Jürgen Heinze and Alfred Buschinger.
Polygyny and functional monogyny in Leptothorax ants (Hymenoptera: Formicidae).
Psyche 95:309-326, 1988.

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POLYGYNY AND FUNCTIONAL MONOGYNY IN
LEPTOTHORAX ANTS (HYMENOPTERA: FORMICIDAE) BY J. HEINZE' AND A. BUSCHINGER*
The number of queens present in colonies of social insects may affect several features of colony structure, such as the relationship between workers within the nest. The high degree of relatedness of nestmates, which is thought to be one of the fundamental traits in the evolution of altruistic behavior in Hymenoptera, can be sus- tained only if all the female brood is produced by one single queen (monogyny) that has been inseminated by only one male (mono- andry).
During the last two decades numerous studies on queen number and colony structure of ants have shown, however, that in about 50 percent of all species colonies may contain several fully fertile queens (Buschinger, 1974a). Some species (e-g., Leptothorax acer- vorum or Myrmica ruginodis) are facultatively polygynous; in other species (e.g., Plagiolepis pygmaea or Formica exsecta) virtually all colonies are polygynous. Colonies of some highly polygynous spe- cies, such as Formicapolyctena, may contain thousands of queens. Polygyny may arise by the cooperative foundation of new colonies by several inseminated young females (pleometrosis), by the fusion of colonies, or by the adoption of young, inseminated females into a colony.
In some taxonomic groups, polygyny appears to be associated with ecological factors, such as patchy distribution of habitats or high instability of nesting sites (Holldobler and Wilson, 1977), and recently queen number has been interpreted as an ecologically responsive trait, explainable by a combination of kin selection and ecological elements (Nonacs, 1988). An obvious advantage of poly- gyny on the colony level is that the presence of multiple fertile 'Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.
2Institut fur Zoologie, TH Darmstadt, Schnittspahnstr. 3 D6100 Darmstadt, West Germany.
Manuscript received by the editor November 21, 1988.



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3 10 Psyche [vo~. 95
queens ensures the colony's continuation in the event of one or more queen deaths. In many monogynous species the death of the queen results in the dissolution of the colony (e.g., Oecophylla spec., Van- derplank, 1960). Polygyny, however, is not the only mechanism for queen replacement observed in ants. In some species, several dealate females may be present in a colony but only one lays eggs. Occa- sionally some of the extra females are sterile, uninseminated females that somehow missed the mating flight. Others are inseminated females, which do not lay eggs in the presence of the fully fertile queen. Tschinkel and Howard (1978) demonstrated the presence of these sterile, inseminated females in colonies of Solenopsis invicta by removing the single fertile queen. In 27 percent of the test colonies a previously sterile female began to lay fertilized eggs. The presence of sterile, though inseminated females, in addition to a fertile queen has been termed "functional monogyny." Origi- nally described by Pardi with the paper wasp, Polistes gallicus (1940; l946), functional monogyny appears to be very rare in ants. In addition to Solenopsis invicta, in which it occurs along with polygyny and monogyny, functional monogyny has so far been proven to exist only in some species of the well-studied ant tribe Leptothoracini: in Leptothorax gredleri (Buschinger, 1968a), Lepto- thorax sphagnicolus (Francoeur, 1986), and in some, if not all spe- cies of the xenobiotic genus Formicoxenus (Buschinger, 1979a; Buschinger and Winter, 1976; Buschinger et al., 1980; Francoeur et al., 1985).
With the exception of L. gredleri, which is fairly common in some populations in Bavaria (Buschinger, 1966), functionally monogy- nous leptothoracines are quite rare. Thus, more detailed studies on colony and population structure are difficult. During the past few years, however, we have collected numerous colonies of a new, func- tionally monogynous species of Leptothorax closely related to the palaearctic species L. muscorum. The taxon is to be described by A. Francoeur (Univ. of Quebec, Chicoutimi); here we again refer to it as Leptothorax spec. A (Heinze and Buschinger, 1987). This ant is common in suitable habitats throughout Quebec and the northern part of New England, and it is abundant especially on the rocky shore of St. Lawrence River near Tadoussac, Quebec. A most important trait of Leptothorax spec. A is that it has a genetically mediated queen-polymorphism, with primarily winged, gynomor-



