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Insemination Controls the Reproductive Division of Labour in a Ponerine

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Insemination Controls the Reproductive Division of Labour in a Ponerine Insemination Controls the Reproductive Division correlation between the occurrence of the two events, since the male data re- of Labour in a Ponerine Ant ported below indicate that the relation- ship is a causal one. Were ovarian ac- Chr. Peeters and R. Crewe tivity to be responsible for changes in Department of Zoology, University of the Witwatersrand, worker behaviour which lead to mat- Johannesburg, 2001, South Africa ing, we would expect to find unmated workers with developed ovaries. None The control of oviposition in insect co- frequent transfer of adults and brood have been found at any time of the lonies is fundamental to the structure between the nests along non-chemical year. Indeed we can state that the hap- of their social systems. In most ant so- trails. Workers are produced for most loid eggs which develop into males are cieties a distinct female caste performs of the year (with a hiatus in egg pro- laid by inseminated gamergates. Insem- the reproductive function, while the duction before winter) and this results ination also produced a change in the worker caste is sterile, or at the most in a nest population with individuals chemical composition of the mandibu- produces trophic or unfertilized (male) of various ages. lar gland pheromone of these ants and eggs. Winged males and virgin queens Single nests and nest complexes of in their behaviour. The mated ants re- are seasonally produced, and leave O. berthoudi were excavated at differ- mained inside their nests for the rest their nests on nuptial flights [1]. Thus ent times of the year, and a large sam- of their lives, except when they were a trend towards reproductive speciali- ple of ants from each unit was dis- carried from one nest to another. They zation and monogyny has accompa- sected. This included a sample of are removed from the normal sequence ' nied the evolution of the division of la- 100 above-ground ants which were all of age polyethism exhibited by their bour. In contrast to this, we have found found to be non-reproductive. Dissec- non-reproductive sisters. that colonies of the ponerine Ophthal- tion of 350 cocoons containing pharate Males were only active above ground mopone berthoudi reproduce by means adults never yielded any winged fe- for a few weeks of the year (February of a large number of unspecialized egg- males. In each nest there are various to the beginning of March). Every day layers. Wheeler and Chapman [2] re- numbers of egg-laying workers, all of during this period a few males left their cognized two distinct evolutionary pat- which are indistinguishable from sterile nests and flew off. They were seen to terns in the ponerines, one leading to workers by simple visual inspection. enter other nests and copulation oc- the development of wingless ergatoid These fertile workers were found to curred underground. Any ant that had (=worker-like) queens as in Lepto- have 3 enlarged ovarioles per ovary, not become active above ground prior genys, and the other associated with the with short strings of developing oo- to the period of male activity had a complete disappearance of the queen cytes and very seldom more than two high probability of becoming insemin- caste and its replacement with fertile large fully formed eggs per individual. ated and hence reproductive; this ac- workers [3]. It is the latter unusual re- The ovarian apparatus of sterile counts for the large number of garner- productive pattern to which we wish workers was the same as that of repro- gates found in the nests sampled at this to direct attention. Wheeler and Chap- ductive ones, but the 6 ovarioles were period (Table 1). Thus the sharp in- man [2] observed a normal male copu- undeveloped. Thus there are no distinct crease in the gamergate to worker ratio lating with a worker in Diacamma, a female castes. Examination of sper- seen from February to March can be genus in which there are no queens. mathecae revealed that ants with active correlated with the pattern of male ac- The fertile workers may be called ga- ovaries had been inseminated, while tivity. During the rest of the year the mergates ("married workers") to dis- ants with undeveloped ovaries had not proportion of gamergates usually de- tinguish them from ergatoids. Work on been inseminated (Table 1). These data creased through the emergence of new a number of species with gamergates demonstrate that insemination triggers non-mated ants. However, the wide [4, 5] has documented that in each col- ovarian activity. This is not simply a variations over a one-year period seen ony there may be one or more fertile workers which supply the eggs that de- Table 1. Reproductive status of individuals from a number of colonies of Ophthalmopone velop into workers and