The origin of workerless parasites in Leptothorax (s. str.) (Hymenoptera: Formicidae).
LEPTOTHORAX (SSTR.) (HYMENOPTERA: FORMICIDAE) Theodor-Boveri-Institut (Biozentrum der Universitat), LS Verhaltensphysiologie und Soziobiologie, Am Hubland, D-97074 Wurzburg, F.R.G.
The evolutionary origin of workerless parasitic ants parasitizing colonies of Leptothorax (s.str.1 is investigated using data on mor- phology, chromosome number, and allozyme phenotype of both social parasites and their hosts. Of the three previously proposed pathways, the evolution of workerless parasites from guest ants or slave-makers is unlikely, at least according to a phenogram obtained by UPGMA clustering of Nei's similarities based on seven enzymes. Intraspecific evolution of the workerless parasites Doronomyrmex goesswaldi, D. kutteri, and D. pacis from their common host, Leptothorax acervorum cannot be excluded with the present data. The workerless parasite L. paraxenus, however, clearly differs from its host, L. cf. canadensis, in morphology and biochemistry, and most probably did not evolve from the latter species. It is proposed to synonymize Doronomyrmex under Lep- tothorax (s. str.).
Manuscript received 19 Junuuiy 1996.
ants, the queens of some parasite species kill all host queens ("murder parasites," Faber, 19691, but in other species parasite and host queen live and reproduce together (inquilines in the strict sense, e.g., Bourke and Franks, 1991). The evolution of social par- asites and in particular of socially parasitic ants has been exten- sively discussed starting with Darwin (1859). Three main routes leading to workerless parasitism have been proposed: workerless parasites might evolve a) directly from the species or species group serving them as host (Emery, 1909; Wasmann, 1909; Kutter, 1969; Buschinger, 1990; Bourke and Franks, 1991); b) from other para- sites, such as temporary parasites, slave-makers, or guest-ants (Wasmann, 1908, 1909; Emery, 1909; Wilson, 1971); or c) from non-parasitic ancestors other than the host species (West-Eberhard, 1990; Bourke and Franks, 199 1).
queen, but not the adult host workers (Buschinger and Klump, 1988; Heinze, 1989; Heinze and Alloway7 1991). Several attempts have been made to deduce the evolutionary ori- gin of formicoxenine murder parasites and inquilines from data on morphology, karyotype, and enzyme phenotype (Buschinger, 198 1, 1990; Heinze? 199 1). Reviewing these previously published results and providing additional unpublished data, here I critically exam- ine the hypotheses on the evolution of workerless parasites in this group and provide evidence that routes a and c are the most likely pathways leading to workerlessness.
Mt. du Lac des Cygnes (Co.
de Charlevoix-Est, Quebec)? Jasper Nat. Park (Alberta; Buschinger, Schumann and Heinze, 1994). Non-parasitic species: L. sp. A: Tadoussac (Co. de Saguenay? Quebec); L. acervorum: Grossos- theim (Bavaria, Germany), Leinburg (Bavaria, Germany), Ilgaz Dagi Ge~idi (Cankiri? Turkey); L. cf. canadensis: Bic (Co. de Rimouski? Quebec)? Tadoussac (Co. de Saguenay, Quebec), Mount Monadnock (Cheshire Co., New Hampshire); L. gredleri: Sommer- hausen (Bavaria? Germany); L. muscorum: Leinburg (Bavaria, Ger- many)? Ilgaz Dagi Ge~idi (Cankiri? Turkey); L. ''muscorum~' C: Maligne Canyon (Alberta); L. retractus: St. Simeon (Co. de Charlevoix-Est); L. sphagnicolus: L'Ascension (Co. de Chicoutimi, Quebec); D. pocahontas: Maligne Canyon (Alberta). Details on the collecting procedure, laboratory rearing, and the life histories and collecting sites are published elsewhere (Heinze, 1989, 1993; Heinze and Ortius, 1991; Heinze, Trunzer, Lechner and Ortius, 1995).
Brunswick, New Heinze et al.
Qukbec, Ontario, and New Brunswick; a morphologically similar species, though with a different chromosome number, Leptothorax "muscorum~~ C, perhaps identical to the variety L. muscorum septentt-ionah (Wheeler, 19 171, is found in the Canadian Rocky Mountains.
jackknifing over taxa (Lanyon, 1985) and by calculating a cophe- netic regression coefficient.
