Polygyny

CHAPTER 6. QUEEN NUMBERS AND DOMINATION

The number of queens profoundly alters several of the key features of colonial organization, including the kinship of the nestmates, the rate of colony growth, and the number and distribution of nests. The past ten years have witnessed an explosive growth of knowledge about this complex subject, with investigators addressing the following questions:

• Why does the number of queens vary among species? The colonies of some species always have a single egg-laying queen. Those of others have up to thousands or, as in the case of the “supercolonial” Formica yessensis of Japan, millions of queens. In still other species the number ranges among colonies from one to many. In addition, the number often shifts through different stages of the colony life cycle.

• Which colony members control the number of queens? Is the number a consequence of dominance and elimination among queens, or do the workers regulate the number?

• How is the number controlled? Regulation of the queen population can be achieved by physical elimination, reproductive castration (perhaps mediated by pheromones), or emigration of supernumeraries.

• What are the consequences of varying queen numbers on the growth and genetic structure of colony populations?

It will be useful to begin with the generally accepted terminology of queen numbers in relation to the life cycle. Monogyny refers simply to the possession by a colony of a single egg-laying queen, or reproductive female--or "gyne," as it is often called in the myrmecological literature. Polygyny is the possession of multiple queens. Oligogyny is a special case of polygyny, in which two to several queens coexist in the same nest but remain well apart from one another (Hölldobler, 1962; Buschinger, 1974a). As a rule, oligogyny in ants is characterized by tolerance of workers toward supernumerary queens combined with intolerance among the queens, so that the queens space out in the same nest (Hölldobler and Carlin, 1985). The founding of a colony by a single queen is called haplometrosis; when multiple queens found a colony the condition is referred to as pleometrosis (Wasmann, 1910b; Wheeler, 1933b). The term metrosis can be used to refer generally to this biological variable. Monogyny can be primary, meaning that a single queen is also the foundress; or it can be secondary, in which multiple queens start a colony pleometrotically but only one of them survives. In a symmetric fashion, polygyny can be primary (multiple queens persist from a pleometrotic association) or secondary (the colony is started by a single queen and others are added later by adoption or fusion with other colonies).

True polygyny, in which two or more queens contribute to egg-laying, has been conclusively demonstrated in many genera in the Ponerinae, Myrmeciinae, Myrmicinae, Dolichoderinae, and Formicinae, both by direct observation of egg-laying and indirectly, through the electrophoretic identification of allozymes in the workers and second generation of reproductives (see for example Pamilo, 1982b, and Berkelheimer, 1984). Without such proof the mere presence of multiple queens in the same nest does not necessarily mean that the colony is polygynous. Queens that are winged are invariably virgin and not active egg-layers. These "alate" individuals are young and native to the nests in which they are found. They await the mating flight and, in most cases, the initiation of new colonies on their own. Even if supernumerary queens are wingless (called "dealate" if they have shed wings they earlier possessed), they still might not be egg-layers. In some species such individuals are inseminated but their oviposition is suppressed by the presence of a major egg-laying queen in the same nest. This form of reproductive latency, also called "functional monogyny," has been demonstrated in Formicoxenus and Leptothorax  by Buschinger and his co-workers (1967, 1968c, 1979a; Buschinger and Winter, 1976; Buschinger et al., 1980b); and in Solenopsis invicta  by Tschinkel and Howard (1978). Functional monogyny has also been reported in Myrmecina graminicola by Baroni Urbani (1968a, 1970). However, Buschinger (1970b) cautioned that these particular observations might have been due to laboratory manipulations, pointing out that functional monogyny has not been observed in colonies collected fresh from the field. In other

species, for example Leptothorax acervorum, the dealate supernumeraries are unfertilized. Buschinger (1967) calls this condition “pseudopolygyny” to distinguish it from true, functional polygyny and latent polygyny. He notes that in Leptothorax, the infertile queens often act like workers by sharing ordinary labor in the nest. On the other hand, Ehrhardt (1970) found that dealated virgin queens of Formica polyctena often contribute to the male brood. Similar observations have been made in polygynous colonies of Solenopsis invicta (D. J. C. Fletcher, personal communication).

