- Email: [email protected]
Evolution of social parasitism in ants
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Slave raids of Amazon ants, the 6eheading of the host colony’s queen by a parasitic Bothriomyrmex female, or the protracted throttling of the host queen by an Epimyrma female which has penetrated a Leptothorax nest, are among the most intriguing Cehaviors to 6e observed in social parasitic ants. The evolutionary origin of thesebehaviors, however, is quite obscure, and further work is needed to elucidate how parasitic fife cycles could have arisen from the ordinary social organization of ants. Social parasitism, as understood in this article, refers to parasitehost relationships between any two species of social insects. As cuckoos exploit the parental care of their hosts, so social parasitic wasps, bees and ants utilize the social accomplishments of other, independent species. The types of social parasitism in ants Social parasitism occurs in a,variety of manifestations, partictirly in ants: so-called guest relations or xenobiosis, temporary parasitism, permanent parasitism with slavery (dulosis) and without slavery (inquilinism). These four basic types can be summarized briefly as follows. A detailed survey is provided by Wilson ’ Guest ants The guest ants of theayrmicine tribe Leptothoracini (now all attributed to one apparently monophyletic genus, Formicoxenus*), have small colonies with up to about a hundred individuals. They live within the nest material or the nest walls of their hosts, which are much bigger species of the genera Formica or Myrmica with large, populous nests. The Formicoxenus build their own little nests well separated from the brood chambers of the hosts, and they themselves care for their brood. They are dependent upon the hosts only with respect to nutrition. Formicoxenus may either beg for regurgitated food directly from a Formica or Myrmica worker, or participate in food exchange (trophallaxis) between two host workers. A guest ant may climb over Alfred Buschinger is at the lnstitut fib Zoologie, 61 Darmstadt, Technische Hochschule, Schnittspahnstr. 3, FRG. This article is dedicated to Heinrich Kutter on the occasion of his 90th birthday. @ 1986. Eleewer Science PubIshers
6 V Amsterdam
Evolutionof SocialParasitism in Ants Alfred Buschinger the legs and dorsum of a Formicu to reach its head, and then lick the food droplet being transferred to another host ant. The trophic parasitism of the guests ants may have evolved from plesiobiosis (the habitual nesting of two ant species in very close vicinity), which is often observed in nature. Temporary parasitism In temporary parasitism, the parasitic species depends on a host species only for foundation of new colonies. Usually, the parasitic queen, after her nuptial flight and insemination, tries to penetrate a host colony where she replaces the original queen. From the parasite’s eggs, a worker force develops with the aid of the host colony workers; the latter finally disappear due to natural aging and losses, and the colony becomes a pure society of the parasitic species. Some peculiar behaviors of the queens have been observed during colony foundation. In Lasius umbratus, the female grasps and chews a worker of the host species (L. niger) and then enters the host nest. There she is said to become more attractive than the original queen3, which finally dies of starvation or is expelled horn the colony. A closely related species, L. reginae, after invading a nest of L. alienus suddenly attacks the much bigger host queen and throttles her to death’ (Fig. I).
Bothriomyrmex decapitans and other species of this genus, in the same situation, cut off the head of the host species queen (of the genus Tapinoma14. Lmsius fuliginosus exhibits a social hyperparasitism in that the queen founds her colonies with the aid of L. umbra&s which is itself a temporary parasite. Temporary parasitism also occurs in several species of wood ants of the Formica rufa group; in some species the queens may either penetrate a Serviformica sp. nest, or join a polygynous nest of their own species. Such colonies then reproduce by budding, often forming huge multinest supercolonies’. Permanent parasitism with slavery The permanently parasitic species depend upon the hosts throughout their lives. In the case of the slavemaking ants, the young queens have to penetrate a host species nest, kill or drive out all adults, and take over the brood. From these pupae emerge the first slaves, and with their aid a number of slavemaker workers are subsequently produced. These workers are often unable to forage, to feed the larvae, or even to eat by themselves. On the other hand, they are usually predisposed for fighting, being equipped with specialized piercing mandibles (as in Polyergus and Strongspecies’r5) or with ylognathus
Fig. I. A temporary parasitic ant queen. lnsius reginac; she penetrates a host species colony (L. alienus) and kills the host queen by throttling her. A similar behavior has evolved convergently in the genus Epimyrma (Fig. 51, which (in contrast to the formicine genus Ltsius) belongs to the subfamily Myrmicinae. Reproducedby permission of Bundewnstalt fiir Ppanznschutz, Wien.
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Fig.2. Scanning electmn micrographs of the heads of slavemaking ants and their slaves. The white bars represent Imm. (a) Polyergusn&tens, the Amazon ant, with saber-shaped mandibles: lb) oneof its slave species, Semiformira lemani, with normally dentate mandibles. Both (at and fbl belong to the subfamily Formicinae. lc) Strongylognathus alpinus, with cowergently evolved piercing mandibles; Id) its slave, Tetramorium aespitum. Both ICI and (d) belong to the subfamily Myrmicinae. fel Harpagwnus sublaevis,a slavemaker with scissorlike toothless mandibles for cutting off the appendages of an opponent; If) Leptotlrorax awwrum, one of its slave species. Both let and (f) belong to the subfamily Myrmicinae. Pictures taken 6y A. Maiazra. FBI I, TH Darmstadt.
toothless mandibles for cutting off the appendages of their opponents (as in Harpugoxenus su6hevis’.6) (Fig. 2). Others have strong stings (CXulep~xenus’l, or produce aggressive glandular secretions or ‘propaganda’ substances (RaptiformLa’L They attack independent, neighbouring colonies of the host or slave species, fight against the defenders, and finally carry back brood to the slavethe maker’s nest. Thus, the slave stock may be replenished several times a year’.
