-holes
and rotten cocoa pods in an experimental cocoa plantation at Centro de
Pesquisas do Cacau, CEPLAC, Itabuna, Bahia, Brazil in 2001 and 2002. In the
laboratory, ants were housed in plastic boxes (19 cm x 9 cm x 9
cm) with a plaster floor, and one chamber (6 cm x 6 cm x 3 cm)
serving as nest cavity. Colonies were kept under near natural conditions
(27°C and 60% humidity, 12 h:12 h light:dark) and fed with diluted honey
and cockroaches (Nauphoeta cinerea) three times per week. The plaster
was regularly wetted.
Correlation between 3,11-diMeC27 and fertility
Mature queens from ten monogynous colonies of P. inversa were
analysed. The cuticular profile of each queen was extracted by Solid Phase
Micro Extraction (SPME), rubbing its gaster with a 7 µm polymethylsiloxane
fiber (Supelco, Bellefonte, PA, USA) and analysed by gas chromatography (see
Chemical analysis). For comparison, we similarly extracted cuticular
hydrocarbons from three founding queens, five virgin queens and seven workers
from queenless colonies (three egg-laying and four foraging workers)
(Table 1). Ants were dissected
the same day as the chemical analysis to assess the status of their ovaries.
All developing eggs present in the ovarioles were counted and their longest
length was measured under a stereomicroscope. The total egg length per
individual was calculated summing the size of all developing eggs found in the
ovarioles. Furthermore, we noted the coloration of the fat body, which darkens
from white to brownish-orange with age, as in other ants (see
Buschinger, 1968).
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To estimate the amount of 3,11-diMeC27 on the cuticle of the ants, we additionally extracted four mature queens from monogynous colonies and eight workers from queenless colonies (three egg-laying and five foraging workers) in 300 µl of pentane for 10 min. After evaporation of solvent, residues were redissolved in 50 µl of pentane containing an internal standard (n-C18) and 2 µl of this solution was analysed by GC (see Chemical analysis).
Chemical analysis
The SPME fibre or the solvent extract was injected into a gas chromatograph
(Agilent Technologies 6890N, Waldbronn, Germany) with a flame ionisation
detector, equipped with a capillary column (Rtx-5; 30 m x 0.25 mm
x 0.50 µm, Restek, Bellefonte, PA, USA). The injector was a
split-splitless type, the carrier gas Helium (flow rate 1 ml
min–1), and the temperature was raised from 70°C to
180°C at 20° min–1 and from 180°C to 280°C at
4°C min–1, then held at 280°C for 15 min. Compounds
were identified from their mass spectra, which were produced by electron
ionisation mass spectrometry using a Hewlett Packard (Palo Alto, CA, USA)
5890A gas chromatograph coupled to an HP 5917A mass selective detector (70 eV
electron impact ionisation).
Synthesis of 3,11-diMeC27
Commercially available 6-bromo-1-hexanol (Aldrich, Stanheim, Germany) was
protected as the tetrahydropyranyl derivative and transformed into the Wittig
salt by using triphenylphosphane. The Wittig reaction with 2-methylbutanal
(Aldrich), catalytic hydrogenation of the reaction product, deprotection and
Swern oxidation furnished 8-methyldecanal. In a parallel approach, commercial
heptadecanol (Aldrich) was converted to the bromide and, subsequently, to the
Wittig salt. This was methylated at the 
-position by using butyl
lithium and methyl iodide. The resulting Wittig salt was reacted with
8-methyldecanal (see above) to yield 3,11-dimethyl-10-heptacosene. The latter
was hydrogenated to yield the target 3,11-dimethylheptacosane. In our hands,
the two-step method, i.e. alkylating the Wittig salt of a primary bromide in
-position, gave much higher yields than a secondary bromide in a
one-step approach (Fig. 1).
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Detection of 3,11-diMeC27 by worker antennae
Gas chromatography with electroantennographic detection (GC-EAD)
The GC-EAD analyses were performed using a HP 6890 gas chromatograph
(Hewlett-Packard) equipped with a DB5-MS column (30 m x 0.32 mm i.d.,
0.25 µm film; J&W Scientific, Folsom, Ca, USA). The temperature was
raised from 50°C to 310°C at a rate of 10°C
min–1, using helium as the carrier gas. A GC effluent
splitter (split ratio 1:1) was used and the outlet was added to a purified and
humidified airstream, directed over the excised antenna of P. inversa
workers. The tip of the excised antenna was cut off and the antenna mounted
between two glass electrodes filled with insect Ringer solution. The electrode
holding the base was connected to a grounded Ag–AgCl wire, the electrode
at the antenna's tip being connected via an interface box to a signal
acquisition interface board (IDAC; Syntech, Hilversum, The Netherlands) for
signal transfer to a PC. The responses of the flame ionization detector (FID)
and the EAD signals were recorded simultaneously. The GC-EAD analyses were
performed first with cuticular surface extracts of P. inversa queens
and then with the synthetic compound 3,11-diMeC27. To detect
`physiologically active' compounds and to discriminate electrophysiological
responses from noise we performed 40 GC-EAD runs for each type of sample.
