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Biochemical Studies on the Relationship Between Socially Parasitic Ants and Their Hosts

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Biochemical Studies on the Relationship Between Socially Parasitic Ants and Their Hosts BiochemicalSystematics and Ecology,Vol. 19, No. 3, pp. 195-206, 1991. 0305-1978/91 $3.00 + 0.00 Printed in Great Britain. © 1991 Pergamon Press DIc. Biochemical Studies on the Relationship Between Socially Parasitic Ants and Their Hosts JORGEN HEINZE Zool. Inst. II, R6ntgenring 10, 8700 WQrzburg, F.R.G. Key Word Index--Doronomyrmex; Harpagoxenus; Leptothorax; Formicidae; Hymenoptera; social parasites; Emery's rule; electrophoresis. Abstract--Analysis of enzyme patterns suggests close phylogenetic relationships between socially parasitic ants of the genera Harpagoxenus and Doronomyrmex and their Leptothorax hosts. Doronomyrmex goess- wa/di and D. kutteri are indistinguishable in enzyme patterns from their host, Leptothorax acervorum. A newly discovered workerless parasite from Canada, L. paraxenus, however, appears to be more closely related to other non-parasitic species than to its host, L. sp.B (= L. canadensis?). The results are discussed with respect to current hypotheses on the evolution of social parasites. Introduction Ants are among the most successful and most abundant insects on Earth. They can be found in the most diverse habitats, and they build their nests almost everywhere: in soil, litter, tree stumps, rock crevices, the mounds of termites and the colonies of other ant species. Among the latter are the social parasites: ants which are no longer capable of feeding themselves or tending their own larvae, but which instead rely on the help of workers from other species. About three per cent of the approximately 9000 ant species are known to lead a permanent or temporary parasitic life [1]. The freshly inseminated queens of social parasites invade the colonies of other species which they parasitize by begging food and letting the hosts take care of their brood. Queens of the north and central European slave-maker Harpagoxenus sub/aevis, for example, kill or expel the host queen and the adult workers. Workers which eclose from the conquered host brood forage, provide the parasites with food, and nurse the Harpagoxenus larvae. The original host workers die within a year or two and have to be replaced. Hence, Harpagoxenus workers perform slave-raids, during which they pillage neighbouring colonies of the host species and carry away their pupae. The queens of some workerless parasites, such as Doronornyrmex kutter/and D. goess- wa/dl; sneak into a host nest, where they are tolerated by the resident ants. They produce sexual offspring but none of their own workers. Whereas D. kutter/is an inquiline, which peacefully lives alongside the fertile host queens, D. goesswa/d/'is a host queen-intolerant parasite. For more than a hundred years biologists have speculated on the evolutionary origin of social parasitism. With the exception of guest ants (see below), social para- sites are often morphologically very similar to their hosts, and in 1909 Carlo Emery concluded that "the slave-making, temporarily and permanently parasitic ants orig- inate from closely related forms which serve them as hosts" [2]. Today, a loose version of "Emery's rule'--parasitic ants and their hosts are closely related--is widely accepted. It has also been suggested that in particular the workerless parasites have evolved intraspecifically from their host species [3-5]. Permanent social parasites are extremely rare. Several species have been found only once and, despite extensive and repeated searches at the typical localities, only museum material is available. The close relationship of parasites and hosts therefore has usually been inferred from (Received 16 November 1990) 195 196 J. HEINZE morphological resemblance rather than detailed phylogenetic analysis [6]. Though electrophoretic data are now commonly used to reconstruct phylogenies of social insects [7], genetic investigations of parasites and their hosts are still comparatively rare. In wasps and bees, it has been inferred from enzyme polymorphisms that cuckoo bumble bees (Psithyrus spp.) are a monophyletic group which radiated secondarily to several host species [8], and that the parasitic wasps are of polyphyletic origin [9] (but see [10, 11]). In ants, the distribution of esterase allozymes suggests that small queens (microgynes) in the nests of Myrmica rubra are genetically isolated from large queens (macrogynes) and presumably belong to a separate, parasitic species [12]. During the last few decades, several teams have intensively studied the parasite- rich myrmicine tribe Leptothoracini. In suitable habitats, these little and inconspicuous ants form dense populations and, in some places, parasites can regularly be collected. Thus, Leptothorax parasites are