Permanent parasitism without slavery Permanent parasites which do not use slaves often lack a worker caste. The females usually coexist with the host species queens in their nest, the parasite brood being reared by the host workers simultaneousiy with their own larvae. In a few instances, e.g. Anergates atratulus, the parasite apparently invades only queenless host species colonies, whereas the ‘ultimate parasite’ Telewtomyrmex scltneideri rides like an ectoparasite on the back of the host colony queen (Fig. 31*.
Frequency and systematic distribution of parasHic ants Among the estimated IOOOO12 000 ant species on earth, the parasitic forms (about 200 species) represent but a small fraction. However, most parasitic ant species are rare and not easily found in the host species populations and colonies; thus the actual number of parasitic species might be considerably higher. Every year some new species are detected, and in a very well known fauna, such as in Switzerland, about one third of the - t 10 ant species is parasitic5. So we may expect that the number of known parasitic species will increase, particularly in the tropics”. The distribution of social parasitic species among the I I living ant subfamilies is surprising. Although the subfamilies apparently do not differ fundamentally in their form of social organization, social parasites are known mainly in the Myrmicinae and the Formicinae (with about 33 and 9 genera respectively). Although some subfamilies comprise few species, it is difficult to understand why parasites are lacking in, for instance, the large subfamily Ponerinae. Moreover, among the myrmicines and formicines the parasitic species are again concentrated, in only a few genera’. A survey of the parasites in different subfamilies reveals that the main types of parasitic life habits (inquilinism, dulosis, and temporary parasitism) have evolved convergently within both the Formicinae and Myrmicinae, temporary parasitism among the Dolichoderinae (one genus, Botkriomyrmex) and Pseudomyrmecinae, and inquilinism in a genus of the Myrmeciinae’,“. Within the myrmicine tribe Leptothoracini alone, slavemaking has apparently evolved five times independently9.12 with different groups of host species, inquilinism at least twice17, and xenobiosis once2. Wilson’” assumes an independent, convergent evolution of nine parasitic species from the myrmicine genus Plreidole. This polyphyletic origin of very similar parasitic life cycles means that there may be certain widespread features of normal social behavior which often become the starting point for parasitic evolution’2.
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Evolutionary progression in parasitic ants In the evolution of parasitism we have to distinguish between the origin of parasitic life habits, which will be dealt with in the following section, and the evolution of life cycles and behavior within parasitic species groups. Considerable progress has been achieved during the past few years, mainly with respect to the latter question. As mentioned above, the guest ants of the genus Formicoxenus are apparently monophyletic*; the frequent coexistence of different ant species nests in close proximity has, surprisingly, not often led to the evolution of xenobiotic relations. There is only one other group (the genus Megafomgrmex) known to exhibit this habit’. Within the guest ant genus Formicoxenus, however, we can observe certain trends which may or may not be affected by their parasitic life habits. The most primitive, or least specialized, form has normal males with wings and black coloration, as in most ants. In other, more derived, species the males become polymorphic, some of them hatching without wings; and in the most specialized F. nitidulus the males are wingless, brown and similar to workers in appearance. The queens in Formicoxenus are generally polymorphic, some being alate, others workerlike, and many intermediate in shape. In fact, queen polymorphism is not unusual in parasitic ants, and is particularly common in the leptothoracines (to which Formicoxenus belongs). For the wood ants (Formica and allied genera), an evolutionary line was long ago proposed by Darwin14; it began with brood predation for food, and led via the facultative slavery of the subgenus Raptiformica to the obligatory dulosis of the Amazon ants, genus Polyergus. More recently, a workerless inquiline, F. talbotae, has been detected in this groupi5. Whether this species is a descendant of a temporary parasitic ancestor, or is derived directly from an independent polygynous form, is open to question. Among the leptothoracines, an evolution from slavemaking species to workerless forms has been documented in the genus Epimgrma. The life history of this genus, its
gastric old queen are shown on top of the host queen, a host species worker is in front of the queen 6u oermission of erouo. Drawina 6u W. tinsenmaier. rearoduced
seemingly ‘remarkably clear evolutionary progression leading from temporary social parasitism to full inquilinism’ (as was summarized for the last time by Wilson? has to be rewritten completely, however. In this genus there is neither a temporary parasite nor a typical full inquiline. Instead, four species conduct well-organized slave raids with group recruitment and stingfighting (Fig. 4); during colony foundation the young queen throttles the host colony queen over weeks or even months (Fig. 5) until she finally dies. In a second group of Epimgrma species the number of workers is drastically reduced to only about 3-5; slave raiding in this group evidently cannot be effective, even though the workers are still able to perform all raiding
Fig. 4. Two Epimyrma ravouxi slavemakers colony.
activities. Finally, two species have been found without any Epimyrma workers: nevertheless, the young queens still throttle the host queens to death and thus differ from true inquilines which coexist with the host species queens”-“. Simultaneously in this genus, an evolution from normal swarming behavior of the alate sexuals to mating in the mother nest, and thus inbreeding, has been found. Three of the slave-raiding species make mating flights; one (E. algeriana) mates inside the nest, and all the ‘degenerate slavemakers’ and the workerless species also do SO’~*~‘. Among the inquilines, two significantly different evolutionary pathways may have been followed. On the one hand, there are some morphologically highly specialized and
sting a Leptothoraw unifasciatus worker defending
the raided
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[email protected]. Like the temporary parasitic Lasius reginae (Fig. I). the Epimynna algeriana queen penetrates a host soecies nest for colonv foundation and throttles the host queen, sometimes for weeks, until she is dead. Photo 6y W. Ek&dt.
