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Polygyny and Polydomy in Three North American Species of the Ant Genus Leptothorax Mayr (Hymenoptera: Formicidae).
Psyche 89:249-274, 1982.
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POLYGYNY AND POLYDOMY IN THREE NORTH
AMERICAN SPECIES OF THE ANT GENUS
LEPTOTHORAX MAYR (HYMENOPTERA: FORMICIDAE)' This paper deals with certain behavioral and ecological factors which may be relevant to the evolution and maintenance of social parasitism in ants. We will argue that some of the same factors which might predispose one species to evolve into a social parasite might make resistance to parasitism difficult for a closely related species,
After their mating flight, the queens of most nonparasitic ant species found new colonies alone, A queen of such a species finds a suitable nesting place, excavates a small cavity, and seals herself inside. She then lays a clutch of eggs and feeds her first larvae a special "baby food" derived metabolically from the degeneration of her wing muscles and fat body. These larvae mature to become female workers which forage for food, enlarge the nest, feed the queen, and rear subsequent broods of workers and reproductives. Mature ant colonies usually occupy only one nest (monodomy). However, the number of queens in typical mature colonies varies. Colonies of some species never contain more than one functional queen (monogyny), while colonies of other species often have multi- ple queens (polygyny) (Buschinger 1974). However, the queens of all known obligatory slave-making, in- quiline, and temporary-parasite species found colonies non-inde- 1. This research was supported by grants to Thomas Alloway from the Natural Sciences and Engineering Research Council of Canada and to Alfred Buschinger from the Deutsche Forschungsgemeinschaft. 2. Erindale College, University of Toronto, Mississauga, Ontario, CANADA L5L 1C6.
3. Fachbereich Biologic, Institut fur Zoologic, Technische Hochschule, 61 Darm- stadt, Schnittspahnstr. 3, Federal Republic of Germany. 4. The Lindenwood Colleges, Saint Charles Missouri, U.S.A. 63301. Manuscript received by the editor August 5, 1982.
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250 Psyche [vo~. 89
pendently. The parasite queen finds a colony of her host species, enters it, and somehow usurps the role of a host-species queen. The host-species workers then raise the parasite queen's brood. Species of temporary parasites possess a completely functional worker caste. At first, the temporary-parasite workers and the host- species workers exist alongside one another. However, when the host-species workers die, they are not replaced; and a pure colony of the temporary-parasite species develops. The workers of slave- making parasites are highly specialized for fighting and raiding the nests of host-species colonies; and as a consequence of their raids during which they capture host-species worker pupae and larvae, a force of host-species workers (or "slaves") is maintained. Inquiline parasites either have no worker caste at all; or, if one is present, the workers seem to play no role in maintaining the colony. In some cases, a continuing supply of host-species workers is maintained by the host-species queen's coexisting with the inquiline queen (Busch- inger, 1970; Wilson, 1971).
This paper presents data concerning several aspects of the behav- ioral biology of three North American species of the ant genus Leptothorax Mayr: L. ambiguus Emery, L. curvispinosus Mayr, and L. longispinosus Roger. These species interested us because they are hosts to three closely related parasite species. All three species are enslaved by the obligatory slave-makers L. duloticus Wesson and Harpagoxenus americanus (Emery); and L. curvispino- sus is the host of the workerless inquiline species L. minutissimus M. R. Smith (Alloway, 1979; Creighton, 1950). Thus, studies of the behavior and ecology of these three nonparasitic species may eluci- date the ethological and ecological circumstances under which social parasitism evolves and is maintained. Headley (1943) and Talbot (1957) reported that the number of queens in nests of L. curvispinosus and L. longispinosus is quite variable. Some nests contain several dealate queens, some contain one, and some contain none at all. Observations indicated that the number of queens in nests of L. ambiguus is also variable (Alloway, unpublished data). In addition, we found that many queenless nests of all three species contained broods which either included worker and queen pupae at the time of collection or matured into worker and queen (as well as male) pupae.