among the best studied socially parasitic ants, and they are the ideal species for a first biochemical approach toward Emery's rule. Electro- phoresis has already been used in a number of leptothoracine species to estimate the relatedness between nestmates [13-15] and to clarify the taxonomic position of species [16, 17]. Inter- and intraspecific genetic diversity is low, and esterase or dehydrogenase isozymes have successfully been used to characterize taxa or to distin- guish between sibling species [17-19]. As part of a study on the systematics of the nearctic Leptothorax "muscorum" complex, it was possible to collect data on the variability of enzymes in a number of socially parasitic species and their hosts. A first qualitative analysis of esterase banding patterns [19] had already supported recent ideas for a systematic revision of the whole tribe [20, 21]. In this paper, more detailed electrophoretic data from parasitic Leptothoracini and their hosts, especially of the genera Leptothorax (s.str.), Doronornyrmex, and Harpagoxenus, are presented. In temperate North America and Eurasia, the complex genus Leptothorax is represented mainly by three subgenera: Leptothorax(s.str.) (= Mychothorax), Myrafant, and Temnothorax.Most of 350 or more named taxa of Leptothoraxare ordinary non- parasitic species. A few are workerless parasites and one species, L. duloticus, is a slave-maker (Table 1). The genus Doronomyrmexcomprises only workerless parasites of L. (s.str.) (with the exception of the dubious D. pocahontas), and the three species of Harpagoxenus available in this study are active slave-makers, with H. canadensisand H. sublaevis enslaving colonies of Leptothorax(s.str.), but H. americanusfound only in nests of Myrafant. Finally, Formicoxenus quebecensis is a guest ant and lives in the nests of Myrrnica alaskensis. Guest ants can be found in colonies of various ant species, to whom they are not closely related. They beg food from their hosts but take care of their brood themselves. The genus Formicoxenusbelongs to the Leptothoracini and has been thought to be closely attached to the subgenus Leptothorax(s.str.) [22]. Materials and Methods Complete colonies of host species were collected during the past five years in numerous localities in North America and Central Europe. Social parasites were collected in the following sites: Doronomyrmex kutteri: Nyehusen, Sweden; Doronomyrmex goesswaldi and D. pacis: La Villette, France; Doronomyrrnex pocahontas: Maligne Canyon (Jasper N. P., Alberta); Harpagoxenus canadensis: St. Sim6on (Comt~ de Charlevoix-Est, Quebec), Tadoussac (Saguenay Co., Qua.), Rouyn-Noranda (Temiscamingue Co., Qua.), MacKenzie Mountain (Inverness Co., Nova Scotia); /4. sublaevis: Nfirnberger Reichswald, F.R.G.; Leptothorax paraxenus; Milton, Ontario; L. wilsoni: Moncton (Westmoreland Co., New Brunswick); Formicoxenus quebecensis: Waswanipi (Co. de Abitibi, Qua.). Single workers, males and females were crushed individually in 40 ill running buffer with 15% glycerol and 0.01% bromothymol blue. Proteins were separated in 12.5-cm-long 7.5% polyacrylamide gels (gel buffers: 0.47 M Tris-HCI, pH 8.8 and 0325 M Tris-HCI, pH 8.0 for phospho- glucose isomerase (PGI); running buffer 036 M glycine, 0.025 M Tris, pH 8.3) at 10°C with a current of approxi- mately 10-20 mA for 3 h, and on 7.5- or 13-cm-long cellulose acetate plates (Cellogel, Milano, and Helena Laboratories, Beaumont, Texas; gel buffer and running buffer: 0.01 M sodium phosphate/citrate, pH 6.4) with a constant voltage of 200 or 350 V for 1.5 h. Dehydrogenases were stained using the following reagents: 2 mg BIOCHEMICAL STUDIES ON PARASITIC ANTS AND HOSTS 197 TABLE 1. RANGE OF THE NON-PARASITIC SPECIES OF LEPTOTHORAX (S.STR.) AND OF THE SOCIALLY PARASITIC SPECIES OF LEPTOTHORAX, HARPAGOXENUS AND DORONOMYRMEX, BASED ON [1 ] AND AUTHOR'S OBSERVATIONS. SPECIMENS OF THE SPECIES PRINTED IN BOLD LETTERS WERE EXAMINED IN THIS STUDY Non-parasitic Typical habitat Known range L. acervotum Alpine and boreal Holarctic (Fabricius, 1973) coniferous forests occasionally in deciduous forests L. muscorum Alpine and boreal Palaearctic (Nylander, 1846) coniferous forests L. gredleri Light pine stands, rose and Central Europe (Mayr, 1855) blackthorn thickets L. scarnni Alpine coniferous forests Caucasus, Pontus (Ruzsky, 1905) L. craesipilis Pine and cottonwood forests U.S. Rocky Mts (Wheeler, 1917) L tetractus Alpine and boreal Nearctic (Francoeur, 1986} coniferous forests L spagnico/us Spruce bogs Central Quebec (Francoeur, 1986) L. sp.A Open alpine and boreal Eastern North America coniferous forests L. sp.B Boreal coniferous forests, Eastern North America occasionally in deciduous forests L. sp.C. Alpine coniferous forests Canadian Rocky Mts L. sp.D Alpine coniferous forests Canadian Rocky Mrs Parasite Host species Known range Type of parasitism L. faberi L. sp.D Jasper N. P.,
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