Francoeur. A. Buschinger and A. Francoeur.
Queen polymorphism and functional monogyny in the ant, Leptothorax spahgnicolus.
Psyche 98:119-134, 1991.

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PSYCHE
Vol. 98 1991 No. 2-3
QUEEN POLYMORPHISM AND
FUNCTIONAL MONOGYNY IN THE ANT,
LEPTOTHORAX SPHAGNICOLUS FRANCOEUR
Queen polymorphism, the occurrence of morphologically differ- ent, mated and egg-laying females in one species of ants, has been demonstrated until recently mainly in social parasites. Particularly among the rnyrmicine tribe Leptothoracini, intermorphic and nearly workerlike queens and fully alate or dealate gynomorphic queens have been found in guest ants such as Formicoxenus nitidu- lus (Buschinger and Winter, 1976), F. provancheri (Buschinger et al., 1980), and F. diversipilosus (Buschinger, 1979 - erroneously named F. hirticornis). Apparently this feature is characteristic of the entire genus (Francoeur et all., 1985). In the slave-making ant, Harpagoxenus sublaevis, a genetic mechanism determining queen polymorphism has been detected (Buschinger and Winter, 1986). Queen polymorphism in leptothoracines, however, is not restricted to parasitic species. Recently it has been found in an as yet unde- termined, independent Leptothorax sp. A from Quebec (Heinze and Buschinger, 1987). A genetic mechanism similar to that in H. sub- laevis is responsible for the queen polymorphism in this species, too (Heinze and Buschinger, 1989). Finally, we report here on queen polymorphism in the recently described Leptothorax sphag- nicolus Francoeur 1986, another free-living species from Quebec. '~nstitut fur Zoologic, FB Biologic, der Technischen Hochschule Darmstadt, Schnittspahnstr.3, D-6100 Darmstadt, FRG wniversite du Quebec i Chicoutimi (Quebec), Canada G7H 2B 1 Manuscript received 18 May 1991.




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120 Psyche [vo~. 98
In addition we provide evidence for functional monogyny in L. sphagnicolus, another feature rarely found in ants. In functionally monogynous ants, a colony normally contains but one inseminated and egg-laying queen, and often alongside her one or several other females may be present which are inseminated but do not develop fertility. Among ants, this phenomenon was first observed in Lep- tothorax gredleri from Europe (Buschinger, 1968), which is an independent ant with exclusively gynomorphic queens. Functional monogyny, however, is characteristic for most of, or perhaps all, the guest ants of the genus Formicoxenus (Francoeur et all., 1985), and also for Leptothorax sp. A (Heinze and Buschinger, 1987). Heinze and Lipski (1990) found that a dominance hierarchy among the mated females of this species is responsible for the sterility of all females except the one in a-position. Ito (1990) described functional monogyny in Leptothorax acervorum from North Japan, a species which in Europe is facultatively polygynous (both colonies with one and several queens occur in a population, Buschinger, 1968). All reproductive females, however, are uni- formly gynomorphic.
Leptothorax sphagnicolus is, therefore, the second example of an independent ant exhibiting both queen polymorphism and func- tional monogyny.
MATERIAL AND METHODS
Considerable numbers of L. sphagnicolus were collected previ- ously in 197211973 during a study on ecological succession of spruce bog (Francoeur and Pepin, 1975, 1 W8), in five sites around Chicoutimi/Qu6bec. The sites and the characteristics of these bogs are described in detail in Francoeur and Pepin (1975). We used this material for an evaluation of the proportions of gynomorphs, inter- morphs and ergatomorphs in the various localities (Tab. I). Additional colonies of L. sphagnicolus were collected by A.F. between 1980 and 1986 in a spruce bog near Saint-Ambroise. This material comprises the type series of the species. Together with material from the same locality (SA in tab. I) which had been extracted from Sphagnum hummocks containing nests of Formica dakotensis, we analyzed these samples more closely in order to demonstrate the morphological variability among the intermorphs (Tab. 11). Finally, colonies of L. sphagnicolus were collected by