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19821 Alloway, Buschinger, Talbot, Stuart & Thomas 251 These observations raised a number of hypotheses. Nests contain- ing more than one dealate queen suggested that some colonies of L. arnbiguus, L. curvispinosus, and L. longispinosus are polygynous. The production of female pupae in queenless nests raised at least three possibilities which are not mutually exclusive. First, a queen- less nest might be part of a polydomous colony with the female pupae being the progeny of one or more queens located in another nest at the time of collection. Second, these species might possess numerous ergatomorphic reproductives, individuals which resemble workers morphologically but which have a spermatheca, can be inseminated, and are capable of laying fertilized female eggs (Busch- inger 1975, 1978). Third, a queenless nest might be the remnant of a colony whose queen had died.
Over a two-year period, nests of L. ambiguus, L. curvispinosus, and L. longispinosus were collected during late March, April, May and early June; and weekly collection of L. ambiguus and L. longi- spinosus were obtained throughout June, July, and August of one summer. We recorded the number of queens present in every nest. In nests containing pupae at the time of collection, the kind of pupae present (queen, worker, and/or male) was also noted. Finally, nests of all three species were collected during the early spring of one year and cultured in the laboratory to determine the sex and caste of the pupae which matured from larvae present in the nests at the time of collection.
Results
Table 1 contains data regarding the proportions of nests collected during the springs of two years which contained 0, 1, or more than 1 queen. About 115 of the nests contained more than one dealate queen; about 1 / 3 contained no queen; and the remainder contained 1 queen. Tables 2, 3, and 4 reveal that the proportion of queenless nests was similar across years and throughout the season. Table 2 presents the numbers and proportions of nests of all three species collected in the spring and containing pupae of various kinds. Table 3 presents similar data for nests of L. ambiguus and L. longispinosus collected throughout the summer. These tables reveal that many freshly collected queenless nests contained female (worker and queen) pupae. Table 4 presents data concerning the broods
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252 Psyche [VOI. 89
Table 1.
Number and Percent of Nests of L. ambiguus, L. curvispinosus, and L. longispinosus Containing 0, 1, or More Than 1 Queen Number of 1. 1. 1.
Queens ambiguus curvispinosus longispinosus Total 0 453 (29.7%)
177 (36.3%) 237 (37.0%) 867 (32.7%)
1 765 (50.3%)
228 (46.7%) 31 1 (48.6%) 1304 (49.2%)
More than 1
304 (20.1%)
83 (17.0%) 92 (14.4%) 479 (18.1%)
Total 1522 ( 100.0%) 488 ( 100.0%) 640 ( 100.0%) 2650 ( 100.0%) which matured from queenless and queenright nests of the three species collected in the early spring and then cultured in the labora- tory. Once again, many queenless nests produced female pupae. Discussion
First, we want to stress that variability in the number of queens in nests of L. curvispinosus and L. longispinosus, first noted by Head- ley (1943) and Talbot (1957), is not a local or transitory pheno- menon and note that the number of queens in nests of L. ambiguus is also quite variable. However, of far greater importance is the large proportion of queenless nests of all three species which produce female (as well as male) pupae. This fact raised questions about the possible existence of ergatomorphic reproductives and polydomy. To demonstrate that a species of ant is facultatively polygynous, one must show that two or more fertile inseminated females can coexist in nests. Headley (1943) and Talbot (1957) reported the occurrence of multiple queens in some nests of L. curvispinosus and L. longispinosus. However, these authors did not determine whether more than one queen was inseminated and egg-laying. Wilson
(1 974a, b) observed several multiple-queen nests of L. curvispinosus and reported that all the queens laid eggs. However, as we shall show, uninseminated queens and workers sometimes lay eggs. Thus, the question of the occurrence of polygyny involving fertile in- seminated queens remained open. In addition, the production of female pupae in many queenless nests of L. ambiguus, L. curvispino- sus, and L. longispinosus suggested, as one possibility, the hypothe- sis that these species might possess frequent ergatomorphic female reproductives.