The current taxonomic confusion concerning the nearctic repre- sentatives of Leptothorax (s.str.) (e.g., Creighton, 1950; Brown, 1955; Francoeur et al., 1985; Heinze, 1989) makes a thorough morphological comparison between non-parasitic Leptothorax (s.str.) and the associated parasitic taxa difficult. Only few charac- ters appear to be stable enough to serve for species distinction (Table 2). The most reliable and most frequently cited characters are the suberect hairs on tibia and scapes in L. acervorum, L. sphagnicolus, Doronomyrmex, and Harpagoxenus, and the indented clypeus in L. gredleri, L. retractus, L. paraxenus, and to a lesser extent also Leptothorax sp. A (Table 2). Both characters, however, may vary between populations: L. acervorum from Alaska, for example, are considerably less hairy than central Euro- pean specimens (Heinze and Ortius, 1991). Other characters which serve to distinguish parasitic genera from Leptothorax (s. str.) are probably mostly adaptations to the parasites' specialized way of life and cannot be used to investigate phylogenetic relationships. Harpagoxenus, e.g., is easily recognized by strong, toothless mandibles and an extraordinarily large head with antenna1 scrobes, all obvious adaptations to slave-making. Similarly, the morpholog- ical features separating Doronomyrmex from Leptothorax are thought to be adaptations to the parasitic life, and some authors question whether Doronomyrmex should be kept as a distinct genus (Brown, 1973; Bolton, 1982).
Table 2. Morphological characteristics and chromosome numbers of Leptothorax (s.str.) and their parasites, based on Bolton (1982), Francoeur et al. (1985), Loiselle et al. (1990), and own observations.
have a standard palp formula of 5 maxillary palps and 3 labial palps, the number may be reduced to 4, 3 in Formicoxenus (Bolton, 1982). However, as shown by Francoeur et al. (1985), there is intergeneric and even intraspecific variation in palp formula in Formicoxenus. The palp formula is similarly reduced to 4, 3 in Leptothorax wilsoni (two queens from Jasper N.P., Alberta, and one individual from Escoumins, Quebec-the palp formula given in Heinze, 1989 for the type material needs to be confirmed by re- examination of material from the type locality) and Doronomyrmex pacis (two individuals from Jenner, Germany; according to Kutter, 1950 males of D. pads from Switzerland have a palp formula of 5, 4). Palp formula is therefore probably not very informative on genus level (Table 2).
Formicoxenus have scattered hairs on their compound eyes, whereas the eyes are thought to be hairless in Leptothorax (Fran- coeur et al., 1985). Hairy eyes, however, are found in L. wilsoni (Heinze, 1989; Table 2). Despite the superficial similarity between L. wilsoni and Formicoxenus in these two characters, L. wilsoni is nevertheless morphologically closer to Leptothorax in others, such as the scape length in males. L. wilsoni shares reduced mandibular dentition with Epimyrma, a slave-making satellite genus of Lep- tothorax (Myrafant), but clearly differs in palp formula and the shapes of petiole and postpetiole.
Most queens of workerless parasites in Formicoxenini, and per- haps of workerless parasitic ants in general, are extraordinarily small compared to queens of the host species (Douwes, 1990; Nonacs and Tobin, 1992). Queens of L. paraxenus are a notable exception, in that they are of similar size as the host queens. As small size is thought to be adaptive in parasites-parasite queens do not need much resources for colony founding and thus, a larger number of less well equipped, small queens can be produced from the same amount of energy available to the colony (Douwes, 1990)-the condition in L. paraxenus might reflect a recent origin from a non-parasitic ancestor.