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Buschinger & Francoeur
A.B on 15 and 19 June, 1983, again in the spruce bog near St.- Ambroise, and on 3 July, 1983, near L'Ascension, in the Saguenay- Lac-St.-Jean area, Quebec. The ants there were found in the upper parts of Sphagnum hummocks, usually in places where just a few Polytrichum stems were growing, bat where the Sphagnum surface was still fully exposed to insolation. The sac-like nesting chambers can be detected when the Sphagnum is gently opened. They reach a depth of 3-5 crn and are coated inside with a layer of apparently chewed Sphagnum leaflets (Fig. 1). The ants were aspirated, but due to the spongy structure of the substratum it is difficult to col- lect complete colonies, a few specimens usually escape. After an inspection of the population of each nest, 21 of them were selected for dissection of all or of representative samples of the ergatornorphs, intennorphs and dealates present. Other colonies were kept alive in order to study their offspring. Dissections were made according to Buschinger and Winter (1976) and Buschinger and Alloway (1 978). Living colonies were kept in formicaries and in daily changing temperatures as described by Buschinger (1974). Fig. 1: Nest of Leprothurax sphagnicoSus within a Sphagnum hummock, seen from above. The nesting chamber of about 3x1 cm is visible in the center, where the Sphagnum was pulled apart,




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122 Psyche [vo~. 98
a) In table I we present the proportions of gynomorphs, inter- morphs and ergatomorphs in the 197211973 samples, from five different spruce bogs. The samples "SA" from the F. dakotensis- inhabited Sphagnum hummocks are included. It appears that the ratios of intermorphs and ergatomorphs vary considerably between the sites (13.1 to 40.2% intermorphs, which are potential queens, as is shown below!), and that gynomorphs are very rare (.7% of the total female population). Table I1 reveals a certain morphological variation among the intermorphs. The proportions of inferior, intermediate and superior intermorphs again vary widely between the samples from different localities.
b) In table I11 the composition of 38 individually collected colonies (= inhabitants of one nest) is analyzed. The colonies evi- dently are very small in comparison with other Leptothorax species where a nest may contain up to several hundred adults. In L, sphagnicolus we found a mean number of 7.5 2 9.8 (median 4.5) specimens, with maxima of 42 and 49 individuals in the largest nests. A size of more than 15 adults is apparently rarely reached. c) Already during collecting in the field we observed that never more than one specimen in each colony had a largely extended gaster. In 23 colonies out of the 38 of table I11 we could identify a female reproductive, and in all these instances it was an inter- morph, even when gynomorphs also were present (no. 29, 30, 37). By dissecting the gynomorphs, intermorphs and representative numbers of ergatomorphs of several colonies we could demon- strate that in fact each colony contains only one mated and egg- laying specimen. However, where more than one intermorphic andlor gynomorphic specimen were found together, all of them were inseminated. They had ovaries with 2x3 ovarioles, the usual number in Leptothorax queens, and a receptacle, whereas the ergatomorphs have only 2x 1 ovarioles, and lack a spermatheca. In the following some results of dissecting shall be detailed. 1. Samples without intermorphs and gynomorphs always con- tained only ergatomorphs with two ovarioles each, without a spermatheca, and not egg-laying (table 111, no. 1, 2, 5, 31, 34). We interpret these samples to be colony fragments where the queen most probably was lost during collecting.



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Table I. Proportions of gynomorphs, intermorphs and ergatomorphs in samples of Leptothorax sphagnicolus from five spruce bogs in Quebec. The material was collected in 197211973 during a study on ecological succession of spruce bog (Fran- coeur and Pepin, 1975, 1978). The samples do not necessarily represent individual, complete colonies. Localities: AM = Saint-Ambroise; SA = Saint-Ambroise, colonies extracted from Sphagnum hummocks containing nests of Formica dakoten- sis; BA = Bagotville; LA = Laterrikre; LE = Saint-Leon; TC = Notre-Dame-du-Rosaire. Locality n samples n gyno- n inter-
morphs morphs
n ergato-
morphs
total n
females
% gyn. int.
of females
erg. n males and
male pupae to
a:
TOTAL 8 5 8 37 1 787 1166 (0.7) (3 1.8) (67.5)* 67 * Figures in parentheses refer to the average percentage of all female specimens.