apparently ‘old’ forms like Teleutomyrmex (Fig. 3) and Anergates, the latter having males which look strangely immature and pupa-like. For these parasites a long evolutionary history is assumed, perhaps including descent from slavemakers’e5. Their particular morphological characters, which in part occur also in other types of social parasites, are termed ‘the anatomsyndrome’ by ical parasitic Wilsonlo. On the other hand, we find among the inquilines many forms which closely resemble their host species, and which are often systematically attributed to their host genera, as in LeptotIiorax kutteri and L. goesswaldi, or Doronomyrmex pacis (Fig. 6); all three are difficult to tell apart from the host species L. aceworum. Curiously enough, these three species may occur sympatritally, all living with the one common host species, and sometimes two of the parasitic species share one host colony2’-24. It is probable that such inquilines have evolved directly from independent ancestors belonging to their host species group5**0. Wilson”” has drawn up a scheme (Fig.‘7) summarizing the hypothetical evolutionary pathways, from diverse origins in independent life through slavery, temporary parasitism or xenobiosis, all leading to inquilinism as the ultimate state. However, there is as yet no direct evidence for an evolution of guest ants towards inquilinisin, or for the pathway from temporary to perma158
nent parasitism. For the branch from slavery to inquilinism there is one example but it appears little substantiated: in the genus Strongy lognatkus (which has several truly dulotic species) there is one, S. testaceus, which is said to live as an inquiline, together with the host species queen. It has a moderate number of workers with the characteristic saber-shaped mandibles of the genus (Fig. 2c), but these workers have never been observed to conduct slave raids. In laboratory experiments, however, they are able to gain slaves from pure host colonies, with little overt fighting, and perhaps with an intricate system of chemical warfare25. Finally, in the example of Epimyrma described above, evolution leads from slavery to a degenerate parasitism which differs from true inquilinism in that the host queen is assassinated. The evolutionary origin of social parasttism The most important and also the most controversial problem is how and why some ants have switched over from independent life to social parasitism. We may split the problem into several questions. ( 1) What behaviors in normal social species give rise to the particular parasitic behaviors (mainly the dependent colony foundation and slave raiding)? (2) Which selective forces and which ecological conditions might be responsible for or might favor the development of parasitic habits? (3) How is the
1986
generally close systematic relationship between hosts and parasites explained? Apart from the guest ants, whose origin and evolution is comparatively easily understood, the questions above can only be answered hypothetically. On the third question, most authors are in accord. Emery26 has pointed out that all the inquilines, slavemakers and temporary parasites are closely related to their respective host species. This may be either because they have evolved directly from the host species (or species-group)26, or because parasites are able to coexist only with very closely related species27. in order to live in a mixed society the two species must have compatible communication systems, similar pheromones for nestmate recognition and so on, and the parasite’s larvae must be adapted ta!@ndular food secretions, feeding habits, etc. of the host species workers. When closely related species are involved, these conditions are most easily fulfilled. The question is thus reduced to the sympatric or allopatric origin of parasite and host: whether the parasite has directly evolved within and from a host species, or whether speciation first occurred, perhaps due to a geographical barrier, and subsequently. one species went over to parasitize its sister species. The latter means is favored, among others, by Wtison’,‘6. However, several authors lean towards the sympatric origin of parasitic species directly ‘in the mother’s lap’5, in the nests or populations of the independent ancestor, which then became the host species’2*2’,28P29. The arguments for this proposition will be discussed later on. To the second question, on the selective forces involved in the evolution of social parasitism, there are, in my opinion, no really convincing answers. Several authors have stressed that independent colony foundation by single young queens is a hazardous period, and that this risk could be avoided either by joining a colony of their own species (leading to polygyny), or by invading a foreign colony and becoming an inquiline or temporary parasite5. It is difficult, however, to understand how such factors
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might cause an ant species to switch over to parasitism, since invading a foreign colony is also a venture12. An important risky aspect, nevertheless, is the similarity between parasitic colony foundation and the acceptance of conspecific queens in polygynous colonies of independent species. This leads back to our first question, on the derivation of parasitic behavioral patterns from normal social ones. Most of the relevant literature refers to the conspicuous behavior of slave raiding. The first hypothesis, suggested by Darwin’4, is that predation on the brood of other species, and the occasional hatching of workers from surplus pupae, may be the origin of slavemaking behavior. This hypothesis, however, does not address the parasitic foundation of colonies in all known slavemaking species. Another hypothesis, proposed mainly by Alloway3’, Holldobler3’ and Wilson’,‘6, claims that territorial interactions between neighbouring conspecific colonies are a preadaption to slavery. Quite often in such interactions, the stronger colony kills the adults of the rival nest and takes over its brood, from which workers develop and join the society. This ‘intravictorious specific slavery’3i, however, also does not explain the parasitic formation. colony mode of Elsewhere” I have proposed to derive the penetration of a host colony by the slavemaker’s queen from the behavior of facultatively polygynous ants, in which the young queens may seek adoption in conspecific colonies, and to derive the brood raiding from the frequently observed brood transportation between nests of polydomous supercolonies. Alloway” has tried to combine both territorial competition and the adoption of young queens as a preadaptation for parasitic colony foundation. Polygyny is apparently also an important feature in the evolution of inquilinism, and perhaps of temporary parasitism’2*28,30 too. A strong argument in favor of this proposition derives from the fact that most inquilines live in polygynous host colonies, and are often polygynous themselvesi2. Slavemaking ants also quite often have polygynous host species. Only in
Fig. 6. Doronomyrmex putis, a workerless inquiline acervorum. Male fright) and female are alate and however, near to the mother nest.
temporary parasites is this association weak, most temporary parasites and their hosts being monogynous. The possibility of formation and genetic isolation, within polygynous colonies, of a subpopulation of sexuals which produce few or no workers has been discussed by Kutter5, Buschinger’2,2’ and EImes28. Ant species or populations may change from monogyny to polygyny (and vice versa) depending on various environmental conditions32, and polygyny is a suf-
which closely have the usual
resembles appearance
its host species, of ant sexuals.
