Morphology and reproductive behaviour of intercastes in the ...

Ins. Soc. 43:421-425 (1996) 1015-1621/96/040421-05 $1.50 + 0.20/0
9 1996 Birkhfiuser Verlag, Basel
Research article
Morphology and reproductive behaviour of intercastes
in the ponerine ant Pachycondyla obscuricornis
O. Dtissmann ~, C. Peeters 2,* and B. H611dobler 1
1 Theodor-Boveri-Institut, Lehrstuhl Verhaltensphysiologie und Soziobiologie der Universitiit,
Am Hubland, D-97074 Wiirzburg, Germany
z CNRS URA 667, Laboratoire d'Ethologie Expdrimentale et Compar~e, Universit~ Paris Nord,
F-93430 Villetaneuse, France
Key words: Ants, Ponerinae, morphology, reproduction, intercastes.
Summary
Queens are usually the functional reproductives in Pachycondyla obscuricornis, but none were
found in one colony collected near Brasilia. In this colony, three adults differed morphologically
from workers; although wingless, their thorax was more or less like that of winged queens (scutum
and scutellum distinct; metanotum larger than that of workers). Another 11 such individuals were
found by opening cocoons. We consider that these are intercastes (sensu Peeters, 1991). Two adult
intercastes were mated and laid eggs. In contrast, all the workers were virgin, but some laid
distinct trophic eggs which were fed to the two reproductives. Following experimental removal of
the intercastes, dominance interactions began among the workers, and reproductive eggs were
then laid. Intercastes with a reproductive function have not been reported previously in the
Ponerinae. They are distinct from ergatoid queens (permanently wingless reproductive caste) or
gamergates (mated egglaying workers).
Introduction
The morphological characteristics of reproductives are highly diverse in the ant sub-
family Ponerinae. The extent of the dimorphism between queens and workers
varies considerably between taxa, and furthermore, wingless "ergatoid" queens
have evolved from winged queens in many species (Peeters, 1993, 1997). In a few
other species a queen caste is absent and instead some workers mate and lay eggs
("gamergates"). An additional category of wingless reproductives may be the "inter-
castes", i. e. various graded stages in a series connecting workers and winged queens
(Peeters, 1991). Two essential criteria help to distinguish reproductive intercastes
from ergatoid queens: (i) phenotypic variability of intercastes within a colony;
* Author for correspondence: CNRS URA 258, Laboratoire d'Ecologie, Universit6 Pierre-et-
Marie Curie, 7 Quai Saint Bernard, F-75252 Paris 05, France.

422 Dfissmann et al.
(ii) coexistence of reproductive intercastes and winged queens, while ergatoid
queens occur instead of winged queens.
In Pachycondyla obscuricornis (tribe Ponerini), winged queens are the functio-
nal reproductives and exhibit limited morphological divergence from workers
(Fresneau, 1984; Oliveira and HOlldobler, 1991). We report that intercastes exist
and are also able to mate and reproduce.
Material and methods
The single colony described here was collected by E Oliveira in "cerrado" (transi-
tion between tropical forest and semi-arid vegetation) near Brasilia (Brazil) in July
1992. About 100 workers and eggs were found, but no queen. We observed the
colony in 1993, at which time 50 adults were present. Forty cocoons were opened to
examine the morphology of pupae. All adults were individually colour-marked and
observed directly for 32 hours (with additional video monitoring). The thoracic
morphology of adults was studied with SEM. Ovaries and spermathecae were dis-
sected to determine reproductive status. Voucher specimens have been deposited in
the Natural History Museum in London.
Results
Morphology
Three female adults differed morphologically from workers; although wingless,
their thoracic structure was more or less like that of a winged queen (mesonotum
differentiated into scutum and scutellum; metanotum larger than in workers;
Fig. 1), and they had three ocelli. Eleven partly pigmented pupae also exhibited a
similar combination of queen and worker characters (Fig. 2). We consider that they
are "intercastes" (sensu Peeters, 1991). Two of the adult intercastes differed from
the third in body size and in the relative shape of thoracic sclerites; intercaste pupae
exhibited similar variability (Fig. 2). However we could not measure the pupae
accurately, and a bigger sample of adults is needed to document within-colony
variation in size.
Reproduction
Two of the three adult intercastes were mated and laid reproductive eggs. Each had
a pair of three developed ovarioles, with dark yellow bodies occurring basally. The
unmated intercaste (which was smaller) was sterile, but her spermatheca was similar
in size to the others.
All the workers were virgin. Their spermathecae were smaller, and therefore
may not be functional. Some workers also exhibited ovarian activity (their six ova-
rioles were shorter than intercastes'), but they laid only trophic eggs (distinct in
shape, and quickly ejected from the gaster). These were immediately given to