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Psyche [VOI. 98
Table 11: Polymorphism of females in individual samples of Leptothorax sphag- nicolus from Saint-Ambroise. The individuals are rated in a series from 1 = ergato- morph, 2-8 = intermorphs, to 9 = gynomorph. Inferior intermorphs (2, 3) have 1 or 2 tiny ocelli and traces of thoracic sutures, intermediate intermorphs (4-6) with 2 or 3 small ocelli and clearly visible thoracic sutures, superior intermorphs (7, 8) have always 3 ocelli and thoracic sutures nearly as complete as in the gynomorphs, but lack the wings or wing stumps.
Sample no.
n individuals belonging to class
1 2 3 4 5 6 7 8 9
Subtotal 169 9 4 13 9 21 38 37 12 312
% 54.2 2.9 1.3 4.2 2.9 6.7 12.2 11.9 3..8 Subtotal 228 43 67 8 9 8 16 5 4 388
% 58.8 11.1 17.3 2.1 2.3 2.1 4.1 1.3 1.0 TOTAL 397 52 71 21 18 29 54 42 16 700
% 56.7 7.4 10.1 3.0 2.6 4.1 7.7 6.0 2.3




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19911 Buschinger & Francoeur 125
Table 111: Composition of 38 samples of Leptothorax sphagnicolus collected on 15 and 19 June, 1983, at St.-Ambroise (SA), and on 3 July, 1983, near L'Ascension (AN). "Fragment" means that presumably only part of the colony was collected. Only specimens found with larvae and within nests were included in this table, not single foragers. The queens were identified by dissection. -
no. loc.
-
TOTAL
%
Gynom.
Interm. Ergatom. Total n Remarks
-
fragment
fragment
incipient col.?
incipient col.?
fragment
intermorph = queen
fragment
fragment
fragment
fragmentlbranch?
fragment? 1 int. = queen
intermorph = queen
intermorph = queen
fragment
fragment
intermorph = queen
intermorph = queen
intermorph = queen
intermorph = queen
intermorph = queen
intermorph = queen
intermorph = queen
intermorph = queen
intermorph = queen
fragrnentlbranch?
1 int. = queen
intermorph = queen
1 int. = queen
1 int. = queen
intermorph = queen
fragment
intermorph = queen
fragmenttbranch?
fragment
intermorph = queen
1 int. = queen
intermorph = queen
fragment, no queen
Mean individuals per nest: 7.5 5 9.8; median: 4.5



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126 Psyche [vo~. 98
2.
Several samples contained workers and intermorphs and/or gynomorphs, but no reproductive queen. Thus, the dealate gynomorph of no. 10 was inseminated, and was found with one worker and a brood. However, this female had never laid eggs, her ovarioles were short and translucent as in vir- gin females, and no corpora lutea were present. Similarly, sample no. 25 contained an inseminated, not laying inter- morph with workers, and no. 33 a gynomorph and an inter- morph, both inseminated but not egg-laying. These samples may represent colony fragments having lost the single reproductive during collecting, or perhaps have recently separated from a "mother colony" (budding, see discussion). 3. The samples no. 26, 28, and 36 comprised 2-3 intermorphs. One of them in each colony was the reproductive queen, the others were inseminated but not laying.
4. In three colonies (no. 29, 30, 37) an egg-laying intermorph was found alongside 1, 3, and 15 gynomorphs, respectively, which were all mated but not laying.
5. Samples no. 3 and 4 consisted of only one intermorph respectively gynomorph, both mated and not laying, per- haps in the process of independent colony foundation. At least the dealate gynomorph of no. 4 had a few visible oocytes in the ovaries with beginning yolk deposition. 6. Usually the inseminated, non-laying intermorphs and gynomorphs had a whitish fat body, indicating that they were not too old, perhaps living in the colonies only since the swarming period of the preceding year. However, the 5 gynomorphs and one intermorph in colony no. 38 had yel- low fat bodies. Such a coloration usually appears in Lep- tothorax species after more than one year of adult life. From these dissection results we may conclude that L. sphagni- colus is monogynous, having only one fully reproductive queen per nest. This queen in most cases is an intermorphic specimen. In a sizeable fraction of the colonies, a number of mated, but non-lay- ing intermorphs and/or gynomorphs are living alongside the queen. In our samples these supernumerary potential queens must have been with their colonies for at least one year, since the colonies contained just eggs, larvae, and a few prepupae, but not yet young