Electroantennography (EAG)
The antennae of P. inversa workers (N=16) were prepared
as described above for GC-EAD trials. Antennal response was expressed as total
depolarisation of the olfactory neurons in mV. Activity was amplified,
recorded and analysed using software from Syntech Company. The testing
solutions were applied on pieces of filter paper (Schleicher & Schuell,
Dassel, Germany) introduced into Pasteur pipettes heated to approximately
50°C. The odour was applied by blowing a pulse of carbon-filtered
humidified air (250 ml min–1) generated by a mechanical
stimulus air controller (Syntech Company) through the Pasteur pipette into a
tube carrying a continuous stream of carbon-filtered humidified air over the
antennal preparation. A recovery period of 30 s was allowed between each
stimulus. We tested each antenna in the following order: air (filter paper
without odour), solvent (pentane), pentane solutions of synthetic 3,11-diMeC27
(10 ng, 100 ng and 1000 ng) and 10 µl of P. inversa cuticular
extract (one ant extracted in 300 µl of pentane for 10 min). Odour
cartridges were replaced after the use of each antenna. For statistical
analysis, the amplitude of the response to the six different samples was
measured for each antenna. Data were normalized calculating the proportion (%)
of each reaction over the total amplitude and analysed by Friedman
repeated-measures analysis of variance (RM-ANOVA) and Wilcoxon test.
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The identification of the cuticular chemical profile of P. inversa
is published elsewhere (Heinze et al.,
2002). In the present study we focus attention on the variation of
a particular unsaturated hydrocarbon: 3,11-diMeC27
(Fig. 2). Mature queens
contained the highest relative amount of 3,11-diMeC27 on the
cuticle (median 44.9%; range 27.1–59.8%). Founding queens had a
considerably lower relative amount of the compound (median 5.3%; range
4.5–6.3%), as well as virgin queens with undeveloped ovaries (median
5.91%; range 3.3–16.3%). Fertile workers had high levels of
3,11-diMeC27 on the cuticle (median 30.3%; range 19–57.2%),
while foraging workers showed the lowest proportion of the compound (median
2.76%; range 2–7.4%). There is a strong positive correlation between the
total egg length (sum of the length of eggs in the ovarioles) and the
proportion of 3,11-diMeC27 on an individual's cuticle (Spearman
Rank correlation coefficient, Rs=0.82, P<0.001,
Fig. 3).
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Solvent extractions with internal standard allowed us to quantify the amount of 3,11-diMeC27 on the ant cuticle. P. inversa queens are significantly larger than workers [thorax length of queens: 4.78±0.11 mm (mean ± S.D., N=8); of worker: 3.95±0.16 mm (N=10)]. Mature queens had a higher quantity of 3,11-diMeC27 (median 5.15 µg; range 4.6–7.11 µg), while egg-laying workers had considerable less (median 0.69 µg; range 0.61–1.32 µg). Foraging workers showed a very low quantity of the compound (median 0.05 µg; range 0.02–0.09 µg).
Detection of 3,11-diMeC27 by workers' antennae
Gas chromatography with electroantennographic detection (GC-EAD)
The antennae of P. inversa workers reacted positively to the
cuticular extract of P. inversa queens. We received a strong response
for 3,11-diMeC27 (Fig.
4), indicating that this is a biological active compound that is
detected by the workers' antennae. A similar reaction was elicited using
synthetic 3,11-diMeC27. There were 21 GC-EAD runs with a good
baseline. We received a strong response for 3,11-diMeC27 in 11 runs and a
weaker response in the other runs, indicating a good repeatability of the
GC-EAD.
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Five further compounds (linear and methyl-branched alkanes and two unidentified substances) showed an EAD signal in several GC-EAD runs. However, since they can be found in small amounts only, they did not produce strong and clearly visible EAD signals. GC-EAD and EAG runs with synthetic compounds in higher concentrations have to be performed to clearly reveal if those compounds are active.
Electroantennography (EAG)
The antenna of P. inversa workers reacted to the EAG stimulation
with the six different samples. Friedman analysis of variance indicates that
the differences among the treatment groups are statistically significant
(Friedman ANOVA, Fr=16.42; P=0.006,
Fig. 5). Pair-wise comparison
showed that only the solution containing 100 ng of 3,11-diMeC27 and
the P. inversa cuticular extract elicited a response significantly
larger than the other treatments (Fig.
5). This indicates that there is probably a threshold for the
amount of 3,11-diMeC27 to be detected, since the solution
containing 10 ng of the compound did not elicit a reaction different from that
of the solvent or the air alone. On the other hand, a highly concentrated
solution (with 1000 ng) of 3,11-diMeC27 did not produce a stronger
response, presumably because of habituation of the receptors.
