Caryl P. Haskins and Roy M. Whelden.
"Queenlessness," Worker Sibship, and Colony Versus Population Structure in the Formicid Genus Rhytidoponera.
Psyche 72:87-112, 1965.

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"QUEENLESSNESS," WORKER SIBSHIP, AND COLONY VERSUS POPULATION STRUCTURE
IN THE FORMICID GENUS RHYTIDOPONERA
INTRODUCTION
William Morton Wheeler, in his Colony Founding Among Ants (1933). called special
attention to the fact that in a number of formicid genera, and particularly in the socially primitive subfamilies Ponerinae and Cerapachyinae, typical alate female forms have never been described. In such genera as Onychomyrmex, Eusphhctus, Acanthostich,~~, Megaponera, and Plectroctena, this normal female may be replaced by a wingless ergatogyne, intermediate in structure between queen and worker. The same condition obtains among certain species of the archaic subfamily Myrmeciinae, as Wheeler also pointed out. In some cerapachyine species, normal females typically coexist with ergatogynes, and such caste duality occurs elsewhere also. In certain respects, the shift from a "queen-like" toward a "worker- like"
form of renroductive female is curious and striking. At first -
sight it may even suggest a reversal of the trend tending to emphasize the dichotomy between more "vegetativeH and more actively "for- aging" forms which, as Wigglesworth ( 1954) and Kennedy ( 1961 ) have pointed out, is so characteristic of evolution in insects generally, whether at the level of "successive polymorphism" in the juvenile and adult phases of the individual, or of "alternative polymorphismH among adult populations of such forms as aphids, migratory locusts, and the social insects. Among the ant genera cited, however, evolution from alate to ergatoid reproductive may only superficially appear to lie in that direction, for the ergatoid is clearly at least as effective a reproductive as the winged female. In most species with such females, moreover, it seems likely that the ergatoid has been directly derived by a stabilization of a queen-worker intercaste, as Brown (1960) has suggested, and merely replaces the normal queen, with no drastic change in the general economy or structure of the colony. Even in the ponerine genus Leptogenys sens. str., where the laying female is no longer morphologically distinguishable from the worker, the course of evolution still seems relatively clear. As Wheeler (1933) pointed out, a normal female is present in the related Lobopelta langii, and 'Carnegie Institution, Washington, D.C.
'Haskins Laboratories, New Durham, New Hampshire 8 7
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88 Psyche [March
in L. ergatogyna the wingless laying female still possesses well de- veloped ocelli and a normal female thorax. In the genus Myrmecia similar series, ranging through increasing female microptery toward total aptery, can be assembled, culminating in the ergatoid-like gynes of, for instance, M. tarsata. In all these species, however, there is little evidence of any significant modification in the social structure of the colony, which remains at base a typically matrifilial community. Certain other ponerine genera referred to by Wheeler, however, may present a rather different picture. In the genera Diacamma, Streblognathus, and Dinoponera, and in some species of Rhytido- ponera, for example, distinguishable ergatogynes have not been reported. A male of a Philippine species of Diacamma has been described in copula with a form indistinguishable from a worker by Wheeler and Chapman ( 1922), suggesting that in this organism the normal reproductive may have been replaced by what is in effect a worker-producing worker. Our overall knowledge of the first three genera, however, is hardly sufficient to support even speculation about their social situations at present. For the genus Rhytidoponera, however, something more is known or knowable, and it may quite possibly represent a situation of considerable interest to the student of social evolution in the Formicidae.
The Ponerine genus Rhytidoponera comprises an extensive but relatively compact series of species inhabiting the Australian and parts of the Melanesian and Malaysian areas, ranging from New Caledonia in the east through New Guinea and neighboring parts of Melanesia to Timor, the Moluccas, and the southern Philippines in the west and occcupying a large portion of the Australian continent and of Tasmania (Brown, 1954, 1958 ; Wilson, 1958, 1959a). They are members of the widely distributed ponerine tribe Ectatommini, bearing considerable resemblance in many respects to the generalized New World tropical genera Acanthoponera and Ectatomma, as well as to the pantropical Heteroponera, with the Old World components of which they may well have shared common ancestry. The females of Ectatomma and Acanthoponera, so far known, are of the normal winged form. Those of Heteroponera may be winged or ergatoid. In at least three species of Rhytidoponera, R. impressa, R. purpurea, and R. chalybaeae, typical winged queens are the rule. Normally a single queen is found in each colony examined in the field, and com- munities appear to be initiated by isolated dealated females following a normal Ponerine dispersion and mating flight. These species are confined in distribution to well-watered and warmer areas, ranging from New Guinea and eastern Queensland rain forest southward