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19911 Buschinger & Francoeur 127
adult sexuals of the current year. Pupae and adult males were found in colonies collected later in July and in August. d) Laboratory rearing of L. sphagnicolus was by far not as suc- cessful as is usual with other leptothoracine species. The colonies collected in JuneIJuly 1983 contained larvae and prepupae. They were kept in artificial summer conditions (Buschinger, 1974) until mid-August, at which time they produced a reasonably high num- ber of males, gynomorphs, intermorphs and ergatomorphs. After an artificial hibernation until mid-November for three months (which is sufficient for many related Leptothorax species) most colonies had lost much brood and workers, and only a few males and female forms appeared in the following artificial summer. In a third labo- ratory summer only one colony still produced four intermorphs. In part, the difficulties with laboratory rearing were due to the fact that the colonies had to be kept quite humid, in order to simulate the conditions in their natural habitat. This however, led to serious growth of mold in the nest chambers.
Table IV reveals the results obtained with rearing of 11 colonies. Due to uncontrolled losses of brood stages and young adults the production values are surely too low; they-represent but the minimum numbers observed. In colony no. 4 and 7 the broods of three other, small colonies were added shortly after collecting of the material, in order to obtain a higher production. The total pro- duction during one, two or three breeding cycles is added up; how- ever, in the column "remarks" we indicate the numbers of individuals produced in the second or third cycles. The breeding results are not unequivocal with respect to the question whether the queen polymorphism is genetically mediated, or due to envi- ronmental influences. Gynomorphs did appear in the offspring of intermorphic queens, alongside of intermorphs, whilst other colonies with intermorphic queens produced only intermorphs. The progeny of gynomorphic queens could not be checked because all colonies had only an intermorphic queen each, even the colonies no. 9 and 19 with dealate gynomorphs (cf. preceding section). In the offspring produced, the percentage of gynomorphs (6.43%) is not much different from that in the original, spring population (6.83% in the colonies reared in the lab, and 9.4% in all colonies of table 111). It is, however, much higher than in the field samples of table I (.7%) and table I1 (2.3%). The percentage of intermorphs



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Table IV: Results of laboratory rearing of Leptothorax sphagnicolus. The colonies were collected in spring condition, with t~t
w
larvae and a few prepupae. In artificial summer conditions they produced sexuals and workers. Some colonies were producing 00
offspring in a second (2), and one colony in a third (3) breeding cycle. Tab. I11 Original composition: Production in (I), (2) or (3) summers: Remarks Col. no. Gyn. Int. Erg. Total Gyn. Int. Erg. Total males - (1)
- (1)
- (1)
8 larvae added (2: 10)
- (1)
- (2: 2 int.)
4
larvae added (2: 2 int.)
1 (1)
3 (2: 3 erg.)
19 (2: 20, 3 int.)
(3: 4 int.)
10 (2: 60, 2 int., 3 erg.)




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19911 Buschinger & Francoeur 129
produced in laboratory culture (32.2%) is comparatively higher than in the original colonies (1 1.1% in the colonies reared, and 12.6% in all colonies of table 111) it matches, on the other hand, some of the values in table I.
The social organization and the caste and morph differentiation system of Leptothorax sphagnicolus surely deserves to be studied with more material and more intensely. Only in comparison with similar situations in related species are we able to interpret our observations with some reliability. Functional monogyny and queen polymorphism in this species are highly probable, and a genetically mediated morph determination as in Harpagoxenus sublaevis (Winter and Buschinger, 1986) and in Leptothorax sp. A (Heinze and Buschinger, 1987, 1989) is likely at least. Functional monogyny in L. gredleri (Buschinger, 1968) and in several Formi- coxenus species (Francoeur et al., 1985) is characterized by the presence of inseminated but non-egg-laying females, always together with one fully reproductive queen, in a colony over the entire year. The "supernumerary" females, after one or more years, have a yellow fat body, whereas in young females, during their first year of adult life, the fat body appears white. In L. sphagnico- lus we found such "supernumerary" females in spring and early summer before the eclosion of new sexuals. Thus, they must have been staying with the colonies for at least one year, since the pre- ceding swarming period. Most of the females, however, had white fat bodies, except those of colony no. 38ltable 111, which appar- ently were older.
An alternative interpretation of the presence of inseminated, yet sterile, females in the colonies would be that they just remain in their mother colonies after having mated in the vicinity, overwin- ter, and that they leave during the following summer, perhaps together with a few workers, forming daughter colonies. Domi- nance behavior between inseminated females may be involved, as reported for Leptothorax sp. A (Heinze, 1990). Some of our sam- ples (table 111, no. 10, 25, 33) could represent such recently formed buds or branch colonies, where the young queen had not yet developed her ovaries to the size of fully reproductive females. The two hypotheses, however, are not mutually exclusive.