Leptothorax They mate,
ficiently frequent phenomenon in ants as to represent a condition from which parasitism may have evolved convergently several times. A conceivable mutation, e.g. causing certain sexuals to mate at a different time of day, might quickly produce a subpopulation of individuals genetically isolated from the original form but still living in its polygynous colonies. Once this isolation has been achieved, development in the inquiline or the dulotic direction may depend upon
COLONY t.BJLTlPLlCATlON BY ADWTION AND BUDDING
I
I
OULOSIS
(SLAVERY1
1
I
-
’~
TEMPORARY
PARASITISM
INPUlLlNlSM A (“PERMANENT PARASITISM”)
XENOBIOSIS
Fig. 7. Hypothetical evolutionary pathways (Wilson’,“) from xenobiosis. temporary or dulosis to inquilinism. Little evidence, however, supports this scheme Reproduced 6y permission of Harvard University Press and E.O. Wilson.
parasitism (see text).
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Fig. 8. Artificial nest with a colony of Harpagoxenussublaevisand Leptothorax acervorum. The nest is made of a plexiglass frame and two microscope slides (76 X 26 mml; the entrance is at the left.
the ability of such a form to produce further workers12. And when the host species evolves towards monogyny, or the parasite spreads into monogynous populations of its host species, selection will favor those parasite queens which are able to replace the host colony queens by force, as in dulotic or temporary parasitic species”. One final aspect of this subject may be mentioned, which has perhaps been underestimated in previous discussions of ant parasitism. Mating within or close to the mother nest instead of a swarming flight has often been recorded in social parasites, mainly in inquilines 1,5,18,21.However, inbreeding does not emerge de nova in parasites. To a greater or lesser degree it is already present in most or all independent polygynous species. Following the kin selection theory, true polygyny (the coexistence of several egg-laying females in a colony1 should be possible only with closely related queens’, and thus with a quite high degree of inbreeding in a population. So although a concise and unequivocally accepted theory on the evolution of social parasitism is still lacking, there are some traits in the social organization of ants which evidently are involved in the frequent and convergent formation of inquilines, slavemakers and temporary parasites. These traits are inbreeding, polygyny, polydomy,
and perhaps territorial behavior, which in various combinations may give rise to the major types of social parasitism. Numerous problems remain unsolved. The unknown evolutionary origin of the throttling and beheading behaviors of colony founding parasitic queens, or of group recruitment in slavemaking leptothoracines (a behavior apparently absent in their independent relatives), the unequal distribution of social parasites in tropical and north temperate ant faunas”. the convergent evolution of the ‘anatomical parasitic syndrome”‘, the apparent lack of social parasites among the numerous fossil ants12, and the genetic implications of inbreeding, illustrate the range of open questions. New techniques, such as isozyme studies for evaluating genetic relationships of parasites and hosts33 and recentlydeveloped methods for breeding social parasitic antsT4 (Fig. 81, will help to increase our knowledge considerably.
I Wilson, E.O. ( 1971 I The Insect Societies. Belknap Press (Harvard University Press) 2 Francoeur. A., Loiselle, R. and Buschinger. A. (1985) Nal. Can. I 12.343-403 3 GbPwald, K. f 19381 Z. Wiss. Zool. I5 I, 101-148 4 Forel,A.11921-19231LeMondeSotiofdes Fourmis du Gfobe ComparPd Celuide PHomme (5 Volsl, Libraire Kundig
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5 Kutter, H. ( 1969) Die Sozialparasilisthen Ameisen der S&weir, Leemann AC 6 Winter, U. (1979) lnsetles Sot. 26. 123-135 7 Ehrhardt, W. (19801 Zoof. Anz. 208. 145-160 8 Regnier, FE and Wilson, E.O. (I971 I Science I72,267-269 9 Buschinger, A., Ehrhard. W. and Winter. U ( 1980) Z. Tierpsycho/. 53. 245-264 IO Wilson. E.O. II9841 InsectesSot. 31,3 16-334 I I Wheeler, W.M. ( I9101 Ants: Their Slructure, Developmentand Behavior, Columbia University Press I2 Buschinger, A. II9701 Biol. Zentralbl. 88, 273-299 I3 Buschinger. A. (19821 in Biosyslematirs of the Social insects IHowse. P.E. and Clement. J-L., edsl, pp. 21 l-222, Academic Press I4 Darwin, C.R. 11859) On the Origin of Species by Means of Natural Seleclion.or the Preservationof Favoured Racesin the Slruggle /or Life, lohn Murray I5 Wilson, E.O. (19761 Psytke83,277-288 I6 Wilson, E.O. f 1975) Sociobiology.The New Synthesis, Belknap Press (Harvard University Press) I7 Winter, U. (19791 Nalunoissens&ten 66, 581 I8 Buschineer. A. and Winter. U. II9851 Entomol. Geier. IO, 65-75 19 Buschinger, A., Winter, U. and Faber, W I I9831 Psyche 903335-342 20 lessen, K. Proc. 10th Int. Congr. lUSSl (in presst 21 Buschinger. A. (1965) InsectesSoc 12, 327-334 22 Kutter, N. (19501 Mitt. Stlrweiz. Ent. Ces 23, 347-353 23 Kutter, H. ( 19671 Mill. Sthweiz. Enl Ges. 40. 78-91 24 Buschinger, A. I1971 I Banner Zooi. Beitr. 22, 322-331 25 lohann. R (19841 Staatsexamensar6eit.T.H Dannstadt 26 Emery, C. I 1909) Biol. Cenlralbl. 29,352-362 27 Dobrzanski. 1. (19651 Acta Biof. Exper. 25, 59-7 I 28 Elmes, G.W II9781 Sysf. Enfomoi 3, 131-145 29 Bourke. A.F.G. and Franks, N.R. Proc. 10th Inl. Conar. IUSSI lin press1 30 Allo&ay, T.M. fld8Ol Am. Nat. I15,247-261 ?I Hblldobler. B. ll976lStiente 192.912-914 32 HBlldobler, B. and Wilson, E.O. (I 9771 Nalurwissenschaften64,8-l 5 33 Douwes. P. and Stille. B. Proc. IOlh Int Conar. IUSSI lin Dress1 34 iuschinger, A., Fischer. K., Guthy, H.P lessen, K. and Winter, U. Psytke lin press)