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19881 Heinze & Buschinger -Leptothorax 311 phic females and more or less workerlike, wingless queens, called intermorphs. Intermorphic queens most probably are of the geno- type Ee and EE, whereas gynomorphs are always ee (Heinze and Buschinger, in prep.).
The small size of colonies and the ease of rearing them in the laboratory make Leptothorax spec. A an ideal ant for studies on colony and population structure and colony foundation behavior related to functional monogyny.
During our studies on L. spec. A we have gathered much data on the occurrence of polygyny in additional North American species of the subgenus Leptothorax s. str. M. R. Smith (= Mychothorax Ruzsky). In this paper we present field data and results of labora- tory experiments concerning the colony structure of Leptothorax spec. A as well as field data on related species. In addition we summarize information on mono- and polygyny in some palaearctic Leptothorax.
A total of 272 complete colonies of Leptothorax spec. A were collected in June 1983, 1985, and 1988 in Quebec (Tadoussac, La Baie, Laurentides). More than 250 additional colonies were gathered since 1979 in Quebec and adjacent areas of Ontario and Northern New England (Me.: Bar Harbor, Baxter State Park; N.H.: Mt. Monadnock). Some dozen colonies were kept alive for several breeding cycles under artificially shortened annual rhythms (Busch- inger, 1974b), in the laboratory at TH Darmstadt, and for several months at room temperature in the MCZ labs in Cambridge. Other Leptothorax, most living sympatrically with L. spec. A, were collected: L. retractus (Que.: Rouyn-Noranda; Alta.: Jasper, Banff), the presently undescribed L. spec. B (Que.: Tadoussac, La Baie, Laurentides; N.H.: Mt. Monadnock), L. spec. C (Alta.: Jasper, Banff, Kananaskis; B.C.: Yoho N.P.), and a Leptothorax species similar to L. spec. B (B.C.: Sutton Pass, Mt. Seymour, Man- ning Provincial Park).
Dissections of females and workers were carried out as described by Buschinger and Alloway (1978). Instead of killing the females by using acetic acid ethyl ether or ethanol, water with a drop of deter- gent was used in most cases, because it kills small ants faster than



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312 Psyche pol. 95
a-females
b-females
ethanol and does not affect the condition of the ovaries by dehydra- tion. The ovaries were prepared by removing the subgenital plate with a pair of tweezers under a binocular microscope at 30X magni- fication. Ovariole development, contents of the receptacle and pres- ence of corpora lutea were studied at 30X to 70X magnification. The condition of the ovaries was rated using the following classification, based on a system by Buschinger (1968a) and Buschinger and Allo- way (1978).
A-females Inseminated, fertile queens. Ovarioles are elon- gated, corpora lutea are present. In the reproduc- tive season they contain numerous eggs with white yolk deposits.
Old, inseminated females, sterile. No corpora lutea present, ovarioles are short. In gynomorphic fe- males, wing muscles replaced by fat body. Fat body usually yellow.
Young, inseminated, sterile females. No corpora lutea, ovarioles are short, sometimes they contain one or two eggs. In gynomorphic females, wing muscles not yet degenerated, fat body white. b->A-females Inseminated, sterile, but eggs in development. Ovarioles more or less elongated, no corpora lutea present.
c-females Not inseminated, sterile.
C-females Not inseminated, ovarioles elongated, containing eggs. Corpora lutea present.
Since the color of the fat body, which changes from white in younger females to yellowish in older ones, was not noted in all cases, we do not differentiate between freshly inseminated, sterile females (b) and those which have already been inseminated during a past season (a-females). Likewise, we do not differentiate between older uninseminated females and young uninseminated females, which have not yet started sexual behavior. As sexuals eclose in late June and July in most areas, inseminated females collected in June or July should all have mated already during the last years, and thus be a-females. Whereas all recently eclosed gynomorphic females are winged, it is not possible to tell this year's intermorphic females from older ones without judging the color of the fat body. Only colonies with several A-females were called polygynous; those with