males. Many berthoudi sampled at different times of the year (see text). All gamergates* examined were features of such a reproductive system inseminated, and all workers had empty spermathecae are still unknown, e.g. how are gamer- gates differentiated, can all workers Date of No, of No. of ants % of ants checked % of mate and if so, what is the proportion excavation ants examined for insemination gamergates* of gamergates in a colony? collected in the sample Ophthalmopone berthoudi is an African gamergates* workers gamergates* workers examined species in which winged queens have never been found; it occurs in semi-arid 16. VII. 1981 247 11 111 100 51 9 regions and feeds on termites. Field ob- 5. XII. 1981 311 125 156 64 12 45 31. I. 1982 140 2 73 - 38 3 servations in Mkuzi Game Reserve, ll. II. 1982 471 11 339 91 36 3 South Africa, have shown that colonies 23. III. 1982 196 95 57 82 26 63 consist of a number of distinct nests 17. X. 1982 348 65 190 21 6 26 separated by various distances. Colony integration is maintained through the * gamergates = fertile workers 50 Naturwissenschaften 71 (1984) 9 Springer-Verlag1984 in the percentage of fertile workers per productives are now restricted to mat- Received August 11, 1983 nest or colony (see December nest; Ta- ing with a sample of the workers, ble 1) show that the numbers are not whose emergence coincides with theirs. regulated. They are a result of the The reproductive division of labour number of male visits, the number of among these workers results from in- 1. Wilson, E.O.: The Insect Societies, young ants present inside the nests dur- semination of young workers, and is p. 27, 136. Cambridge, Mass.: Harvard ing the mating period, the foundation not the consequence of a conflict over Belknap Press 1971 of new nests and the occurrence of col- reproductive fitness [11] between 2. Wheeler, W., Chapman, J. : Psyche 29, ony fission. This situation is unlike that members of a colony. Mating of males 203 (1922) found in most other polygynous ants with particular workers occurs by 3. Ward, P.: ibid. 88, 109 (1981) 4. Haskins, C., Whelden, R. : ibid. 72, 87 chance and hence cannot be affected [6]. Gamergates of the previous year (1965) have largely disappeared (see January by directional selection. This may ac- 5. Haskins, C., in: Development and Evo- and February nests; Table 1) by the count for the lack of specialization in lution of Behaviour, p. 355 (eds. Aron- time the next set of males becomes ac- the ovaries of the gamergates of son, L., et al.). San Francisco : Freeman tive, and are then replaced by a new O. berthoudi and suggests why queens 1970 cohort of inseminated workers. have not been re-evolved [12]. 6. H611dobler, B., Wilson, E.: Natur- Careful observations of laboratory col- wissenschaften 64, 8 (1977) We are grateful to D. Brothers and W. 7. Alexander, R.: Ann. Rev. Ecol. Syst. 5, onies housed in perspex-covered nests Brown for critically reviewing this have failed to reveal any evidence of 325 (1974) manuscript, and also to M. Keeping 8. Michener, C., Brothers, D.: Proc. Nat. aggressive interactions between and M. Centner. We thank B. Bolton Acad. Sci. USA 71,671 (1974) marked gamergates and workers, or for the ant identifications, and W. 9. Hamilton, W.: Ann. Rev. Ecol. Syst. 3, among gamergates themselves. This in- Brown for suggesting the use of the 193 (1972) dicates that there are no dominance term "gamergate". This work was sup- 10. Crozier, R., in: Social Insects, Vol. 1, hierarchies among the reproductives, ported by grants to the Animal Com- p. 223 (ed. Hermann, H.). New York: Academic Press 1979 and no resulting inhibition of laying or munication Research Programme from oophagy. Circumstantial evidence indi- 11. Trivers, R., Hare, H. : Science 191, 249 the University of the Witwatersrand (1976) cates that all fertile workers lay eggs and the Council for Scientific and In- at a slow rate (a maximum of 3-4 eggs/ 12. Crozier, R., in: The Biology of Social dustrial Research. We thank the Natal Insects, p. 4 (eds. Breed, M., Michener, week), and thus their cooperative Parks Board for permission to work in C., Evans, E.). Boulder: Westview Press breeding is necessary for colony main- Mkuzi Game Reserve. 1982 tenance. Our results afford an insight into a unique formicid reproductive system, one where the functional differentia- Ein neues Sinnesorgan bei Gammarus tion into fertile and sterile workers can be accounted for by mechanistic argu- E. Schwedhelm ments other than the genetic ones used Institut ffir Angewandte Zoologie der Universit~it, D-5300 Bonn in the kin selection and parental ma- nipulation hypotheses. The complete Mit einem Rasterelektronenmikroskop len Gliedern aul3er dem Dactylus; ihre loss of the queen caste undermines the der Firma Cambridge (MK II) und mit Anzahl nimmt von der Basis bis zum notion of parental manipulation [7, 8] histologischen Schnitten von 7gm Propodus kontinuierlich ab.
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