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19651 Haskins and Whelden - Rhytidoponera 89 along a belt down the eastern edge of Australia at least as far as south central Victoria (Brown, 1958).
In a second and much larger group of Rhytidoponera species, an exactly opposite situation obtains with respect to the queen. Many of
these species include among the largest and most conspicuous members of the genus, are widely distributed, abundant, and well known, especially in the drier areas of Australia, and have been extensively collected over long periods. Yet in none of them has a reproductive morphologically or functionally distinguishable from a normal worker ever been described.
Finally there is a third group, designated by Brown (1958) the Rhytidoponera metallica complex, which may be the most interesting from the standpoint of social evolution. The type species is one of the most widely distributed and ubiquitous of Australian ants; an inhabit- ant of thickly populated as well as remote situations over a very large area both temperate and subtropical; and so familiar as to have been known to a wide public for many years by the popular name of "greenhead" ant. Alate typical queens of this species have been described, and are represented in limited numbers in some collections, notably that of the Harvard Museum of Comparative Zoology. Wheeler described a single dealate and possibly colony-founding female of R. inornata, a member of the complex from southwestern Australia in 1931 (Brown, 1958). Brown (1958) has described a dealate female of another related species, R. aspera, collected by H. Hacker in southeastern Queensland and also in the Harvard Museum of Comparative Zoology. A single perfect female of R. victoriae, taken by Brown at Seaford, Victoria, is in the same col- lection. But it is striking that so few typical females have been identified in a complex of species as extraordinarily abundant and well-collected. It is clear that the vast majority of colonies in nature must exist without such females.
Even more interesting is the fact that in no species of R hytidoponera, including those of the metallica complex, has a queen-worker inter- mediate ever been recorded. This could suggest that evolution to the loss of the typical female took a somewhat different course from that in the Lobopelta-Leptogenys complex or even in Heteroponera. Instead of the alate female reproductive being morphologically modi- fied toward a stabilized intermediate between queen and worker while continuing the same functional role in the colony, the original queen caste may have disappeared entirely and one or more laying workers substituted as the usual reproductives. If, as Carroll Williams (in Brown, 1960) has suggested, worker development in ants is due to a



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90 Psyche [March
precocious decline of juvenile hormone titer in the maturing larva, or if on the other hand as Brian (1959, 1961) proposes, to a sharp rise in the concentration olf ecdyson near the critical period or periods of caste determination in larval ontogeny, it seems conceivable that mutations have accumulated in evolution affecting neurosecretory products or processes or timing, such that the threshold for worker- queen determination is passed only rarely in species of the R. metallica complex, and never in many of the larger species. Alternatively, it is conceivable that dimorphic female reproductive forms originally existed, as they presently do, for example, in species of Neophyrcaces, one form being ergatoid and the other unmodified, and that further evolution resulted in the loss of the latter and so close an approxi- mation of the worker form, by the former that it is no longer dis- tinguishable except through its reproductive capacity. If the latter course has been the actual one, however, we should perhaps suspect that the fertile "workers" would be comparatively rare in the Rhyti- doponera colony, at least as rare as are the laying true queens in colonies of relatively primitive pleometrotic species. It appears, as will later be indicated, that they are in fact much more abundant. Whatever the channel of evolution at the level of individual morphology, its end result poses some intriguing questions about the direction of evolution in Rhytidoponera at the level of the society. Some years ago Sturtevant ( 1938)) and later Williams and Williams ( 1957)) emphasized the evolutionary significance of the close family relationships which typically obtain among the members of the matrifilial colony so characteristic of the higher social Hymenoptera. Very recently W. D. Hamilton ( 1964), in two important papers, beginning with Haldane's C 1955) concept of the evolutionary sig- nificance of genetically based altruistic behavior, has derived a quantity in
social evolution that he defines as "inclusive fitness." It may be regarded in certain respects as an analogue at the social level of the concept of Darwinian reproductive fitness at the level of the individu- al. Like the latter it should be found to maximize in evolution. This maximization, in the social insects, has obviously involved an extra- ordinary evolution of worker altruism, at both structural and behavioral levels. Now as Hamilton demonstrates, it can be expected that such an evolution will be positively correlated with the maintenance of close genetic relatedness among the members of a colony. In the absence of arth he no genes is, the closest genetic relation- ship between queen and worker possible in a colony is that of mother to daughter, and among workers that of siblings. The pronounced evolutionary trends toward the inclusion of but two generations in the