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Slave raids of Amazon ants, the 6eheading of the host colony’s queen by a parasitic Bothriomyrmex female, or the protracted throttling of the host queen by an Epimyrma female which has penetrated a Leptothorax nest, are among the most intriguing Cehaviors to 6e observed in social parasitic ants. The evolutionary origin of thesebehaviors, however, is quite obscure, and further work is needed to elucidate how parasitic fife cycles could have arisen from the ordinary social organization of ants. Social parasitism, as understood in this article, refers to parasitehost relationships between any two species of social insects. As cuckoos exploit the parental care of their hosts, so social parasitic wasps, bees and ants utilize the social accomplishments of other, independent species. The types of social parasitism in ants Social parasitism occurs in a,variety of manifestations, partictirly in ants: so-called guest relations or xenobiosis, temporary parasitism, permanent parasitism with slavery (dulosis) and without slavery (inquilinism). These four basic types can be summarized briefly as follows. A detailed survey is provided by Wilson ’ Guest ants The guest ants of theayrmicine tribe Leptothoracini (now all attributed to one apparently monophyletic genus, Formicoxenus*), have small colonies with up to about a hundred individuals. They live within the nest material or the nest walls of their hosts, which are much bigger species of the genera Formica or Myrmica with large, populous nests. The Formicoxenus build their own little nests well separated from the brood chambers of the hosts, and they themselves care for their brood. They are dependent upon the hosts only with respect to nutrition. Formicoxenus may either beg for regurgitated food directly from a Formica or Myrmica worker, or participate in food exchange (trophallaxis) between two host workers. A guest ant may climb over Alfred Buschinger is at the lnstitut fib Zoologie, 61 Darmstadt, Technische Hochschule, Schnittspahnstr. 3, FRG. This article is dedicated to Heinrich Kutter on the occasion of his 90th birthday. @ 1986. Eleewer Science PubIshers
6 V Amsterdam
Evolutionof SocialParasitism in Ants Alfred Buschinger the legs and dorsum of a Formicu to reach its head, and then lick the food droplet being transferred to another host ant. The trophic parasitism of the guests ants may have evolved from plesiobiosis (the habitual nesting of two ant species in very close vicinity), which is often observed in nature. Temporary parasitism In temporary parasitism, the parasitic species depends on a host species only for foundation of new colonies. Usually, the parasitic queen, after her nuptial flight and insemination, tries to penetrate a host colony where she replaces the original queen. From the parasite’s eggs, a worker force develops with the aid of the host colony workers; the latter finally disappear due to natural aging and losses, and the colony becomes a pure society of the parasitic species. Some peculiar behaviors of the queens have been observed during colony foundation. In Lasius umbratus, the female grasps and chews a worker of the host species (L. niger) and then enters the host nest. There she is said to become more attractive than the original queen3, which finally dies of starvation or is expelled horn the colony. A closely related species, L. reginae, after invading a nest of L. alienus suddenly attacks the much bigger host queen and throttles her to death’ (Fig. I).
Bothriomyrmex decapitans and other species of this genus, in the same situation, cut off the head of the host species queen (of the genus Tapinoma14. Lmsius fuliginosus exhibits a social hyperparasitism in that the queen founds her colonies with the aid of L. umbra&s which is itself a temporary parasite. Temporary parasitism also occurs in several species of wood ants of the Formica rufa group; in some species the queens may either penetrate a Serviformica sp. nest, or join a polygynous nest of their own species. Such colonies then reproduce by budding, often forming huge multinest supercolonies’. Permanent parasitism with slavery The permanently parasitic species depend upon the hosts throughout their lives. In the case of the slavemaking ants, the young queens have to penetrate a host species nest, kill or drive out all adults, and take over the brood. From these pupae emerge the first slaves, and with their aid a number of slavemaker workers are subsequently produced. These workers are often unable to forage, to feed the larvae, or even to eat by themselves. On the other hand, they are usually predisposed for fighting, being equipped with specialized piercing mandibles (as in Polyergus and Strongspecies’r5) or with ylognathus
Fig. I. A temporary parasitic ant queen. lnsius reginac; she penetrates a host species colony (L. alienus) and kills the host queen by throttling her. A similar behavior has evolved convergently in the genus Epimyrma (Fig. 51, which (in contrast to the formicine genus Ltsius) belongs to the subfamily Myrmicinae. Reproducedby permission of Bundewnstalt fiir Ppanznschutz, Wien.
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Fig.2. Scanning electmn micrographs of the heads of slavemaking ants and their slaves. The white bars represent Imm. (a) Polyergusn&tens, the Amazon ant, with saber-shaped mandibles: lb) oneof its slave species, Semiformira lemani, with normally dentate mandibles. Both (at and fbl belong to the subfamily Formicinae. lc) Strongylognathus alpinus, with cowergently evolved piercing mandibles; Id) its slave, Tetramorium aespitum. Both ICI and (d) belong to the subfamily Myrmicinae. fel Harpagwnus sublaevis,a slavemaker with scissorlike toothless mandibles for cutting off the appendages of an opponent; If) Leptotlrorax awwrum, one of its slave species. Both let and (f) belong to the subfamily Myrmicinae. Pictures taken 6y A. Maiazra. FBI I, TH Darmstadt.
toothless mandibles for cutting off the appendages of their opponents (as in Harpugoxenus su6hevis’.6) (Fig. 2). Others have strong stings (CXulep~xenus’l, or produce aggressive glandular secretions or ‘propaganda’ substances (RaptiformLa’L They attack independent, neighbouring colonies of the host or slave species, fight against the defenders, and finally carry back brood to the slavethe maker’s nest. Thus, the slave stock may be replenished several times a year’.
