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Rhytidoponera Sp InSectes Sociaux, Paris Masson, Paris, 1987 1987, Volume 34, n ~ 2, pp. 75-86 THE REPRODUCTIVE DIVISION OF LABOUR IN THE QUEENLESS PONERINE ANT RHYTIDOPONERA SP. 12 C.P. PEETERS School of Zoology, University of New South Wales, P.O. Box 1, Kensington N.S.W., Australia 2033 Re~u le 15 octobre 1986 Accept6 le 9 mars 1987 SUMMARY Mated workers have replaced the queen as the functional egg-layers in several species of ponerine ants. In such queenless species, the reproductive status of workers can only be determined through ovarian dissections. However, the presence of yolky oocytes is not necessarily an indication of active egg-laying. In Rhytidoponera sp. 12, a substantial proportion of the workers confined under, ground have many large yolky oocytes in their ovaries. Examination of various details of oogenesis (size and appearance of basal oocytes,...) revealed that oocytes do not mature in unmated workers, and that they accumulate in the ovaries. In the 21 mated workers found in a colony excavated in October 1985, there were fewer large yolky oocytes, and the dense accumulations of yellow bodies indicated that eggs were laid regularly. Thus reproductive differentiation among the workers is controlled by insemination. The lack of egg-laying activity by unmated workers was confirmed by monitoring brood production in the laboratory. Trophic eggs do not seem to exist. Various characteristics of worker reproduction in ponerine ants are discussed. RESUME La division des rSles reproducteurs chez Rhytidoponera esp~ce 12, une fourmi Pon6rine sans reine Des ouvri6res fdcond6es ont remplac6 la reine (darts sa fonction de pondeuse) chez plusieurs esp6ces de fourrnis pondrines. Darts ces esp~ces sans reine, l'6tat reproductif des ouvri6res ne peut 6tre d6termin6 qu'avec la dissection des ovaires. Cependant, la prdsence d'ovocytes en vitellogen~se n'indique pas n6cessairement qu'il y ait ponte d'o~ufs. Chez Rhytidoponera esp6ce 12, une grande proportion des ouvri6res actives ~t l'int4rieur du nid ont beaucoup d'ovocytes en vitellogen6se darts leurs ovaires. L'examen de certains d6tails de l'ovogen6se (talUe et apparence des ovocytes basaux..) a d6montr6 76 C.P. PEETERS que les ovocytes ne mflrissent pas chez les ouvri~res non f6cond4es, et qu'ils s'accumulent dans les ovalres, Chez les 21 ouvri~res f4cond4es trouv4es dans une colonie d4terr6e en Octobre 1985, il y avait moins de gros ovocytes en vitellogen~se, et les accumulations denses de corps jaunes indiquaient que les ceufs 4taient pondus r6guli~rement. Donc la s6paration des r61es parmi les ouvri~res est contr616e par la f6condation. L'absence de ponte par les ouvri6res non f4cond4es a 4t4 confirm4e par 1'4tude du d4veloppement du couvain darts des groupes de fourmis au laboratoire. Les 0eufs trophiques ne semblent pas exister. Certaines caract4ristiques de la reproduction ouvri~re chez les fourmis pon4rines sont discut4es. INTRODUCTION The queen caste does not exist in various species of ants belonging to the sub-family Ponerinae, and ilthe reproductive function is perforce carried out by the workers. In OphCtialmopone berthoudi, egg-laying is restricted to the mated workers, and these produce both workers and males (PEETF.RS and Cm~wv., 1985a). Thus insemination controls the reproductive division of labour. In contrast, PAMILO et al. (1985) reported that, in Rhytidoponera sp. 12, a majority of the workers (both mated and unmated) exhibit ovarian activity, and that mated workers have less active ovaries than unmated workers from deep regions of the nests. This then implies that unmated workers also lay eggs, although PAMILO et al. concluded that these unfertilized eggs may have atrophic function. CROZIER et al. (1984) used allozyme data to establish the presence of h number of egg-layers in colonies of Rhytido- ponera sp. 12. This paper aims to highlight the difficulties involved in the assessment of reproductive activity in ponerine worker societies, where the mated egg- layers (= gamergates, PEETERS and CREWE, 1984) are morphologically iden- tical to their infertile nestmates. MATERIAL AND METHODS The population of Rhytidoponera sp. 12 ANIC studied (from Fowler's Gap Research Station, western New South Wales) is the same as that described in CROZIER et al. (1984) and PAMILO et al. (1985). An exceptionally populous colony was excavated on 7 October 1985, and the inhabitants were collected in groups according to the areas of the nest in which they had been found (jig. 1). During theevening prior to the nest excavation, workers present outside the nest entrance were collected separately. In addition, 17 foragers active over the previous days had been colour-marked. Due to time limitations, only a sample of this colony was dissected (table I). Only 10 of the " above ground " workers were dissected, but additional workers active in an identical context (including foragers) were collected in April 1986 and dissected. While DIVISION OF LABOUR IN RHYTIDOPONERA 