Parasite queens are typically characterized by a broadened post- petiole, a strong ventral petiolar spine, and a larger Dufour's gland compared to their hosts. These features, however, are not restricted to social parasites but may be found to a varying degree also in the queens of free-living species such as Leptothorax sp. A and L. gredleri.
whereas their host L. cf. canadensis has 17 or 18 (Heinze and Buschinger, 1989; Loiselle et al., 1990). UPGMA clustering of Nei's indices calculated from seven enzyme systems which are of diagnostic value in the studied species results in the phenogram shown in Fig. 1. Original data and Nei's indices are given in Tables 3 and 4. Goodness of fit of the cluster analysis to the data was tested by comparing a matrix of cophenetic values, calculated from the tree matrix, with the origi- nal similarity matrix. The resulting cophenetic correlation of r = 0.809 suggests a rather mediocre fit (Mantel t-test, t = 6.53, p = 1.000). Nevertheless, the overall branching pattern is remarkably stable. Two fundamental dichotomies are found in all 21 Fig. 1. Phenogram obtained by UPGMA clustering of Nei's indices from electro- morph frequencies of several species of Leptothorax (s.str.), Doronomyrmex, Formi- coxenus quebecensis, and Harpagoxenus sublaevis. For abbreviations see Table 3.
species: Dgoe: 0. goesswaldi (9 virgin queens from 3 colonies); Dku: D. kutieri (8 virgin queens from 2 colonies); Dpac: D. pacis (5 virgin queens from 3 colonies); Dpoc: D. pocahontax (10 workers from 3 colonies); Fqu: Formicoxenus quebecewis (12 workers from 4 colonies from different populations); Hx: Harpapxenus sublae- vis (26 workers from 8 colonies); LA; L. sp. A (209 workers from 17 colonies; LaG, LaR, LaT: L. acervorum from Gropostheirn (Germany, 196 workers from 89 colonies), Reichswald (Germany, between 64 and 1420 workers from 10 to 140 colonies), and Ilgaz Dagi Gyidi (Turkey, 49 workers from 7 colonies); LC: Lep- tothorax C (10 workers from 4 colonies); LcB, kM, LcT: L. cf. canadensis from Bic (Quebec, ! 13 workers from 13 colonies), Mt. Monadnock (New Hampshire, 131 workers from 17 colonies) and Tadoussac (Qud~w. 66 workers from 10 colonies); Lgr: L. gredleri (between 20 and 299 workers from 29 colonies); hu, LmuT, L. muscorum from Reichswald (between 20 and 569 workers front 76 colonies) and Ilgaz Dagi Ge~idi (20 workers from 5 colonies); Lpm L. paraxenus (10 virgin queens from 4 colonies}; Let: L retractus (10 workers from 2 colonies); Lsp: L. sphagnicolus (10 workers from 2 colonies); h i : L witsod (8 virgin queens from 4 colonies).
The enzymes are Glucose-6-phosphate isomerase (GPI, referred to as PGI in Hei me, 1989, 199 1). Phosphoglucomutase (EM), 6-Phosphogluconate dehydmge- nase (PGD), Malate dehydrogenase (MDH), Ismitrate dehydrogenase (IDH), Matic enzyme (ME), and Lactate dehydrogenase (LDH). All species share the same elm- tromorph of tetrazolium oxidase. v, s, rn, n, f, and x denote different migration velocity during electrophoresis; blanks in the table indicate missing data.
and L. acervorum, as suggested by the phenogram in Fig. 1. It has recently been shown that D. pocahontas is not a workerless para- site and thus does probably not belong to the workerless Dorono- myrmex. The shiny, long-haired queens, morphologically similar to D. pacis but strikingly different from their nestmate workers, are probably a special morph of a species whose queens and workers are typically short-haired and dull (Buschinger and Heinze, 1993). In a previous study using cellulose acetate electrophoresis, "shiny" queens and workers of D. pocahontas from three colonies from the type locality differed from other studied species in having a very slowly migrating electromorph in the enzyme 6-Phosphogluconate dehydrogenase (PGD, Heinze 1989). According to the results of the present study with polyacrylamide gels, workers from three colonies with "dull" queens from the same collecting site, how- ever, predominantly had the slowly migrating PGD electromorph found commonly also in other taxa in cluster B (Table 3). In one colony, workers were heterozygous for the slow and the fast migrating electromorph. More data on this ant and morphologi- cally similar taxa from the Rocky Mountains are needed to eluci- date the status of D. pocahontas.
L. paraxenus differs from its host, L. cf. canadensis in several enzymes (Table 3) and is attached to cluster B. L. wilsoni is closely associated neither with one of its two hosts, L. cf. canadensis and L. sp. A, nor with Formicoxenus, but is more similar to species in cluster A than to cluster B species.