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19651 Haskins and Whelden - Rhytidoponera 91 colony structure and toward the restriction of fertilized reproductives in the colony to a single or a few individuals, so evident in a great number of ant species, both evidently contribute to maintaining this maximal degree of relatedness within the community. Exceptions to both trends, to be sure, are known. On the one hand, they are well illustrated by the puzzling situations explored in species of the Formica obscuriventris group (King, 1949, 1955 ; King and Sallee, 1951) and the Formica rufa group (Sturtevant, 1938; Chauvin, Courtois, and Lecompt, I 961 ) where it appears that young reproductives, even of different species, may be adopted by large colonies, thus prolonging the existence of the colony well beyond the second generation and introducing both multiple queens and what must be a remarkable degree of unrelatedness among the worker personnel of individual colonies. Exceptions to the second trend may be presented by the numerous pleometrotic species of ants, though it is still unclear, as in the Polybiine and Polistine wasps, how usually such multiple reproductives are in fact sisters, and how often or how elaborately special behavior patterns may be adapted to restricting reproduction in practice to a single dominant female, or to preventing non-sisters from coexisting in the colony. In this context, the course of social evolution in the genus Rhyti- doponera is of special interest, as is the probable degree of average relatedness among the workers of a single community of both normal and "queenless" forms. In the so-called "queenless" species, do workers in fact regularly give rise to workers? Is the same true of those species possessing functional typical queens? Is worker pro- duction accomplished in one or both groups through parthenogenetic thelytoky, so common among lower nonsocial Hymenoptera, and frequently reported in the Cape honey bee? Such thelytoky has been described in ants by several investigators over a long period of years, including Reichenbach ( I 902) , Crawley ( I 9 I 2), and Cornstock ( 1903) for Lasius niger, Haskins and Enzmann ( 1945) for Aphaeno- gaster picea and A. lamellidens, Soulie (1960) for Cremastogaster, and Otto ( 1960) for Formica polyctena, while Ledoux ( 1949, 1954) has reported extensively on a specialized social adaptation of thely- toky in the workers of Oecophylla. If such thelytoky obtains in Rhytidoponera, the pattern of relatedness among colony members might be quite different than if laying workers possess developed spermatheca and are fertilized in the manner normal to ordinary ergatoid queens, by active low-flying males from other colonies. Such males are indeed characteristic of all species of Rhytidoponera, both those possessing and those lacking typical queens. Do laying workers