Permanent parasitism without slavery Permanent parasites which do not use slaves often lack a worker caste. The females usually coexist with the host species queens in their nest, the parasite brood being reared by the host workers simultaneousiy with their own larvae. In a few instances, e.g. Anergates atratulus, the parasite apparently invades only queenless host species colonies, whereas the ‘ultimate parasite’ Telewtomyrmex scltneideri rides like an ectoparasite on the back of the host colony queen (Fig. 31*.
Frequency and systematic distribution of parasHic ants Among the estimated IOOOO12 000 ant species on earth, the parasitic forms (about 200 species) represent but a small fraction. However, most parasitic ant species are rare and not easily found in the host species populations and colonies; thus the actual number of parasitic species might be considerably higher. Every year some new species are detected, and in a very well known fauna, such as in Switzerland, about one third of the - t 10 ant species is parasitic5. So we may expect that the number of known parasitic species will increase, particularly in the tropics”. The distribution of social parasitic species among the I I living ant subfamilies is surprising. Although the subfamilies apparently do not differ fundamentally in their form of social organization, social parasites are known mainly in the Myrmicinae and the Formicinae (with about 33 and 9 genera respectively). Although some subfamilies comprise few species, it is difficult to understand why parasites are lacking in, for instance, the large subfamily Ponerinae. Moreover, among the myrmicines and formicines the parasitic species are again concentrated, in only a few genera’. A survey of the parasites in different subfamilies reveals that the main types of parasitic life habits (inquilinism, dulosis, and temporary parasitism) have evolved convergently within both the Formicinae and Myrmicinae, temporary parasitism among the Dolichoderinae (one genus, Botkriomyrmex) and Pseudomyrmecinae, and inquilinism in a genus of the Myrmeciinae’,“. Within the myrmicine tribe Leptothoracini alone, slavemaking has apparently evolved five times independently9.12 with different groups of host species, inquilinism at least twice17, and xenobiosis once2. Wilson’” assumes an independent, convergent evolution of nine parasitic species from the myrmicine genus Plreidole. This polyphyletic origin of very similar parasitic life cycles means that there may be certain widespread features of normal social behavior which often become the starting point for parasitic evolution’2.
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Evolutionary progression in parasitic ants In the evolution of parasitism we have to distinguish between the origin of parasitic life habits, which will be dealt with in the following section, and the evolution of life cycles and behavior within parasitic species groups. Considerable progress has been achieved during the past few years, mainly with respect to the latter question. As mentioned above, the guest ants of the genus Formicoxenus are apparently monophyletic*; the frequent coexistence of different ant species nests in close proximity has, surprisingly, not often led to the evolution of xenobiotic relations. There is only one other group (the genus Megafomgrmex) known to exhibit this habit’. Within the guest ant genus Formicoxenus, however, we can observe certain trends which may or may not be affected by their parasitic life habits. The most primitive, or least specialized, form has normal males with wings and black coloration, as in most ants. In other, more derived, species the males become polymorphic, some of them hatching without wings; and in the most specialized F. nitidulus the males are wingless, brown and similar to workers in appearance. The queens in Formicoxenus are generally polymorphic, some being alate, others workerlike, and many intermediate in shape. In fact, queen polymorphism is not unusual in parasitic ants, and is particularly common in the leptothoracines (to which Formicoxenus belongs). For the wood ants (Formica and allied genera), an evolutionary line was long ago proposed by Darwin14; it began with brood predation for food, and led via the facultative slavery of the subgenus Raptiformica to the obligatory dulosis of the Amazon ants, genus Polyergus. More recently, a workerless inquiline, F. talbotae, has been detected in this groupi5. Whether this species is a descendant of a temporary parasitic ancestor, or is derived directly from an independent polygynous form, is open to question. Among the leptothoracines, an evolution from slavemaking species to workerless forms has been documented in the genus Epimgrma. The life history of this genus, its
gastric old queen are shown on top of the host queen, a host species worker is in front of the queen 6u oermission of erouo. Drawina 6u W. tinsenmaier. rearoduced
seemingly ‘remarkably clear evolutionary progression leading from temporary social parasitism to full inquilinism’ (as was summarized for the last time by Wilson? has to be rewritten completely, however. In this genus there is neither a temporary parasite nor a typical full inquiline. Instead, four species conduct well-organized slave raids with group recruitment and stingfighting (Fig. 4); during colony foundation the young queen throttles the host colony queen over weeks or even months (Fig. 5) until she finally dies. In a second group of Epimgrma species the number of workers is drastically reduced to only about 3-5; slave raiding in this group evidently cannot be effective, even though the workers are still able to perform all raiding
Fig. 4. Two Epimyrma ravouxi slavemakers colony.
activities. Finally, two species have been found without any Epimyrma workers: nevertheless, the young queens still throttle the host queens to death and thus differ from true inquilines which coexist with the host species queens”-“. Simultaneously in this genus, an evolution from normal swarming behavior of the alate sexuals to mating in the mother nest, and thus inbreeding, has been found. Three of the slave-raiding species make mating flights; one (E. algeriana) mates inside the nest, and all the ‘degenerate slavemakers’ and the workerless species also do SO’~*~‘. Among the inquilines, two significantly different evolutionary pathways may have been followed. On the one hand, there are some morphologically highly specialized and
sting a Leptothoraw unifasciatus worker defending
the raided
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[email protected]. Like the temporary parasitic Lasius reginae (Fig. I). the Epimynna algeriana queen penetrates a host soecies nest for colonv foundation and throttles the host queen, sometimes for weeks, until she is dead. Photo 6y W. Ek&dt.
