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0300-3256188 $3.00 + .OO Pergamon Press plc 01988 The Norwegian Academy of Science and Letters Zoologica Scripta, Vol. 17, No. 3, pp. 293-295,1988 Printed in Great Britain The crenellate lining of the Dufour gland in the genus Aenictus: a new character for interpreting the phylogeny of Old World army ants (Hymenoptera, Formicidae, Dorylinae) JOHAN P. J. BILLEN and WILLIAM H. GOTWALD JR Accepted 7 July 1987 Billen, J. P. J. & Gotwald, W. H. Jr. 1988. The crenellate lining of the Dufour gland in the genus Aenictus: a new character for interpreting the phylogeny of Old World army ants (Hymenoptera, Formicidae, Dorylinae) .-Zool. Scr. 17: 293-295. The Dufour gland epithelium in Aenictus has a crenellate appearance, a condition previously found only in the primarily African genus Dorylus. This character, taken alone, strongly suggests that these two genera share a common ancestry, as is presently reflected in their placement in the subfamily Dorylinae, and that an independent, convergent origin for them, as has been proposed in the triphyletic hypothesis for army ant evolution, is incorrect. Johan P. J . Billen, Limburgs Universitair Centrum, Department SBM, B-3610 Diepenbeek, Belgium. Address for correspondence: Zoological Institute, University of Leuven, Naamsestraat 59, B-3000 Leuven, Belgium. William H. Gotwald Jr, Utica College of Syracuse University, Department of Biology, Utica, NY 13502. U.S.A. Introduction Army ants are characterized by their distinct behaviour of nomadism and group predation (Wilson 1958) and by their pantropical distribution. Two major groups can be clearly distinguished on the basis of zoogeographical, morphological and ethological characteristics: the Ecitoninae in the New World and the Dorylinae in the Old World tropics (Gotwald 1982; Snelling 1979). The Dorylinae comprise two tribes, with the Dorylini (single genus Dorylus Fabricius, 1793) mainly confined to Africa and the Aenictini (single genus Aenictus Shuckard, 1840) best represented in tropical Asia. There are considerable differences, however, between the members of both tribes, especially in their external morphology. Based on these differences and on the geological interpretation of their actual geographical distribution the hypothesis of a triphyletic origin for the army ants has been advanced (Gotwald 1979). In this regard, both doryline groups have been believed to have arisen independently from each other and independently from the Neotropical Ecitoninae. Our present paper is based on the recent discovery that the Dufour gland morphology represents a valuable character to distinguish between the Ecitoninae and the African Dorylini (Billen 1985). This stimulated us to investigate the Dufour gland in Aenictus and to compare its morphology with that of Dorylus. Malaysia (Borneo), in June 1985 by one of us (WHG). Their posterior abdominal halves were fixed for 2-4 h in 2% glutaraldehyde in 50 mM sodium cacodylate buffer, pH 7.3, containing 150 mM saccharose. Tissues were kept in buffer solution until arrival in Belgium, where they were post-fixed for 1 h in 2% osmium tetroxide in the same buffer. After dehydration in an acetone series, tissues were embedded in Araldite. Double stained thin sections were examined with a Philips EM 400 electron microscope. Results The morphology of the Dufour gland is similar in the workers of all three Aenictus species investigated. The gland is a small, pyriform sac that opens in the sting base through a slit-like duct, ventral to the opening of the poison gland duct. As in other ants, the duct of each of these sting glands has its own, independent muscular supply. In the Dufour gland muscle fibres insert onto both the dorsal and ventral duct wall. The poison gland duct, on the other hand, only shows muscular insertion onto its ventral side, while the dorsal wall displays a much thickened, rigid cuticular lining (Fig. 1). The ultrastructural organization in the muscular attachment region shows the occurrence within the duct cells of bundles of microtubules that form the structural link between the adhering myofilaments and the overlying cuticle, which has a thickness of approx. 1p m (Fig. 2). The secretory part of the Dufour gland is comprised of a glandular epithelium that also lines the central reservoir space (Figs. 1, 3). The epithelial thickness is fairly constant, though it may vary from 4 to 10 p m between Material and methods individuals. Rounded or slightly ovoid nuclei occupy a basal position in the cells and have a diameter of between Worker individuals of Aenictus dentatus Forel, 1911 (Utica College COIL no. SAC-002), A . laeviceps (Fr. Smith, 1858) (SAC-009) and Aenictus 3 and 5 pm. The cytoplasm is characterized by a moderate sp. (SAC-013) were collected at Bako National Park, Sarawak, East network of smooth endoplasmic reticulum, relatively 293 Zoologica Scripta 17 294 J . P. J . Billen & W. H . Gotwald Jr Figs. I-5.-1-3. Aenictus dentatus.-I. Longitudinal section showing the Dufour gland (Dg)and the poison gland duct ( P d ) .DdDufour gland duct; MFmuscle fibres.-2. Detail of the ventral wall of the Dufour gland duct, with intracellular bundles of microtubules ( M T ) and adhering muscle fibres ( M F ) . ct cuticle.-3. Dufour gland epithelium. Note crenellate apical border and intercellular junctions mostly coinciding with intercrenellar tops (arrows). M F muscle fibres; M mitochondria; N n u c l e u s . 4 . Crenellate Dufour gland epithelium in Doryfus nigricans.