77 20 MOUND ground layer li< oha er -20 im I~ chamber 2 -40 I I shaft " chamber -60 11 i~, chamber 3 Fig. 1. -- Schematic cross-section of the nest excavated on 7 October 1985. Fig. 1. -- Coupe sch6matique au travers du hid d6terr4 le 70ctobre 1985. all the workers from chamber 2 were dissected, the shaft chamber was not sampled. Two sampling procedures were used to estimate the total number of gamergates in the remaining groups: (1) random - workers from chamber I were mixed together in a container and half of them were taken and dissected. (2) subjective - workers from chamber 3 were selected for dissection on the basis of their behaviour (e.g. active in the open, or confined to dark areas). The ants were kept in a laboratory nest consisting of a sheet of red perspex lying on top of a depression in soil; they were fed on meal- worms and honey water. Notes were made on the pattern of oocyte development in each worker dissected, and the spermathecae were examined in part of the sample. RESULTS A large proportion (82 %) of ~he workers dissected (n = 296) were found to have medium--large yolky oocytes in their ovarioles. However, only 21 inseminated workers were found. During the course of the dissections, consistent differences in ovarian activity were perceived between mated and unmated workers. Eventually, a set of diagnostic characters allowed the recognition of the ovaries of mated workers without prior examination of their spermathecae. The principal criterion for recognizing mated workers was the presence of large, dense accumulations of dark-yellow inclusions at the base of the ovaries. In contrast, only tiny light-yellow inclusions were found in the ovaries of most of the unmated workers. These inclusions appear to be 78 C.P. PEETERS yellow bodies ("corpus lutea") which are produced when nurse cells (" trophocytes ") degenerate (BILLEN, 1985). This normally occurs whenever a basal oocyte passes into the oviduct, and thus the conspicuous aggregation of yellow bodies found at the base of almost every ovariole in mated workers is evidence of active egg-laying. Yellow bodies can also be produced during oocyte resorbtion (e.g. MINKENBEI~G and PETIT, 1985), and this would account for their presence in very small quantities in unmated workers. Rare ovipo- sition by unmated workers cannot be totally excluded, but was never observed in the laboratory. In addition to yellow bodies, there were distinct differences in the pattern of oocyte growth between mated and unmated workers (except in one individual). One class of workers had many large, opaque (i.e. with yolk deposits) oocytes in their ovaries; there were up to four of these oocytes in each of the six ovariotes (fig. 2). In each ovariole, the basal oocyte was markedly larger than the next yolky oocyte ; usually it was abnormally- shaped (round, not oval), and bigger than eggs collected from the nest. The yolky oocytes in each ovariole were often squeezed together, and as a result their shapes were distorted. Sometimes adjacent oocytes were fused together. Finally, the internal macrostructure of these oocytes (especially the basal ones) was abnormal; the yolk had a mottled appearance, and this became more pronounced after a few minutes in a Ringer's solution. Workers with these ovarian characteristics ,were invariably found to have empty spermathecae (n ---- 123). In contrast, there were much fewer yolky oocytes in the ovaries of mated workers, and as a result they appeared less " active ". There were seldom more than four mature basal oocytes per individual, and one or more ovarioles often contained no yolky oocytes at all (fig. 3). Mature basal oocytes had regular shapes and sizes (relative to eggs), and yolk consistency was normal. In the few ovarioles that contained two opaque oocytes, the second oocyte was markedly smaller than the basal one. They were not squeezed together, and often nurse cells could be seen in the space between successive oocytes. I conclude that the oocytes in unmated workers do not mature. They are never laid, and thus they accumulate in the ovaries giving an impression of high " activity". In mated workers however, mature basal oocytes are laid regularly, and there is a dynamic turn-over of material. Thus an ovariole without several large yolky oocytes is not necessarily less active. These results indicate that there is an association between insemination and repro- ductive activity. Many of the workers active in the nest entrances after nightfall also had ovaries with many yolky oocytes in them. All were unmated. However, foragers showed definite signs of oocyte resorbtion. In most cases, only the basal oocytes remained, and the subsequent ones had either disappeared or DIVISION OF LABOUR IN RHYTIDOPONERA 79 Fig. 2 --Cl0se,u p of a developed ovary from an unmated worker. Note that there are a few opaque oocytes squeezed together in each of the three ovarioles, and that the yolk in tttelbasal oocytes has a mottled appearance.
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