In a neighbor joining tree, which, however, showed poorer fit to the original data (r = 0.691, t = 5.174, p = 1.000), F. quebecensis is attached to L. retractus and L. cf. canadensis, whereas L. wilsoni and Harpagoxenus are closer to the taxa of cluster B. Morphology, allozyme phenotype, and chromosome number were compared to analyze the evolution of workerless social para- sites in the ant tribe Formicoxenini. Though the data are as yet not sufficient for a thorough cladistic analysis, similarities in morpho- logical and biochemical characters which I consider to be neutral in natural selection support the results of previous more qualitative studies (Buschinger, 198 1, 1990; Heinze, 199 1).
The slave-making and workerless parasites studied here appear to be phylogenetically close to their hosts. Though the workerless L. wilsoni and the guest-ant genus Formicoxenus differ in several enzyme systems and morphological features from other taxa inves- tigated in this study, they clearly belong to the Formicoxenini and within this tribe are probably closer to Leptothorax (s.str.) and its parasites than to Leptothorax (Myrafant) or other Leptothorax sub- genera (see also Buschinger, 1981; Francoeur et al., 1985; Heinze, 1991). Harpagoxenus slave-makers and workerless Leptothorax and Doronomyrmex clearly cluster with species of Leptothorax (s.str). The data thus support what has been called "a loose version of Emery's rule." In 1909, Emery suggested for slave-makers and workerless parasites that they "all originate from closely related forms which serve them as slave or host species," based on mor- phological similarities between parasites and hosts. Ward (1989) proposed to distinguish between a loose form of Emery's rule- parasites and their hosts are close relatives (see also Wasmann, 1909)-and a strict form-for a given parasite-host pair, the sister group of the parasite lineage includes the host species (Ward, pers. comm.). The loose version appears to hold in all host-parasite pairs investigated so far (Ward, 1989; Agosti, 1994; Sanetra, Heinze and Buschinger, 1994), with exception of guest ants which explicitly were never included in this rule. A relationship as suggested by the strict version, resulting from sympatric or allopatric speciation, cannot be disproven for some formicoxenine ants. Allozyme simi- larities suggest a close relationship between at least two of the three palaearctic, workerless Doronomyrmex and their common host, L. acervorum, as previously deduced from morphological characters (e.g., the presence of suberect hairs on scapes and tibia (Buschinger, 1990)), sequence comparisons of a mitochondria1 cytochrome b gene (Baur, Sanetra, Chalwatzis, Buschinger and Zimmermann, 1995), and an internal transcribed spacer adjacent to the 5.8s rRNA gene (Baur, Sanetra, Chalwatzis, Buschinger and Zimmermann, 1996). On the other hand, L. acervorum, L. gredleri, L. muscorum, and other taxa in cluster B are very similar in almost all studied enzyme systems, and it therefore cannot be ruled out that the three Doronomyrmex originated jointly or independently from ancestors other than L. acervorum.
Morphological similarities between the Doronomyrmex species and L. acervorum might be convergent adaptations to parasitic life with a common host species instead of synapomorphies. Morpho- logical traits of parasites might serve to "camouflage" the parasite in the host colony or to increase the parasite queen's colony found- ing success. Hair length, e.g., may vary within a monophyletic group, perhaps in response to the condition in the host: the degen- erate slave-maker Epimyrma kraussei has long hairs like its host, Leptothorax recedens, but much other data suggests a common ori- gin of long- and short-haired Epimyrma (Buschinger, 1989). In any case, the result that the workerless Doronomyrmex are closer to some Leptothorax (s.str.) (cluster B) than to others (cluster A) clearly corroborates the view that the genus Doronomyrmex ought to be synonymized under Leptothorax (s.str.) (Brown, 1973; Bolton, 1982). Alternatively, Leptothorax (s.str.) would be a para- phyletic taxon. I therefore propose to synonymize Doronomyrmex under Leptothorax (s.str.).