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19821 Alloway, Buschinger, Talbot, Stuart & Thomas 253 Table 2. Number and Percent of Queenright and Queenless Nests of L. ambiguus, L. curvispinosus, and L. longispinousus Containing Pupae and/ or Alate Reproductives of Various Types at the Time of Collection (1977-78) - -
Queenright Nests
Q and/or Q and/ or
Species 0 Only $ and 8 8 Only Total
L. ambiguus 180 (83.3%)
31 (14.4%)
5 (2.3%) 216 (100.0%)
L. curvispinosus
23 (53.5%)
19 (44.2%)
1 (2.3%) 43 (100.0%)
L. longispinosus
76 (66.1%)
33 (28.7%)
6 (5.2%) 1 15 (100.0%)
Total 279 (74.6%) 83 (22.2%) 12 (3.2%) 374 (100.0%) Queenless Nests
Q and/ or
Q and/ or
Species 0 Only $ and 8 8 Only Total
L. ambiguus
90 (80.4%)
16 (14.3%)
6 (5.4%) 112 (100.0%)
L. curvispinosus 19 (59.4%)
9 (28.1%)
4 (12.5%) 32 (100.0%)
L. longispinosus 35 (50.0%) 24 (34.3%)
11 (15.7%)
70 (100.0%)
Total 144 (67.3%) 49 (22.9%) 21 (9.8%) 214 (100.0%) Materials and Methods
To determine whether polygyny involving inseminated queens occurs in these species, we dissected all the queens present in sam- ples of nests containing more than one dealate queen. To determine whether ergatomorphic female reproductives occur frequently, we dissected all the "workers" from five queenless nests of each species which had produced female broods when cultured in the laboratory. For each queen or worker dissected, we noted the following characteristics:
the number of ovarioles.
the length of the ovaries. In young virgin queens, the ovaries are thin and about 314 the length of the queen's gaster. When a queen becomes fertile, her ovaries grow until they eventually become as long as her entire body. In old fertile queens, the folded and coiled ovarioles enlarge until they almost completely fill the gaster.
the presence or absence of any growing oocytes in the ovarioles. The ovarioles of sterile individuals contain no oocytes; and in hibernating fertile queens, the oocytes are transparent. As yolk is
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254 Psyche [VOI. 89
deposited in growing oocytes, they become opaque; and ripe eggs are white.
the presence or absence of corpora lutea in the bases of the ovarioles. These yellowish residues of nutritional cells remain in the ovaries when eggs have been laid.
the presence or absence of a full or empty spermatheca. Individ- uals with no spermatheca or an empty spermatheca are incap- able of laying fertilized eggs which develop into workers or queens. An empty spermatheca appears as a small, transparent bladder on the common oviduct. When full of sperm, the sperma- theca is white and superficially resembles a ripe egg in size and coloration.
Results:
Our dissections enabled us to distinguish several physiologically different kinds of queens. To simplify the presentation of data, we Table 3.
Number of Queenright and Queenless Nests of L. ambiguus and
L. longispinosus Collected during June, July, and August and the Composition of their Broods
L. ambiguus
Queenless nests Queenright nests
Type of Brood
Type of Brood
9, ?4? Q? g?