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Psyche [Vol. 98
Queen polymorphism has been documented for Harpagoxenus sublaevis (Winter and Buschinger, 1986), in Formicoxenus species (Francoeur et al., 1985), and in Leptothorax sp. A (Heinze and Buschinger, 1988, 1989). In these cases, both intermorphic and fully gynomorphic specimens have been found to be the reproduc- tives of field colonies. In L. sphagnicolus, all our colonies had intermorphic queens, if any, and gynomorphs were only found as "supernumerary", inseminated but not laying females. Only one gynomorph (Table 11, no. 4) perhaps was becoming a functional queen, having slightly developed ovaries. However, she was found alone, with a brood, but without workers. So, more field studies are necessary in order to find, perhaps, colonies with actual repro- ductive gynomorphs.
The question of a genetic mechanism involved in the production of gynomorphs and intermorphs must be studied with crossbreed- ing experiments, as in Harpagoxenus sublaevis (Buschinger, 1978) and in Leptothorax sp. A (Heinze and Buschinger, 1989). Since most of the female reproductives are wingless intermorphs, we may assume that this species exhibits a stationary sexual calling behavior, as Harpagoxenus sublaevis and many other leptotho- racines (Buschinger and Alloway, 1979), and mating in laboratory colonies already has been observed (Francoeur, 1987). This is a favorable precondition for breeding experiments. The laboratory conditions, temperature regime, humidity, food, were surely differ- ent from field conditions, and obviously not optimal. Nevertheless both gynomorphs and intermorphs were produced in fairly high numbers (Tab. IV). This result is consistent with our assumption of a genetic mechanism involved in morph determination also in L. sphagnicolus: With an environmental control of morph differentia- tion we would expect that, under uniform laboratory conditions, only one queen morph is formed.
The adaptive significance of the intermorphic queens in L. sphagnicolus may be the same as in Formicoxenus and in L. sp. A: They all inhabit small, patchily distributed spots in a wide, non- inhabitable environment. These patches are the nests of host species in the case of xenobiotic Formicoxenus species (Francoeur et al., 1985), and not very large rock outcrops within dark and often humid forest areas in the case of L. sp. A (Heinze and Buschinger, 1987, 1989), each, however, suited to bear a



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19911 Buschinger & Francoeur 131
population of several dozen or more nests. The Sphagnum hum- mocks which are suitable for L. sphagnicolus also are quite scat- tered in the large spruce bogs, with wide areas being too humid or too dry. the species, thus, may use a mixed strategy of colonizing a suitable patch with branch colonies, and intermorphic queens which are unable to fly away, and perhaps spreading to other patches by alate females.
The recently described ant, Leptothorax sphagnicolus, is inhab- iting Sphagnum hummocks in spruce bogs in Quebec. Its queens are usually intermorphic, i.e., morphologically between the worker and the alateldealate female. Gynomorphs are rare, but very proba- bly they also can be queens of colonies. Like a few other, mostly parasitic leptothoracines, L. sphagnicolus exhibits a queen poly- morphism. Each colony has only one fully fertile queen, but along- side her a number of mated, non-egg-laying females may be present. The colonies are thus functionally monogynous. The supernumerary potential queens, after mating, stay with their mother colony at least until the next summer, perhaps longer. Some of them presumably leave the nest, together with workers, in order to establish own colonies (budding). The adaptive value of combined functional monogyny and queen polymorphism is discussed.