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), but the
absolute amount does not reach that of mature queens, perhaps due to the
smaller body size of workers. We showed that the proportion of
3,11-diMeC27 on the ant cuticle is positively correlated with ovary
development and egg production. Our results are in line with recent
correlative studies showing that ovarian activity affects cuticular compounds
in other ponerine ants (Monnin et al.,
1998; Peeters et al.,
1999; Liebig et al.,
2000; Cuvillier-Hot et al.,
2001,
2002), in bumble bees
(Ayasse et al., 1995) and
social wasps (Sledge et al.,
2001). This supports the hypothesis that 3,11-diMeC27
is a `pheromonal queen signal' (sensu
Keller and Nonacs, 1993), from
which workers can deduce reliable information about the productivity of the
queen or a worker. Workers are probably also capable of quantitatively
distinguishing between fertile, inseminated queens and fertile, uninseminated
workers, as the latter have much smaller total amount of this substance on
their body surface.
Workers need to assess the queen's fertility, since they benefit from
refraining from reproduction and helping the queen (increasing their own
inclusive fitness) only if it is mated and highly productive
(Bourke, 1988). The reliability
of cuticular levels of 3,11-diMeC27 as a signal of fertility is
based on its physiological connection with ovarian development. When there is
a direct link between a signal and some underlying aspect of the signaller's
condition, lying may be physically impossible. Physical constraint is the
simplest mechanism for the maintenance of honestly, and its effectiveness was
shown, for example, in birds displaying ornamental carotenoid colorations
(e.g. Johnstone, 1997). A
P. inversa queen or worker, with undeveloped ovaries, seems to simply
be unable to produce high amount of 3,11-diMeC27: virgin queens and
foraging workers had undeveloped ovaries and very low levels of
3,11-diMeC27. The only virgin queen producing eggs had a
proportionally high level of the cuticular compound, confirming that this is
not connected with the mating status. This suggests that workers might refrain
from reproducing in the presence of an unmated queen to whose offspring they
would be less closely related than to their own offspring. Nothing is known
about hierarchy formation and rank acquisition in colonies containing virgin
queens and workers only. Virgin queens are possibly better egg-layers and also
more capable of behavioural dominance than workers. Further studies are needed
to investigate this point.
Social insects provide a suitable model system to investigate whether
signals are honest (Zahavi,
1987; Grafen,
1990) or manipulative (Krebs
and Dawkins, 1984). It has been argued that manipulative
`pheromonal queen control' has never been demonstrated in social insects and
is difficult to explain evolutionarily
(Keller and Nonacs, 1993).
Nonetheless, in the case of P. inversa, the action of
3,11-diMeC27 as a physiological inhibitor of ovarian development
(pheromonal control over reproduction) cannot be completely excluded.
Intriguingly, in our study, the cuticular level of 3,11-diMeC27 in
founding queens stays quite low, despite their capability of laying eggs.
During the founding stage, queens do not need to communicate their fertility
since the worker caste is absent. Moreover, in one old queen (QX1),
egg-production appeared to have decreased, while the 3,11-diMeC27
level remained quite high. The fact that 3,11-diMeC27 is the
cuticular compound producing the strongest reaction of workers' antennae,
supports the persuasive hypothesis that it is a clear informative signal. The
positive correlation with egg production, and its occurrence in egglaying
workers, suggests that it is an honest signal of fertility. Further studies
are needed to clarify whether there is a possibility for manipulation in this
signalling system. As pointed out by Keller and Nonacs
(1993), worker reproduction
should decrease with increased number of queens in a colony (polygyny). More
queens would produce more pheromone and exhibit a greater control over worker
reproduction. Alternatively, if the pheromone is only an informative signal,
the number of queens should not affect worker reproduction. P.
inversa is facultatively polygynous, thus suitable for testing this
hypothesis. Occasional worker reproduction is likely to occur in queenright
colonies of P. inversa since there is evidence for worker policing by
eggeating (cf. Ratnieks,
1988). Workers of P. inversa are able to discriminate
between worker-laid eggs and queen-laid eggs. In a queenright discriminator
colony, workers eliminate eggs laid by non-nestmate workers but care for eggs
laid by non-nestmate queens (P. D'Ettorre, J. Heinze and F. L. W. Ratnieks,
personal observation). Worker-laid eggs and queen-laid eggs have a different
chemical signature, which may allow workers to discriminate between them.
Queenlaid eggs possess a significantly higher amount of
3,11-diMeC27 on the surface than worker-laid eggs, probably due to
a contamination from the cuticle to the egg-surface (cf. similar findings in
Dinoponera quadriceps; Monnin and
Peeters, 1997). This is likely to be an example of the
widespread pheromonal parsimony, with 3,11-diMeC27 serving as
fertility signal and protecting queen-laid eggs from policing.
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Acknowledgments |
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References |
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