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19881 Heinze & Buschinger - Leptothorax 313 supernumerary a-females in addition to one single queen were called functionally monogynous.
Isoelectric focusing in ultrathin polyacrylamid gels was carried out to estimate relationships of nestmates within some colonies, and to secure conspecifity of allopatric colonies (Heinze and Buschinger, 1988).
Leptothorax spec. A
Fifty four of a total of 206 queenright colonies of Leptothorax spec. A collected in June 1983,1985, and 1988 contained more than one and up to seven females (Table 1). In additional colonies col- lected in July 1987 and 1988, we counted up to 10 and more females, most of them inseminated. Because at the end of July this year's females have eclosed and may already have mated, it cannot be ruled out, however, that the higher number of females found at that time may be a transient phenomenon and that the young mated females will leave their mothers' nests before hibernation. It is quite certain that all females found in June colonies have hibernated in the nest, and we also found females in July and even August whose fat body color indicated that they had not eclosed recently. All of the females and some of the workers in 30 colonies col- lected in June, and in an additional 59 colonies collected in July, were dissected. In all but four colonies only one female was found to be inseminated and fertile and, thus, a queen; the other females, though most were inseminated, did not show any corpora lutea and their ovarioles were only poorly developed (Table 2). In at least two of the four colonies with two A-females, workers engaged in heavy fighting and the queens were attacked. In these cases it is probable that neighboring nests were mixed by error during collection. Both gynomorphic and intermorphic queens were accompanied by inseminated, sterile females, gynomorphic or intermorphic or both, but the percentage of June colonies with a gynomorphic queen and additional females was distinctly smaller (4.2 percent) than that of comparable colonies with intermorphic queens (28.9 percent). This difference is striking in each of the June collections and it is present in the July collection also. The majority of the supernumer- ary females (61 out of 80) were inseminated, but sterile. In three queenright colonies all the additional females were uninseminated.



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Table 1. Number of gynomorphic (G) and intermorphic (I) females in colonies of some species of the sub- w
hÌÔr
genus Leptothorax s. str. ^.
Number of females
Species
I G I + G
Percentage of colonies
and date No. of with >1 female'
collected colonies0 1 2 3 4 > 1 2 3 4 > 2 3 4 > I G S spec.A6/83 88 18 38 7 2 1 1 18 - - - - I l l - 22.4 0.0 20.0 6/85 120 40 38 7 1 1 10 16
- 1 1 -
1 - 1 3
33.3 11.1 32.5
6/88 64
8 30 7 4 1 1
12
- - - -
- -
1 1 30.2
0.0 26.8
7/88 87 13 20 2 3 3 2 36
7 -
- -
- 1
- 5 33.3 16.3
23.0
spec. B 6/83 39 7 2 7 3 1 1 - 15.6
6/85 32 12 1 3 2 2 - 3 35.0
7/87 65 15 4 2 2 3 - 3 16.0
6/88 6
1 3 1 - - 1 40.0
7/88 29 2
1 2 7 3 1 4 55.6
retractus 7/88 14 - 1 1 - 1 - 2 21.4
8/88 16 2 5 5 1 - 3 64.3
spec.C8/88 31 3 1 3 3 3 1 8 53.6
Data from the literature:
acervorum2 754
muscorum2 294
gredleri* 190
kutteri2 22
spec. C3 27
n
'Excluding colonies without a female
<
^
ZBuschinger, 1968a rn
3Buschinger, 1979b l-rt