Reproductive intercastes in a ponerine ant 423
Figure 1. Scanning electron micrographs (dorsal view) of the alitrunk of P. obscuricornis: (a) dealate queen,
(b) intercaste, (c) worker. Note the relative proportions of thoracic sclerites. Scutum and scutellum of workers
are fused. (a = pronotum; b = scutum; c = scutellum; d = mesonotum; e = metanotum)
1%....j I
Figure 2. Comparison of partly pigmented pupae of various castes, showing the thoracic sclerites of a worker,
a workerlike intercaste, a queenlike intercaste, and a winged queen

424 Dtissmann et al.
either one of the fertile intercastes, who ate them. Thus, reproduction in this queen-
less colony was monopolized by the two mated intercastes. They tended to remain
near the eggs, but walked inside the nest frequently; they never foraged.
Experimental removal of the mated intercastes triggered the production of
male-destined reproductive eggs by more than 10 workers.
Dominance behaviour
Antennal boxing occurred whenever the two reproductive intercastes met, but
neither reacted submissively, suggesting that they had equal status. Workers
were never attacked, and they did not exhibit aggression in the presence of the
reproductives. However, when the reproductives were removed, biting and jerking
began among the workers. This aggression decreased in intensity after one week.
Viable eggs were laid by various high-ranking workers, indicating that dominance
interactions regulate ovarian activity. The unmated intercaste had a low rank and
remained sterile.
When the reproductive intercastes were re-introduced (they had been isolated
with a few workers for 4 weeks, and continued to lay eggs), they were initially
attacked by high-ranking workers. After 4-5 days however, the intercastes had
regained their dominant status. When the colony was dissected (two weeks after
this re-introduction), the ovaries of the previously ovipositing workers had much
fewer yolky oocytes than those of the reproductive intercastes.
Discussion
In ants and other highly eusocial insects, female larvae develop according to either
of two developmental programs, which produce morphologically discrete forms
(queens and workers) (e. g., Wheeler, 1986). Intermediates do not exist in the vast
majority of species, irrespective of whether queens are winged or ergatoid. How-
ever adults with intermediate phenotypes occur in some ants; they result from the
expression of various queen traits during the development of worker-presumptive
larvae (or vice-versa) (reviewed in Peeters, 1991). In the subfamily Ponerinae, inter-
castes have been described in Ponera pennsylvanica (Holliday, 1903), and more
recently in Hypoponera bondroiti (Yamauchi et al., 1996). They also occur in
H. eduardi, although they were referred to as ergatoid queens (Brown, 1958: 23;
Peeters, 1991: 6) based on the limited data of Le Masne (1956).
The term "intercaste" describes a morphological state - no inference is made
about function. Intercastes can be rare and aberrant (indeed lacking a spermatheca)
in some species (e.g., Leptothorax nylanderi, Plateaux, 1970), or mate and reproduce
in others, e.g., various leptothoracines (Buschinger and Heinze, 1982), Techno-
myrmex albipes (Tsuji et al., 1991), Myrmecina graminicola (Ohkawara et al., 1993).
Some of these reproductive intercastes are able to succeed the founding queen, and
their occurrence is associated with colony fission. We have here documented the
ability of mated intercastes to reproduce instead of the queen in one colony of
Pachycondyla obscuricornis.

Reproductive intereastes in the ponerine ant 425
An important characteristic of intercastes is their morphological variability
within a species and within a colony. Thoracic structure, body size and internal traits
may vary continuously between the queen and worker extremes (Peeters, 1991).
Since queen-worker differentiation is limited in P. obscuricornis (ovariole number
is the same; Fresneau, 1984), variation among intercastes is expected to be relatively
inconspicuous, although it is apparent in the thoracic sclerites. We do not know
whether intercastes are produced in queenright colonies of P. obscuricornis.
Acknowledgements
We thank Paulo Oliveira for collecting this colony, as well as Dominique Fresneau, Diana Wheeler
and an anonymous reviewer for useful comments on this manuscript. This work was supported by
the Deutsche Forschungsgemeinschaft (Leibniz Prize to B.H.) and a Procope collaborative grant
(B.H. and C.R).
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Received 12 January 1996;
revised 26 May 1996;
accepted 10 June 1996.