-5. Dufour gland epithelium of uniform thickness in Eciton burcheffi.Figures 4 and 5 from Billen (1986). numerous mitochondria in the basal region and sometimes some small electron-dense inclusions. A few electron-lucid vacuoles with a diameter of nearly 1 pm are randomly dispersed (Fig. 3). The epithelium has a crenellate apical border. The lateral cell membranes are very much folded in the upper cell half, with the most apical part of this intercellular Zoologica Scripta 17 junction nearly always coinciding with an intercrenellar top (Figs. 1,3). As a result, the majority of the cells show an apical depression that corresponds with the narrow crenel between adjacent tops. The apical cell membrane displays a simple topography and closely adjoins the overlying cuticle, which has a uniform thickness between 0.20 and 0.25 pm ( 4 5 times Dufour gland morphology in Aenictus army ants 295 thinner than in the duct region). The basal plasmalemma shows only a very few invaginations. The gland is surrounded by a thin basement membrane (around 50 nm thick) and a few rather thin muscle fibres (Fig. 3). The Dufour gland epithelium in Dorylini and Ecitoninae is shown for comparison (Billen 1986). Species of Dorylus (and the subgenus Anomma) have a crenellate epithelium, with a very well defined sequence of crenel tops and depressions (Fig. 4). In Eciton, and later confirmed in Labidus and Neivamyrmex, the entirely different epithelium has a very uniform thickness and is characterized by a basal accumulation of lateral cell membrane foldings (Fig. 5). between the glands in Aenictus and Dorylus suggests a common origin for these two genera. This evidence supports the current placement of both genera in the subfamily Dorylinae (see Snelling 1979; Gotwald 1982), implying a common ancestry for all of the Old World army ants, a group that furthermore arose independently of the New World army ants (subfamily Ecitoninae). The crenellate condition of the epithelial lining in both Old World genera does not support the triphyletic hypothesis for the army ants proposed by Gotwald (1979) and supported by recent research on gastral exocrine glands by Jensen (1986). Although the ancestral relationships of the Old World army ants remain unclear, the results of this study imply a monophyletic origin. Discussion Acknowledgements AS in other ants, the Dufour gland in Aenictus is formed by a reservoir sac, lined with a secretory epithelium, and a slit-like duct. The latter contains an extensive muscular apparatus that allows the Dufour gland to discharge its secretion independently from the poison gland (Billen 1982, 1986). The cytoplasmic organization of the glandular cells corresponds with that of the Dufour gland in other ant species and is in accordance with the production Of low weight lipophilic substances k Quennedey 1974; Billen 1986). No information is available on the chemical composition of the Dufour gland in Aenictus nor on its function. It is probably involved in secretion of hydrocarbons with an eventual pheromonal function, as is common among the Formicidae (Blum & Hermann 1978). The most obvious character of the gland in Aenictus is the crenellate aspect of its epithelial lining and the coincidence of intercellular junctions with the intercrenellar tops. This particular condition is all the more remarkable, because it is most similar to that of the Dufour gland in the other Old World army ant genus Dorylus. No other ant species investigated thus far shows a comparable epithelial type, as was revealed by ultrastructural examination of 60 species representing the 8 major subfamilies among the Formicidae (Billen 1986). Given the Dufour gland’s apparent systematic importance in the ants in general (Billen 1986), and the army ants in particular (Billen 1985), the striking similarity We are grateful to EIS Plaum for technical assistance in sample preparation for electron microscopy. JPJB thanks the Belgian National Fund for Scientific Research for a senior research assistantship. The research contributions of WHG were supported by National Science Foundation (U.S.A.) grant BSR-8403385. References Billen, J. 1982. The Dufour gland closing apparatus in Formica sanguinea Latreille (Hymenoptera, Formicidae).-Zoomorphology 99: 235-244. Billen, J. 1985. Comparative ultrastructure of the poison and Dufour glands in Old and New World army ants (Hymenoptera, Formicidae).-Actes Coil. lnsectes Soc. 2: 17-26. Billen, J. 1986. Comparative morphology and ultrastructure of the Dufour gland in ants (Hymenoptera, Formicidae).-Ent. gen. 11: 165-181. Blum, M. S. & Hermann, H. R. 1978. Venoms and venom apparatuses of the Formicidae: Myrmeciinae, Ponerinae, Dorylinae, Pseudomyrmecinae, Myrmicinae, and Formicinae. In Arthropod venoms (ed. S. Bettini): 801-869. Springer Verlag, Berlin. Jessen, K . 1987. Gastral exocrine glands in ants-functional and systematical aspects. In Chemistry and biology of social insects (eds J. Eder & H. Rembold): 445446. J. Peperny Verlag, Miinchen. Gotwald, W. H . 1979. Phylogenetic implications of army ant zoogeography (Hymenoptera: Formicidae).-Ann. ent. Soc. Am. 72: 462467. Gotwald, W. H. 1982. Army ants. In Social insects 4 (ed. H. R. Hermann): 157-254. Academic Press, New York. Noirot, C. & Quennedey, A. 1974. Fine structure of insect epidermal glands.-A. Rev. Enf. 19: 61-80. Snelling, R. R. 1982. Systematics of social Hymenoptera. In Social insects2 (ed. H. R.Hermann): 369453. Academic Press, New York. Wilson, E. 0. 1958. The beginnings of nomadic and group-predatory behavior in the ponerine ants.-Evolution 12: 24-31. Zoologica Scripta I 7