The strict version of Emery's rule is not supported in L. para- xenus and L. wilsoni. Both parasites are clearly distinct in morphol- ogy, karyotype, and enzyme pattern from their common host, L. cf. canadensis. L. wilsoni was recently found in colonies of a second host species, Leptothorax sp. A (Heinze et al., 1995), but a closer phylogenetic relationship between them also appears unlikely based on morphology and enzyme patterns.
has previously been considered by West-Eberhard (1990) and Bourke and Franks (1991) to explain the occurrence of parasite- host pairs only loosely following Emery's rule: in a species with alternative reproductive strategies, a phenotype adapted to para- sitizing conspecific colonies might have switched from its conspe- cific ancestral host to a new host species. This study was supported by the Deutsche Forschungsgemein- schaft (Heisenberg-grant He 162316-1). I thank S. Trenkle for tech- nical assistance, S. Kauffmann, B. Hulsen, S.P. Cover, T.M. Alloway and others for help in the field, and A. Buschinger and R. Schumann for material of L, wilsoni and Formicoxenus quebecen- sis from populations in western North America. P. S. Ward, Univ. of California, Davis, provided helpful comments on the manu- script.
Agosti, D. 1994. A new inquiline ant (Hymenoptera: Formicidae) in Cataglyphis and its phylogenetic relationship. J. Nat. Hist. 28:918-919. Allies, A.B., A.F.G. Bourke, and N.R. Franks. 1986. Propaganda substances in the cuckoo ant Leptothorax kutteri and the slave-maker Harpagoxenus sublaevis. J. chem. Ecol. 12: 1285-1293.
Baur, A., N. Chalwatzis, A. Buschinger, and F.K. Zimmermann. 1995. Mitochon- drial DNA sequences reveal close relationships between social parasitic ants and their host species. Curr. Genete. 28:242-247. Baur, A., M. Sanetra, N. Chalwatzis, A. Buschinger, and F.K. Zimmermann. 1996. Sequence comparisons of the internal transcribed spacer region of ribosomal genes support close relationships between parasitic ants and their respective host species (Hymenoptera: Formicidae). Insectes Soc. 4353-67. Bolton, B. 1982. Afrotropical species of the myrmicine ant genera Cardiocondyla, Leptothorax, Melissotarsus, Messor and Cataulacus (Formicidae). Bull. Brit. Mus. Nat. Hist. 45:307-370.
Bolton, B. 1994. Identification Guide to the Ant Genera of the World. Harvard Uni- versity Press, Cambridge, Massachusetts. Bourke, A.F.G., and N.R. Franks. 1991. Alternative adaptations, sympatric specia- tion and the evolution of parasitic, inquiline ants. Biol. J. Linn. Soc. 43:157-178.
Brown, W.L., Jr. 1955. The ant Leptothorax muscorum Nylander in North America. Ent. News 66:43-50.
Brown, W.L., Jr. 1973. A comparison of the Hylean and Congo-West African rain forest ant faunas. In: Tropical forest ecosystems in Africa and South America: a comparative review (Eds. Meggers, B.J., E.S. Ayensu, and W.D. Duckworth), Smithsonian Inst. Press, Washington, 161-185 p.
Buschinger, A. 1971. Zur Verbreitung der Sozialparasiten von Leptothorax acervo- rum (Fabr.) (Hym., Formicidae). Bonner Zool. Beitr. 22: 322-33 1. Buschinger, A. 1974. Zur Biologie der sozialparasitischen Ameise Leptothorax goesswaldi Kutter (Hym., Formicidae). Insectes SOC. 21 : 133-144. Buschinger, A. 1981. Biological and systematic relationships of social parasitic Leptothoracini from Europe and North America. In: Biosystematics of social insects (Eds. P.E. Howse and J.-L. Clement), Academic Press, London, 21 1-222 p. Buschinger, A. 1982. Leptothorax faberi n.sp., an apparently parasitic ant from Jasper National Park, Canada (Hymenoptera, Formicidae). Psyche 80: 197-209. Buschinger, A. 1986. Evolution of social parasitism in ants. Trends Ecol. Evol. 1: 155-160.
Buschinger, A. 1987. Biological arguments for a systematic rearrangement of the ant tribe Leptothoracini. In: Chemistry and biology of social insects (Eds. Eder, J. and H. Rembold), J. Peperny, Miinchen, p. 43. Buschinger, A. 1989. Evolution, speciation, and inbreeding in the parasitic ant genus Epimyrma (Hymenoptera, Formicidae). J. evol. Biol. 2:265-283. Buschinger, A. 1990. Sympatric speciation and radiative evolution of socially para- sitic ants-heretic hypotheses and their factual background. Z. Zool. Syst. Ev01.-Forschung. 28:241-260.