8 only Q and g and 8 8 only 9 and g and 8 June 0 5
0 0 28 0
July 0 11
17 1 3 7 7 1
August 2 9
8 2 3 2 77
L. longispinosus
Queenless nests Queenright nests
Type of Brood
Type of Brood
Q, ! 2 9 Q3 g7
8 only Q and g and 8 8 only Q and and 8
June 0 0
1 0 2 I
July 0 0
4 0 1 I2
August
0 0
I 0 0 3
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19821
Alloway, Buschinger, Talbot, Stuart & Thomas will employ a set of terms developed by Buschinger (1968) to de- scribe these individuals. These terms are defined as follows: A-queen: An inseminated, fully fertile queen. The ovaries are as long, or nearly as long, as the whole body. The ovarioles con- tain many developing oocytes; and conspicuous corpora lutea are present. The spermatheca is full of sperm. Such queens are normally more than a year old.
b-queen: An inseminated young queen. At the time of our study (in mid-summer), the ovaries were about half their eventual length and contained developing oocytes. Sometimes a small corpus luteum was visible in the base of one or two ovarioles. The
spermatheca was full. We believe that these females had mated the previous summer and were in the process of becoming fully fertile. After mating, newly inseminated queens have very short ovarioles with no developing oocytes. If a nest, before the mat- ing season, contains one or more A-queens and one or more b-queens with growing oocytes, we conclude that that nest represents a11 or part of a colony which adopted one or more newly mated queens the previous summer.
Table 4. Number and Percent of Queenright and Queenless Nests of L. umbiguus, L. curvispinosus and L. longispinosus Collected in the Spring of 1979 which Produced Broods of Various Compositions when Cultured in the Laboratory Species
L. ambiguus 68 (47.5%)
60 (42.0%)
15 (10.5%) 143 (100.0%)
L. curvispinosus
95 (65.5%)
49 (33.8%)
1 ( 0.7%) I45 (100.0%)
L. longispinosus
42 (56.0%)
22 (29.3%) 1 I (14.7%) 75 ( 100.0%)
Total
205 (56.5%)
131 (36.1%) 27 ( 7.4%)
363 (~00.0%)
Q and/or Q and/or
Species g only g and 8 8 only Total
L. ambiguus 37 (52.1%) 24 (33.8%)
I0 (14.1%)
71 (100.0%)
L. curvispinosus 35 (43.2%)
38 (46.9%)
8 ( 9.9%) 8 I ( 100.0%)
L. longispinosus
12 (38.7%)
I2 (38.7%)
7 (22.6%) 3 I (100.0%)
Total 84 (45.9%)
74 (40.4%) 25 ( 13.7%)
1 83 ( 100.0%)
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25 6 Psyche [vo~. 89
c-queen: An uninseminated, old, sterile female. The ovaries are short and contain no oocytes. The spermatheca, if present, is empty; but it may not be present. The wing muscles are degen- erate and have been replaced by fat body. (The term d-queen would denote a young dealate female which had not been inseminated. The reproductive organs resemble those of c- queens, but the wing muscles have not yet degenerated, We found no d-queens, probably because we performed our dissec- tions before the sexual brood had eclosed.) C-queen: An uninseminated, egg-laying female with ovarioles like those of an A-queen. Sometimes there is no spermatheca. In this paper, we report the occurrence of significant numbers of individuals of this type for the first time in Leptothoracine ants. However, they occur rather frequently in colonies of Formica polyctena Foerster (Ehrhardt 1970) and Monomorium pha- raonis (L.) (Petersen & Buschinger 1971). The origin of these females in nests of L. ambiguusl L. curvispinosusl and L. longi- spinosus is unclear. They may be old individuals which were once inseminated but whose supply of sperm has been ex- hausted. However, the existence of egg-layers with no sperma- theca indicates that insemination is not a necessary prerequisite for fertility. Recently U. Winter (personal communication) found that Harpagoxenus sublaevis males often transmit very little or no sperm during their first copulation. Thus, a queen which had mated only once with such a male might become fertile after receiving only the secretions of the males's acces- sory glands. Perhaps a similar mechanism accounts for the existence of C-queens in these species of Leptothorax. The results of the dissections of queens of each species and of workers will be presented separately.
I. Leptothorax ambiguus
A total of 88 dealate females from 30 multiple-queen colonies was dissected. Only about 112 the multiple-queen nests contained more than one A-queen and were thus "truly polygynous" (see Table 5). Three of these truly polygynous nests also contained one or two b-queens and were thus in the process of developing polygyny to a higher degree.