apparently ‘old’ forms like Teleutomyrmex (Fig. 3) and Anergates, the latter having males which look strangely immature and pupa-like. For these parasites a long evolutionary history is assumed, perhaps including descent from slavemakers’e5. Their particular morphological characters, which in part occur also in other types of social parasites, are termed ‘the anatomsyndrome’ by ical parasitic Wilsonlo. On the other hand, we find among the inquilines many forms which closely resemble their host species, and which are often systematically attributed to their host genera, as in LeptotIiorax kutteri and L. goesswaldi, or Doronomyrmex pacis (Fig. 6); all three are difficult to tell apart from the host species L. aceworum. Curiously enough, these three species may occur sympatritally, all living with the one common host species, and sometimes two of the parasitic species share one host colony2’-24. It is probable that such inquilines have evolved directly from independent ancestors belonging to their host species group5**0. Wilson”” has drawn up a scheme (Fig.‘7) summarizing the hypothetical evolutionary pathways, from diverse origins in independent life through slavery, temporary parasitism or xenobiosis, all leading to inquilinism as the ultimate state. However, there is as yet no direct evidence for an evolution of guest ants towards inquilinisin, or for the pathway from temporary to perma158
nent parasitism. For the branch from slavery to inquilinism there is one example but it appears little substantiated: in the genus Strongy lognatkus (which has several truly dulotic species) there is one, S. testaceus, which is said to live as an inquiline, together with the host species queen. It has a moderate number of workers with the characteristic saber-shaped mandibles of the genus (Fig. 2c), but these workers have never been observed to conduct slave raids. In laboratory experiments, however, they are able to gain slaves from pure host colonies, with little overt fighting, and perhaps with an intricate system of chemical warfare25. Finally, in the example of Epimyrma described above, evolution leads from slavery to a degenerate parasitism which differs from true inquilinism in that the host queen is assassinated. The evolutionary origin of social parasttism The most important and also the most controversial problem is how and why some ants have switched over from independent life to social parasitism. We may split the problem into several questions. ( 1) What behaviors in normal social species give rise to the particular parasitic behaviors (mainly the dependent colony foundation and slave raiding)? (2) Which selective forces and which ecological conditions might be responsible for or might favor the development of parasitic habits? (3) How is the
1986
generally close systematic relationship between hosts and parasites explained? Apart from the guest ants, whose origin and evolution is comparatively easily understood, the questions above can only be answered hypothetically. On the third question, most authors are in accord. Emery26 has pointed out that all the inquilines, slavemakers and temporary parasites are closely related to their respective host species. This may be either because they have evolved directly from the host species (or species-group)26, or because parasites are able to coexist only with very closely related species27. in order to live in a mixed society the two species must have compatible communication systems, similar pheromones for nestmate recognition and so on, and the parasite’s larvae must be adapted ta!@ndular food secretions, feeding habits, etc. of the host species workers. When closely related species are involved, these conditions are most easily fulfilled. The question is thus reduced to the sympatric or allopatric origin of parasite and host: whether the parasite has directly evolved within and from a host species, or whether speciation first occurred, perhaps due to a geographical barrier, and subsequently. one species went over to parasitize its sister species. The latter means is favored, among others, by Wtison’,‘6. However, several authors lean towards the sympatric origin of parasitic species directly ‘in the mother’s lap’5, in the nests or populations of the independent ancestor, which then became the host species’2*2’,28P29. The arguments for this proposition will be discussed later on. To the second question, on the selective forces involved in the evolution of social parasitism, there are, in my opinion, no really convincing answers. Several authors have stressed that independent colony foundation by single young queens is a hazardous period, and that this risk could be avoided either by joining a colony of their own species (leading to polygyny), or by invading a foreign colony and becoming an inquiline or temporary parasite5. It is difficult, however, to understand how such factors
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might cause an ant species to switch over to parasitism, since invading a foreign colony is also a venture12. An important risky aspect, nevertheless, is the similarity between parasitic colony foundation and the acceptance of conspecific queens in polygynous colonies of independent species. This leads back to our first question, on the derivation of parasitic behavioral patterns from normal social ones. Most of the relevant literature refers to the conspicuous behavior of slave raiding. The first hypothesis, suggested by Darwin’4, is that predation on the brood of other species, and the occasional hatching of workers from surplus pupae, may be the origin of slavemaking behavior. This hypothesis, however, does not address the parasitic foundation of colonies in all known slavemaking species. Another hypothesis, proposed mainly by Alloway3’, Holldobler3’ and Wilson’,‘6, claims that territorial interactions between neighbouring conspecific colonies are a preadaption to slavery. Quite often in such interactions, the stronger colony kills the adults of the rival nest and takes over its brood, from which workers develop and join the society. This ‘intravictorious specific slavery’3i, however, also does not explain the parasitic formation. colony mode of Elsewhere” I have proposed to derive the penetration of a host colony by the slavemaker’s queen from the behavior of facultatively polygynous ants, in which the young queens may seek adoption in conspecific colonies, and to derive the brood raiding from the frequently observed brood transportation between nests of polydomous supercolonies. Alloway” has tried to combine both territorial competition and the adoption of young queens as a preadaptation for parasitic colony foundation. Polygyny is apparently also an important feature in the evolution of inquilinism, and perhaps of temporary parasitism’2*28,30 too. A strong argument in favor of this proposition derives from the fact that most inquilines live in polygynous host colonies, and are often polygynous themselvesi2. Slavemaking ants also quite often have polygynous host species. Only in
Fig. 6. Doronomyrmex putis, a workerless inquiline acervorum. Male fright) and female are alate and however, near to the mother nest.
temporary parasites is this association weak, most temporary parasites and their hosts being monogynous. The possibility of formation and genetic isolation, within polygynous colonies, of a subpopulation of sexuals which produce few or no workers has been discussed by Kutter5, Buschinger’2,2’ and EImes28. Ant species or populations may change from monogyny to polygyny (and vice versa) depending on various environmental conditions32, and polygyny is a suf-
which closely have the usual
resembles appearance
its host species, of ant sexuals.