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92 Psyche [March
of the "queenless" species occur only one to a colony, or are they present in some numbers? If the latter, are they commonly actual siblings, or how closely are they, on average, related? Is there a tendency, in the "queenless" species, to confine worker production to a single individual even if a number of potential worker-producers are present? If such laying workers are in fact fertilized, are their mates normally derived from the same or from other colonies? Are such workers singly or multiply inseminated? Is a single individual inseminated more than once during its lifetime? What is the average contribution of male progeny by the non-fertilized members of the colony, and how is the production of males regulated? How resistant is the genus to extreme inbreeding? Is it the rule that a proportion of each successive brood of workers brought to maturity in a colony is fertilized and that these individuals remain with the parent colony, so prolonging the life of the community well beyond the normal two generations, or do newly fecundated workers typically leave the parental nest? How indeed are new colonies normally formed? Such questions as these must be answered before any critical assessment of the direction of social evolution in Rhytidoponera can be undertaken. The results reported in the present paper, derived in the course of some ten years of investigation of the genus both in the field and in the artificial nest, represent the early stages of an obser- vational attempt to provide answers to a very few of them. SOURCE OF WORKER AND MALE BROOD IN A SPECIES OF RHYTIDOPONERA POSSESSING NORMAL QUEENS
Rhytodoponera purpurea
Rhytidoponera purpurea is a typical member of the R. impressa group, in which normal queens are characteristic. A single such queen is typically found in each colony taken in the field. According to
Brown
(1954) the species occurs in New Guinea and ranges in Australia through the rain forests of the Cairns-Atherton Tableland region of northern Queensland.
On December 27, 1963, a typical, populous colony of R. purpurea, comprising the parent female, some 250 workers, and numerous larval and pupal brood including sexual males and females, was collected near Kuranda in northern Queensland. The following day a similar colony was taken at Millaa Millaa on the Atherton Tableland. In early January these colonies were housed in a type of modified earth- containing glass Lubbock nest used throughout these investigations. The colony from Kuranda was divided at the time of nesting into several isolated groups of workers with broods of cocoons and larvae. Only one such group had access to the brood female. The colony



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19651 Haskins and Whelden - Rhytidoponera 93 from Millaa Millaa was divided into two portions, one with and one without the brood queen.
An interval was then allowed to permit
the maturation of larvae and pupae in the nests at the time of capture. In the fragments of both colonies lacking parent queens, as well as in those where the normal females were present, oviposition soon oc- curred, and fairly copious broods were shortly reared. By late March abundant pupae were present in several groups. In that month, and over a following period until mid-January, 1965, samples of cocoons were regularly withdrawn from these colony-fragments and opened, and their contained pupae scored for sex and caste. The results, in which the numbers of pupae in all the queenless fragments of Colony No. I are summed for each date, appear below: No. of Colony
Dates of Assay of Pupal and Young Adult Samples -------
Fragment Examination Workers - Males
A (Kuranda-
4/29/64 23 pupae; 3 callows 0
with parent
6/ 4/64 14 pupae; 0
female)
7/12/64 15 pupae; I callow 0
9/20/64 15 pupae 0
12/ 5/64 34 pupae 0
1/19/65 30 pupae 0
Total: 131 worker pupae ; 4 callow workers ; 0 males. B-E (Kuranda -
fragments of
colony without
brood queen)
4/29/64 0
5/10/64 0
6/ 4/64 0
7/12/64 0
9/20/64 0
12,' 5/64 0
1/19/65 0
Total: 180 male pupae; 26
47 pupae; 26 adults
3 pupae
12 pupae
10 pupae
27 pupae
34 pupae
47 pupae
male adults; 0 workers.
A (Millaa-Millaa - 4/29/64 23 pupae ; 2 callows 0 with parent 6/ 4/64 39 pupae 0
female) 6/22/64 1 pupa 0
12/ 5/64 32 pupae 0
1/19/65 29 pupae 0
Total: 124 worker pupae; 2 callow workers; 0 males. B (Millaa-Millaa -
4/29/64
3 callows* 15 pupae
fragment without 6/ 4/64 0
5 pupae
parent female)
6/22/64 0
4 pupae
9/20/64 0 8 pupae
12/ 5/64 0 14 pupae
1/19/65 0 14 pupae
Total: 60 male pupae; 3 callow workers.* *These callow workers, found fresh-hatched on April 29, 1964, almost certainly represent the final fragment of maturing brood collected with the original colony, and seem with little doubt to have been progeny of the fertilized brood female.