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19821 Alloway, Buschinger, Talbot, Stuart & Thomas 257 Table 5.
Number and Type of Dealate Females in Multiple-Queen Colonies of Leptorhorax ambigus
Colony n Dealate
No. P? A-QQ b-QQ C-QQ C-QQ Remarks
Colonies No.
1-15 are truly
polygynous
Colonies No.
16-23 are
becoming
polygynous
Colony fragment?
+C-Q without
spermatheca
Colony fragment?
Total 88 43 16 7 22
Another 7 nests (No. 16-23 in Table 5) were in the process of becoming polygynous. They contained 1 A-queen and 1 or 2 b- queens. One nest (No. 23) contained 2 b-queens only and was thus also becoming polygynous, although it lacked an A-queen. A number of nests contained one or more C-queens. Most of these
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258 Psyche [vo~. 89
individuals were living with A-queens. Two C-queens without a spermatheca were found in this sample (in nests No. 24 and 25). 2, Leptothorax curvispinosus
A total of 64 dealate queens from a sample of 23 multiple-queen nests was dissected. As was the case for L. ambiguus, we found all four categories of dealate females in L, curvispinosus (see Table 6). However, approximately 314 of the curvispinosus nests (74%) con- tained multiple A-queens, as compared to only about 112 of the arnbiguus nests. In addition, all 7 of the multiple-queen curvispino- sus nests which had only 1 A-queen contained one or more b-queens and were thus becoming polygynous. The total number of C-queens was much lower in curvispinosus than in ambiguus. However, we found 3 C-queens with no spermatheca; and 2 of these were fully fertile.
3. Leptothorax longispinosus
A total of 79 queens from a sample of 26 multiple-queen nests was dissected. The proportion of nests containing more than one A-queen was 65%; and all but one of the other nests contained either one or more b-queens living with an A-queen or more than one b-queen without an A-queen (see Table 7). The only exception was nest No. 23 which contained 7 C-queens living with a single A- queen. One of these C-queens had no spermatheca. 4. The number of ovarioles in queens
Table 8 shows that queens of L. ambiguus usually have 6 ovari- oles (both ovaries combined). Six is the usual number of ovarioles for most European species of the subgenus Leptothorax sensu strict0 (=Myrafant M. R. Smith 1950) and for species of the subge- nus Mychothorax (=Leptothorax sensu M. R. Smith) (Buschinger, unpublished data). However, L. curvispinosus queens most commonly have 8 ovarioles; and L. longispinosus queens most com- monly have 7. Moreover, the number of ovarioles in L. longispino- sus queens is very variable; and the distribution of ovarioles in single specimens of this species can be quite asymmetrical, One queen with 10 ovarioles had 6 on the left side and 4 on the right; another with 11 ovarioles had 4 on the left and 7 on the right. There was no evidence that the number of ovarioles is correlated with a queen's function in a nest. The number of ovarioles often varied considerable among
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19821 Alloway, Buschinger, Talbot, Stuart & Thomas 259 Table 6. Numbers and Type of Dealate Females in Multiple-Queen Colonies of Leptothorax curvispinosus
Colony n Dealate
No. QQ A-QQ b-QQ c-QQ C-QQ Remarks
Colony No.
1-16 truly
polygynous
+C-Qwithout
spermat heca
Colony No.
17-23
becoming polygynous
'c-Q without
spermatheca
+C-Q without
spermatheca
-
- --
Total 64 46 14 1 3
queens in single nests, especially in L. longispinosus. Moreover, b- and C-queens on average had no fewer ovarioles than A-queens. 5. Workers
All the queenless nests whose workers were dissected contained one or more egg-laying individuals (see Table 9). However, none of the fertile workers possessed a spermatheca. Thus, we presume that
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