The origins of polygyny
Polygyny can arise by one or the other of three means: pleometrosis, with the multiple founding queens remaining together after the first workers appear; the adoption of extra inseminated queens after their nuptial flights; and the fusion of colonies. Different ant species have played upon these devices in various ways to produce a remarkable diversity of statistical patterns of queen numbers. In many species, the colonies employ them to create mixed strategies of colony founding and structure.

The most versatile species studied to date in this regard is the Australian meat ant Iridomyrmex purpureus (Hölldobler and Carlin, 1985). Most new colonies are founded by single queens, following the nuptial flight in the spring month of October. Sixty-five of 72 newly founded nests excavated near Canberra contained a single queen, six contained two queens, and one contained three queens. As the nearby inseminated queens scurry over the ground and then start to dig a burrow in the soil, they are attacked by many enemies. Greaves and Hughes (1974) reported losses of 80 percent or higher from ground-feeding birds alone. Many other queens are killed by hostile workers of their own species when they stray too near the established colonies. But, surprisingly, other queens succeed in digging their nest chambers in the immediate vicinity of mature Iridomyrmex purpureus. Not only are most of these females tolerated by the resident workers, they are often attended and protected. The workers even help them dig the chambers (see Figure 6-1). Such actions are likely to protect the foundresses from hostile ants, birds, and other predators. Meat ant workers are extremely aggressive, biting enemies and spraying them with poisonous secretions from their pygidial glands. Hölldobler and Carlin believe that the queens protected in this manner are the ones fortunate enough to settle near their natal nests, so that the foundresses are also likely to be absorbed into the mother colonies to become supernumerary queens. Thus variation in queen numbers appears to be due at least in part to the vicissitudes of foundress association and tolerance by neighboring mature colonies.

Variation in the number of queens, usually less complexly organized than in Iridomyrmex purpureus, is widespread but not universal in the ants. Among 46 nests of Aphaenogaster rudis excavated by Headley (1949), for example, no queens were found in 6 of the nests, a single queen was found in each of 38 nests, and two queens each were found in 2 nests. Talbot (1951) obtained similar proportions in the 71 additional nests of Aphaenogaster rudis. In 20 nests of Prenolepis imparis excavated in Missouri, Talbot (1943a) found no queens in 3 of the nests, a single queen in each of 15 nests, and two queens in each of 2 nests. In Florida, Tschinkel (1988c) found most colonies of P. imparis to be polygynous, with a range of 1-6 and a mean of 4 queens per nest. In Lasius flavus, colonies with more than one queen occur but are rare (Waloff, 1957). The same is true of harvester ants in the genus Pogonomyrmex; in one sample of 70 Pogonomyrmex rugosus incipient nests studied by Pollock and Rissing (1985), only four contained more than one queen. Mature colonies, however, contain only one queen (Hölldobler, unpublished observations). The level of polygyny can vary geographically within the same species. Some local populations of the fire ant Solenopsis invicta are primarily monogynous, others primarily polygynous (Tschinkel and Howard, 1978; Fletcher et al., 1980). Unfortunately, most species reported to be polygynous have not been studied carefully enough to establish that the queens are all fully fertile and inseminated.

Although precise data are not available for enough species to assess the Formicidae as a whole, it is our impression from a good deal of field experience that the mature colonies of the majority of species are strictly monogynous. It is reasonably supposed that properties in colony organization tend to bias species toward monogyny in the course of evolution, and that the tendency is reversed only when special ecological constraints are imposed on the species (Hölldobler and Wilson, 1977b; Oster and Wilson, 1978). Two such properties can be expected as a consequence of evolution by natural selection. First, queens of all kinds of social insects should prefer to retain personal reproductive rights and surrender none to their sisters or daughters, because they are more closely related to their daughters and sons than to their nieces, nephews, and grandoffspring. Furthermore, queens living in multiples are likely to contribute fewer offspring than if they were the sole egg-layers, an effect in fact documented experimentally in Leptothorax curvispinosus by Wilson (1974b) and in Plagiolepis pygmaea  by Mercier et al. (1985a,b). Second, workers should prefer to have only one queen serving as the colony progenitrix. In species with colonies of small to moderate size, the rate of colony growth, and hence the amount of colony genetic fitness, is limited primarily by the number of workers and not by the number of queens, one queen usually being able to supply as many eggs as a worker force can rear. This effect has been demonstrated, for example, in the myrmicine genera Tetramorium (Brian et al., 1967), Myrmica  (Elmes, 1973), and Leptothorax  (Wilson, 1974b). Since extra queens would then be an unnecessary energetic burden on the colony, an especially significant factor during the colony's early growth, it should be of advantage to the workers to eliminate them. In short, one can reasonably expect the dominant queen and the workers to conspire to eliminate supernumerary queens during the early phase of colony growth and thus to attain a state of monogyny.