Buschinger, A., and K. Fischer. 1991. Hybridization of chromosome-polymorphic populations of the inquiline ant, Doronomyrmex kutteri (Hym., Formicidae). Insectes SOC. 38:95-103.
Buschinger, A., and J. Heinze. 1993. Doronomyrmex pocahontas: not a workerless parasite but still an enigmatic taxon (Hymenoptera, Formicidae). Insectes Soc. 40:423-432.
Buschinger, A*, and B. Klump. 1988. Novel strategy of host-colony exploitation in a permanently parasitic ant, Doronomyrmex goesswaldi. Naturwissenschaften 75:577-578.
Buschinger, A., and R.D. Schumann. 1994. Records of Leptothorax wilsoni Heinze 1989, from western North America. Psyche 101 : 13-1 8. Buschinger, A., H. Cagniant, W. Erhardt, and J. Heinze. 1988. Chalepoxenus brun- new, a workerless "degenerate slave-maker" ant (Hymenoptera, Formicidae). Psyche 95:253-263.
Buschinger, A., R.D. Schumann, and J. Heinze. 1994. First records of the guest ant Formicoxenus quebecensis Francoeur from western Canada (Hymenoptera: Formicidae). Psyche 101 :53-57.
Douwes, P. 1990. Morphology of the parasitic myrmicine ant. In: Social insects and the environment (Eds. Veeresh, G.K., B. Mallik, and C. A. Viraktamath). Oxford & IBH, New Delhi, 147-148 p.
Emery, C. 1909. ~ber den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen. Biol. Centralbl. 29:352-362. Faber, W. 1969. Beitrage zur Kenntnis sozialparasitischer Ameisen. 2. Aporomyrmex ampeloni nov. gen., nov. spec. (Hym. Formicidae), ein neuer per- manenter Sozialparasit bei Plagiolepis vindobonensis Lomnicki aus osterreich. Pflanzenschutz Ber. 39:39-100.
Fischer, K. 1987. Karyotypuntersuchungen an selbstandigen und sozialparasitischen Ameisen der Tribus Leptothoracini (Hymenoptera, Formicidae) im Hinblick auf ihre Verwandtschaftsbeziehungen. unpubl. Ph.D. thesis, TH Darmstadt. Francoeur, A. 1986. Deux nouvelles fourmis nkarctiques: Leptothorax retractus et Leptothorax sphagnicolus (Formicidae, Hymenoptera). Can. Ent. 118:1151-1164.
Francoeur, A., R. Loiselle, and A. Buschinger. 1985. Biosyst6matique de la tribu Leptothoracini (Formicidae, Hymenoptera). 1. Le genre Formicoxenus dans la region holarctique. Naturaliste can. (Rev. ~col. Syst.) 11 2:343-403. Franks, N.R., M. Blum, R.-K. Smith, and A.B. Allies. 1990. Behaviour and chemi- cal disguise of cuckoo ant Leptothorax kutteri in relation to its host Leptothorax acervorum. J. chem. Ecol. 16: 1431-1444. Heinze, J. 1989. Leptothorax wilsoni n. sp., a new parasitic ant from eastern North America (Hymenoptera: Formicidae). Psyche 96:49-6 1. Heinze, J. 1991. Biochemical studies on the relationship between socially parasitic ants and their hosts. Biochem. Syst. Ecol. 19:195-206. Heinze, J. 1993. Habitat structure, dispersal strategies and queen number in two boreal Leptothorax ants. Oecologia 96:32-39. Heinze, J., and T.M. Alloway. 1991. Leptothorax paraxenus n. sp., a workerless social parasite from North America (Hymenoptera: Formicidae). Psyche 98: 195-206.
Heinze, J., and A. Buschinger. 1987. Queen polymorphism in a non-parasitic Lep- tothorax species (Hymenoptera, Formicidae). Insectes Soc. 34:28-43. Heinze, J., and A. Buschinger. 1988. Polygyny and functional monogyny in Lep- tothorax ants (Hymenoptera: Formicidae). Psyche 95:309-325. Heinze, J., and A. Buschinger. 1989. Queen polymorphism in Leptothorax spec. A: its genetic and ecological background (Hymenoptera: Formicidae). Insectes Soc. 36: 139-155.