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19881 Heinze & Buschinger - Leptothorax 315 Five colonies in the June samples lacked fertile queens, but had one to three intermorphic b->A-females and additional b-females. Of 36 colonies that had only a single female, 10 did not have a fertile queen but did have an intermorphic b->A-female, which in some cases was just ready to lay her first eggs. These presently queenless colonies usually were quite small and consisted of few (1 to 10) workers and some brood. We did not find any queenless colonies with gynomorphic b->A females. All gynomorphic females that were the only female in the colony were found to be fully fertile. (In these evaluations the 12 colonies with both female morphs were not included. Females were dissected in only five of these colonies; in one case the queen was a gynomorph. Genetically mediated queen polymorphism in Leptothorax spec. A turned out to be a helpful tool in evaluating the relatedness of the different females in a col- ony. In one colony from Tadoussac, for example, the intermorphic queen produced only intermorphic female sexuals. One of the supernumerary females, however, was an inseminated gynomorphic female.)
C-females, not inseminated, but fertile females, which produce males, were found in two or three colonies in the field. Other Leptothorax
As the data in Table 2 indicate, colonies of the closely related Leptothorax spec. B, of the Western species C and of L. retractus frequently contained several females. Here dissections proved, how- ever, that all three species regularly have truly polygynous societies. In colonies of spec. B, which were collected in June, usually all inseminated females were fertile. Colonies of L. retractus and L. spec. C were examined in August; here a certain percentage of the females may have been only recently inseminated and thus not yet fertile.
Colony founding in L. spec. A
Of the more than 500 colonies of Leptothorax spec. A collected by us since 1979 in North America, only two appeared to be incip- ient colonies, consisting of a single queen (one gynomorph and one intermorph) and brood. In two or three more cases the colony con- sisted of two females, one fertile, the other not, and brood. The occurrence of colonies without a fertile queen (see above) but with nearly fertile b->A-females, in June, suggests that colony founda- tion by budding or colony fission takes place.



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316 Psyche [vo~. 95
Table 2.
Dissection results in colonies of Leptothorax s. str. with more than one female. AA, two or more fully fertile queens (polygyny); AAb, AAc, AAbc, two or more fully fertile queens, accompanied by one or several b- and/or c-females (polygyny); Ab, Ac, Abc, one fertile queen, accompanied by one or several b-females (functional monogyny) and/ or c-females; b, c, be, one or several b- and/ or c-females without queen.
AA AAb AAbc AAc Ab Abc Ac bc b c Total %AA spec. A June 2a la - 10 4 3 2 2 - 24 8.9 July - - 1 - 3 8 4 2 2 3 2 1
spec. B 7 3
3
1 1 1 1 - - 17 76.5
retract us
2 1
1 -
1 - I - - - 6 66.7
spec. C
1 -
1 - 1 - 2 2 2 9 22.2
Data from the literature:
be, b, c
acervorum' 40 2 3 12 3 2 54 5 121 47.1
muscorum2 3 - 5 1 17 15 9 6 56 16.1
gredleril - - 26 20 - 46
spec. C3 2 -
- - - -
3 66.7
'In two of these colonies fighting between workers was observed. IBuschinger, I968a
2Buschinger, 1967
3Buschinger, 1979b
In experiments carried out at the TH Darmstadt, L. spec. A females were given the chance to mate in arenas containing their maternal colony and in addition, empty nesting sites. Both winged gynomorphic and wingless intermorphic females perform a station- ary sexual calling behavior similar to that of other leptothoracine ants, the so called bbLocksterzeln" (Buschinger, 1968b). Whereas intermorphic females regularly started sexual display within a short distance of the nest entrance, winged females usually showed some flight activity before they began sexual calling. Most intermorphic females returned into their mothers' colonies within a few hours after mating, and none of 41 intermorphic females, compared to 13 of 43 gynomorphic females, hibernated outside their mothers' nests. Under laboratory conditions no young, inseminated female, intermorphic or gynomorphic, successfully founded a colony on its own and raised brood during the first following summer. The majority of inseminated females, which were kept separate from workers, were able to survive two, three, or more hibernations. Both intermorphic and gynomorphic females left their