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Psyche [March
Thus, summing the output of the two colonies together over the period of approximately a year after observation was begun, those fragments containing a brood queen produced a total of 255 pupae which were identified as workers, 6 identifiably callow workers, and no males. Those fragments of both colonies containing workers only brought to maturity a total of 240 pupae identified as males and 26 identified young adult males, a total of 266 males. In Colony No. 2 B, three callow workers were also brought to maturity at the time of an early count. It seems a safe assumption, however, that these indi- viduals represented the final, delayed residual of queen-laid brood "inherited" from the partitioning of the colony some three months earlier.
Thus it seems very clear that in R. purpurea worker brood is entirely derived from the fertilized brood female in typical Formicid fashion. Workers, however, can produce and rear a prolific male brood, at least in the absence of the parent female. Whether the male brood which typically appears seasonally in large numbers in normal wild colonies is queen- or worker-derived, or both, is an interesting and important question for future investigation. It applies with equal cogency, of course, to the vast range of "normal" Formicid species.
SOURCE OF WORKER AND MALE BROOD IN SPECIES WHERE NORMAL QUEENS ARE RARE OR ABSENT
R hytidoponera metallica
Between December 23 and 25, 1963, a number of vigorous colonies of Rhytidopo~era metaZZica were collected at various points in the Blackall Range in Queensland, Australia, some sixty miles north and thirty miles east of Brisbane. No perfect females were found. These colonies were housed and maintained in modified glass Lubbock nests of the same design as those used for R. purpurea. After a preliminary incubation period of approximately six months, to allow brood resident in the colonies at the time of capture to mature, samples of cocoons were withdrawn at intervals', opened, and the contained pupae scored for sex and caste. Callow workers that were obviously fresh-hatched were scored at the same time. The result are given in the table below (P. 95).
Thus a total of 644 worker pupae or young adults were produced in the five "queenless" colonies of R. metallica over a period of little more than six months, and only I I males. It seems clear that worker production by morphological workers is a normal feature of this species.




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Haskins and
Dates of
Colony No. Examination
1. 7/12/64
12/15/64
1/23/65
2. 7/12/64
12/15/64
1/23/65
3. 7/12/64
12/15/64
1/23/65
4. 7/12/64
12/15/64
1/23/65
5. 12/15/64
Whelden - Rhytidoponera 95
Assay of Pupal and Young Adult Samples
Workers
Males
pupae ; 1 fresh-hatched callow 0
pupae; 13 fresh-hatched callows 0
pupae; 1 fresh-hatched callow 2 pupae
pupae
2 pupae
pupae; 36 fresh-hatched callows 0
Pupae 4 pupae
pupae 0
pupae; 6 fresh-hatched callows 0
pupae; 4 fresh-hatched callows 0
pupae 0
pupae; 28 fresh-hatched callows 0
pupae; 4 fresh-hatched callows 2
pupae; 23 fresh-hatched callows 1
Queensland appears to lie near the northern limit of the natural range of R. metdica. Ample confirmation that the same situation obtains elsewhere in its range, however, was provided by counts made from a single colony of the species taken at Sutherland, N. S. W., on June 2, 1952, and observed continuously in the artificial nest over a ten-year period. This colony contained no typical females when collected, though much later in its history so'me were produced, as will be described later. It was kept as a single unit in the standard glass modified Lubbock type of nest until July 8, 1956, when it was split into three portions, one of which perished rather shortly. The second and third were maintained in Lubbock nests until January I, 1962, when the second also died out. The third portion survived somewhat longer, but eventually perished on July 30, 1962. Throughout the ten years of observation, these two colony frag- ments were kept in closed foraging arenas, to which no males could enter from outside and from which no individuals matured within could escape. The ants established and maintained regular kitchen- middens within these arenas, outside the nests proper. The ambient humidity of the arenas was maintained low, and the contents of the middens therefore remained well preserved and readily recognizable for considerable periods. Thus periodic removal of the middens and examination of their contents could provide a rather accurate picture of the quality and type of brood produced. Until June 13, 1954 (two years after observation was begun), only workers were brought to maturity. A count of cocoon fragments accumulated in the middens at intervals during this period thus



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96 Psyche [March
offered a measure of the number of workers produced from worker parentage. Only cocoon fragments were tallied which either were nearly intact 01- which included the larval meconium, thus ensuring that each fragment represented no more than one individual.