Leptothorax They mate,
ficiently frequent phenomenon in ants as to represent a condition from which parasitism may have evolved convergently several times. A conceivable mutation, e.g. causing certain sexuals to mate at a different time of day, might quickly produce a subpopulation of individuals genetically isolated from the original form but still living in its polygynous colonies. Once this isolation has been achieved, development in the inquiline or the dulotic direction may depend upon
COLONY t.BJLTlPLlCATlON BY ADWTION AND BUDDING
I
I
OULOSIS
(SLAVERY1
1
I
-
’~
TEMPORARY
PARASITISM
INPUlLlNlSM A (“PERMANENT PARASITISM”)
XENOBIOSIS
Fig. 7. Hypothetical evolutionary pathways (Wilson’,“) from xenobiosis. temporary or dulosis to inquilinism. Little evidence, however, supports this scheme Reproduced 6y permission of Harvard University Press and E.O. Wilson.
parasitism (see text).
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Fig. 8. Artificial nest with a colony of Harpagoxenussublaevisand Leptothorax acervorum. The nest is made of a plexiglass frame and two microscope slides (76 X 26 mml; the entrance is at the left.
the ability of such a form to produce further workers12. And when the host species evolves towards monogyny, or the parasite spreads into monogynous populations of its host species, selection will favor those parasite queens which are able to replace the host colony queens by force, as in dulotic or temporary parasitic species”. One final aspect of this subject may be mentioned, which has perhaps been underestimated in previous discussions of ant parasitism. Mating within or close to the mother nest instead of a swarming flight has often been recorded in social parasites, mainly in inquilines 1,5,18,21.However, inbreeding does not emerge de nova in parasites. To a greater or lesser degree it is already present in most or all independent polygynous species. Following the kin selection theory, true polygyny (the coexistence of several egg-laying females in a colony1 should be possible only with closely related queens’, and thus with a quite high degree of inbreeding in a population. So although a concise and unequivocally accepted theory on the evolution of social parasitism is still lacking, there are some traits in the social organization of ants which evidently are involved in the frequent and convergent formation of inquilines, slavemakers and temporary parasites. These traits are inbreeding, polygyny, polydomy,
and perhaps territorial behavior, which in various combinations may give rise to the major types of social parasitism. Numerous problems remain unsolved. The unknown evolutionary origin of the throttling and beheading behaviors of colony founding parasitic queens, or of group recruitment in slavemaking leptothoracines (a behavior apparently absent in their independent relatives), the unequal distribution of social parasites in tropical and north temperate ant faunas”. the convergent evolution of the ‘anatomical parasitic syndrome”‘, the apparent lack of social parasites among the numerous fossil ants12, and the genetic implications of inbreeding, illustrate the range of open questions. New techniques, such as isozyme studies for evaluating genetic relationships of parasites and hosts33 and recentlydeveloped methods for breeding social parasitic antsT4 (Fig. 81, will help to increase our knowledge considerably.
I Wilson, E.O. ( 1971 I The Insect Societies. Belknap Press (Harvard University Press) 2 Francoeur. A., Loiselle, R. and Buschinger. A. (1985) Nal. Can. I 12.343-403 3 GbPwald, K. f 19381 Z. Wiss. Zool. I5 I, 101-148 4 Forel,A.11921-19231LeMondeSotiofdes Fourmis du Gfobe ComparPd Celuide PHomme (5 Volsl, Libraire Kundig
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5 Kutter, H. ( 1969) Die Sozialparasilisthen Ameisen der S&weir, Leemann AC 6 Winter, U. (1979) lnsetles Sot. 26. 123-135 7 Ehrhardt, W. (19801 Zoof. Anz. 208. 145-160 8 Regnier, FE and Wilson, E.O. (I971 I Science I72,267-269 9 Buschinger, A., Ehrhard. W. and Winter. U ( 1980) Z. Tierpsycho/. 53. 245-264 IO Wilson. E.O. II9841 InsectesSot. 31,3 16-334 I I Wheeler, W.M. ( I9101 Ants: Their Slructure, Developmentand Behavior, Columbia University Press I2 Buschinger, A. II9701 Biol. Zentralbl. 88, 273-299 I3 Buschinger. A. (19821 in Biosyslematirs of the Social insects IHowse. P.E. and Clement. J-L., edsl, pp. 21 l-222, Academic Press I4 Darwin, C.R. 11859) On the Origin of Species by Means of Natural Seleclion.or the Preservationof Favoured Racesin the Slruggle /or Life, lohn Murray I5 Wilson, E.O. (19761 Psytke83,277-288 I6 Wilson, E.O. f 1975) Sociobiology.The New Synthesis, Belknap Press (Harvard University Press) I7 Winter, U. (19791 Nalunoissens&ten 66, 581 I8 Buschineer. A. and Winter. U. II9851 Entomol. Geier. IO, 65-75 19 Buschinger, A., Winter, U. and Faber, W I I9831 Psyche 903335-342 20 lessen, K. Proc. 10th Int. Congr. lUSSl (in presst 21 Buschinger. A. (1965) InsectesSoc 12, 327-334 22 Kutter, N. (19501 Mitt. Stlrweiz. Ent. Ces 23, 347-353 23 Kutter, H. ( 19671 Mill. Sthweiz. Enl Ges. 40. 78-91 24 Buschinger, A. I1971 I Banner Zooi. Beitr. 22, 322-331 25 lohann. R (19841 Staatsexamensar6eit.T.H Dannstadt 26 Emery, C. I 1909) Biol. Cenlralbl. 29,352-362 27 Dobrzanski. 1. (19651 Acta Biof. Exper. 25, 59-7 I 28 Elmes, G.W II9781 Sysf. Enfomoi 3, 131-145 29 Bourke. A.F.G. and Franks, N.R. Proc. 10th Inl. Conar. IUSSI lin press1 30 Allo&ay, T.M. fld8Ol Am. Nat. I15,247-261 ?I Hblldobler. B. ll976lStiente 192.912-914 32 HBlldobler, B. and Wilson, E.O. (I 9771 Nalurwissenschaften64,8-l 5 33 Douwes. P. and Stille. B. Proc. IOlh Int Conar. IUSSI lin Dress1 34 iuschinger, A., Fischer. K., Guthy, H.P lessen, K. and Winter, U. Psytke lin press)