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19881 Heinze & Buschinger -Leptothorax 317 nests to search for food and fed their own larvae. Only one single gynomorphic queen, however, managed to rear her own workers in the second summer after mating; in most cases the brood eventually died.
In the laboratory, supernumerary females have been found to survive for several artificial breeding cycles in the presence of the old queen. Aggression of the workers toward their young inseminated sisters was observed only in colonies with gynomorphs. Here 13 of 19 females, which had been put back into their mothers' nest and were not given the chance to escape, were killed by workers within a few weeks after copulation, their antennae and legs having been cut off. The dissection showed that in most of these females the devel- opment of eggs had already started and the ovarioles were elon- gated. Four other inseminated females were tolerated in this colony for at least one hibernation. Foreign inseminated females were never tolerated by a colony, regardless of the morpha. In several cases, fission of colonies with two or more inseminated females occurred after hibernation. Old nesting sites were aban- doned and workers moved brood and adults into two or even three different new nesting sites. In comparable situations, colonies with only one single female usually gathered in one nesting site after a few days. Spontaneous fission of colonies with several females, however, led in three instances to two independent societies each, which did not exchange brood or workers. One colony fused again after two breeding cycles, but only after one of the two queens had died.
Queen replacement was observed in five colonies, where a hitherto sterile female became fertile after the old queen had died. In two colonies, this event was pursued in electrophoretical enzyme analy- sis. The esterase locus #7 is variable in Leptothorax spec. A and in other related species; its at least four different allozymes can be separated by isoelectric focusing (Heinze and Buschinger, 1988). Queen replacement was reflected in a change of the esterase geno- type of worker pupae. A colony from Baie Ste. Catherine, Que., which before had workers with the esterase genotypes BC and BD, now reared diploid brood with the genotype AC, too, thus decreas- ing the relatedness of workers within the colony. In an additional colony from Rivikre Romaine, Que., queen replacement led to a change in the morpha of young females. Whereas the old queen had



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3 18 Psyche [vo~. 95
reared both morphs, the replacement queen only produced inter- morphic females.
Of the 222 colonies of Leptothorax spec. B two contained a single queen and brood only, and a third one consisted of two fertile females and brood. Three more colonies might have been incipient, too, but here one worker had already eclosed. However, 7 of 14 colonies of a dark brown ant morphologically similar to L. spec. B, which were collected near Vancouver, B.C., in August 1988, were found without workers.
The ant tribe Leptothoracini consists of several hundred species of small- to medium-sized ants, which form colonies of several dozen to few hundreds of workers. It exhibits a rich variety of different social structures and colony foundation behaviors. Apart from social parasites, which may be inquilines, degenerate slave- makers, active dulotes, and xenobiotic guest ants, the non parasitic species have been found to be obligatorily monogynous, function- ally monogynous, or facultatively polygynous (Buschinger, 1974a). We here report on functional monogyny and polygyny in some species of the subgenus Leptothorax s.str. M. R. Smith (= Mycho- thorax Ruzsky) from North America. Between 20 and 30 percent of the colonies of L. retractus, L. spec. B, and L. spec. C are truly polygynous. The fertility of several inseminated females has been proven by dissection; in a number of cases, egg-laying has been directly observed. In Leptothorax spec. A, about one-fourth of all colonies with intermorphic queens contained additional, insemi- nated females, again mostly intermorphs, which in almost all cases have been found to be sterile. An occasional polygyny in Lepto- thorax spec. A cannot be ruled out but it seems to be very rare. There are two important differences between functional mono- gyny in polistine wasps and in Leptothoracini. In Polistes gallicus, Pardi (1940; 1946) had observed that when two females cooperate in colony foundation, the more aggressive one becomes queen, and the subordinate one becomes worker. In colonies with several females, however, ovary size and fertility correspond to the female's rank in a dominance hierarchy. Several females may lay eggs, though in dif- fering degrees, and functional monogyny is sometimes guaranteed only by differential egg consumption by the dominant a-female



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19881 Heinze & Buschinger -Leptothorax 319 (Gervet, 1964). In most cases the coexistence of several inseminated females in one nest is transient, and it resembles the regulation of queen number in obligatorily monogynous ants after colony foun- dation by pleometrosis (Buschinger, 1974a). In leptothoracine ants, on the other hand, functional monogyny is total and may be a lasting phenomenon. Only the queen has fully developed ovaries; those of the supernumerary females are always undeveloped. The presence of b->A-females with elongated ovarioles in colonies of Leptothorax spec. A is restricted to a short period of time and leads to colony fission or, as was observed in the lab, to aggressive be- havior toward the young female and finally to her death. Whether dominance hierarchies exist in colonies with several supernumerary females, as in Polistes, is not yet known. Our observations suggest that, comparable to primary and secon- dary polygyny, functional monogyny in Leptothoracini may arise in two ways. Intermorphic females, and perhaps gynomorphic females also, are easily accepted in their mothers' colonies after mating, and they may stay there for several breeding cycles. The other possibil- ity, a pleometrosis-like colony foundation with several inseminated young females, one of which becomes fertile, has been observed in