Heinze, J., and S. Kauffmann. 1993. The socially parasitic ants of Turkey. Zool. Middle East 8:3 1-35.
Heinze, J., and D. Ortius. 1991. Social organization of Leptothorax acervorum from Alaska (Hymenoptera: Formicidae). Psyche 98:227-240. Heinze, J., and T.A. Smith. 1990. Dominance and fertility in a functionally monog- ynous ant. Behav. Ecol. Sociobiol. 27: 1-10. Heinze, J., N. Lipski, and B. Holldobler. 1992. Reproductive competition in colonies of the ant Leptothorax gredleri. Ethology 90:265-278. Heinze J., R.J. Stuart., T.M. Alloway, and A. Buschinger. 1992. Host specificity in the slave-making ant Harpagoxenus canadensis M.R. Smith. Can. J. Zool. 70: 167-170.
Heinze, J., B. Trunzer, K. Lechner, and D. Ortius. 1995. A second host species of the inquiline ant Leptothorax wilsoni. Psyche 102:73-77. Holldobler, B., and E.O. Wilson. 1990, The Ants. Belknap Press of Harvard Univer- sity Press, Cambridge, Massachusetts.
Imai, H.T., R.H. Crozier, and R.W. Taylor. 1977. Karyotype evolution in Australian ants. Chromosoma 59:341-393.
Kutter, H. 1950. ~ber Doronomyrmex und verwandte Ameisen. Mitt. Schweizer. Entomol. Ges. 23:347-353.
Kutter, H. 1969. Die sozialparasitischen Ameisen der Schweiz. Vierteljahresschr. Naturforsch. Ges. Zurich 1 13: 1-62.
Lanyon, S.M. 1985. Detecting internal inconsistencies in distance data. Syst. Zool. 34:397403.
Loiselle, R., A. Francoeur, and A. Buschinger. 1990. Variations and taxonomic sig- nificance of the chromosome numbers in the nearctic species of the genus Lep- tothorax (s.s.) (Formicidae: Hymenoptera). Caryologia 43: 32 1-334. Nonacs, P., and J.E. Tobin. 1992. Selfish larvae: development and the evolution of parasitic behavior in the Hymenoptera. Evolution 46: 1605-1 620. Provancher, L. 1887. Fam. 10 - Les Formicides. In Additions et corrections au vol- ume 2 de la faune entomologique due Canada, traitant des Hymenoptkres, p. 224-249, Quebec.
Rohlf, F.J. 1990. NTSYS-pc. Numerical taxonomy and multivariate analysis sys- tems. Exeter, New York.
Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425. Sanetra, M., J. Heinze, and A. Buschinger. 1994. Enzyme polymorphism in the ant genus Tetramorium Mayr and its social parasites (Hymenoptera: Formicidae). Biochem. Syst. Ecol. 22:753-759.
Ward, P.S. 1989. Genetic and social changes associated with ant speciation. In: The Genetics of Social Evolution (Eds. Breed, M.D., and R.E. Page). Westview Press, Boulder, Colorado, p. 123-148.
Wasmann, E. 1908. Weitere Beitrage zum sozialen Parasitismus und der Sklaverei bei den Ameisen. Biol. Centralbl. 28:257-271. Wasmann, E. 1909. ~ber den Ursprung des sozialen Parasitismus, der Sklaverei und der Myrmekophilie bei den Ameisen. Biol. Centralbl. 29:683-703. West-Eberhard, M.-J. 1990. Parallel size-related alternatives in males and females and the question of sympatric speciation in Hymenopteran social parasites. In: Social Insects and the Environment (Eds. Veeresh, G.K., B. Mallik, and C.A. Viraktamath). Oxford & IBH, New Delhi, p. 162-163. Wheeler, W.M. 1910. Ants. Columbia University Press, New York. Wheeler, W.M. 1917. The mountain ants of western North America. Proc. Am. Acad. Arts Sci. 52:457-569.
Wilson, E.O. 197 1. The Insect Societies. Belknap Press of Harvard University Press, Cambridge, Massachusetts.
Further investigations since the submission of the manuscript have led to small changes in allele frequencies, which slightly affect the branch- ing pattern in cluster B. The overall pattern, however, remained stable.