Under a wide range of conceivable conditions, independent colony foundation should be a second trait favored by natural selection. If entire colonies can be started by one or a few queens, mother colonies producing such females can deploy far more of them over greater distances than otherwise comparable colonies that reproduce by swarming. Each swarm drains off a part of the original worker force, and its dispersal range is limited by the difficulties inherent in mass orientation and mobility. Swarming is likely to be of advantage only if the survival rate of queens is overwhelmingly greater when they are accompanied by workers than when they proceed alone.

In addition, haplometrosis can be expected to be the preferred mode of independent colony foundation. Unless circumstances give a large advantage to founding in groups, each queen should attempt to start a colony well away from all possible rivals. The tendency just cited toward the restitution of monogyny by both the dominant queen and the first worker force means that a queen choosing to become a member of a group of n founding queens has a 1/n chance of surviving to be the nest queen.

Finally, colony foundation should be claustral whenever possible. The highest mortality of social insect workers occurs during foraging trips, and it is probable that the same is true of founding queens forced to leave their nests in order to search for food.

In sum, a first logical examination of the more abstract general properties of insect societies leads us to expect that natural selection will lead species to monogyny, haplometrosis, and claustral nest founding. Yet deviations from this expected pattern are many and exceedingly diverse. In the case of the fire ant Solenopsis invicta, for example, local strains of polygyne colonies have originated and flourished repeatedly in various parts of the United States since 1940 (Greenberg et al., 1985).

The adaptive significance of polygyny
An examination of the trends toward polygyny can, if examined on a broader theoretical context, shed light on the evolution of other aspects of social behavior. Let us begin with a comparison of two of the major groups of social Hymenoptera. Most ant species are monogynous and obligatorily haplometrotic. Within most major phyletic lines, polygyny and swarming appear to be evolutionarily derived conditions. Among the wasps, in contrast, only the temperate zone species of Vespa and Vespula  are known to be obligatorily haplometrotic. Belonogaster, Mischocyttarus, and Polistes are sometimes haplo- and sometimes pleometrotic, while most or all of the Polybiini, containing 20 of the 26 known social wasp genera, are polygynous and reproduce by swarming (Evans and West-Eberhard, 1970; Spradbery, 1973). We suggest the following simple explanation for the difference. When an ant colony moves to a new nest site, for example following a disturbance by a predator, it must walk to the new site. The workers are wingless, and the queen must travel on the ground with them. Thus queens can afford to shed their wings following the nuptial flight and initiate claustral colony foundation. In all but a few species they histolyze their alary muscles to nurture the first worker brood within a completely closed cell. Since they never need to take flight again, the queens are able to take advantage of the surplus energy available in the alary muscles. Both wide dispersal and independent, claustral colony founding are within their reach. Since these are the optimum techniques under almost all conceivable conditions, most ant species have evolved to acquire them.

When wasp colonies are disrupted, they fly to a new nest site. Lengthy ground travel is not only unnecessary but would be disadvantageous for insects so fully adapted to life in the air. Because the queens must fly with them, they must "stay in shape" by not losing their flight muscles. The nest queens of Vespa lose the power of flight as they become older, presumably because of the weight of their ovaries, but this is the exception rather than the rule in social wasps. Thus wasp queens are less well equipped to be solitary foundresses. Since independently founding individuals find it disadvantageous to convert the alary muscles into energy for the brood, they must engage in the risky process of foraging for food. It appears to follow that wasp species should be more likely to rely on pleometrosis or even swarming, which is in fact the case.

Why, then, does polygyny occur at all in ants? It is evidently derived in evolution and has arisen repeatedly during the 100-million-year evolution of these insects, despite the fact that it has certain intrinsic disadvantages. When a phenomenon displays this kind of pattern, the biologist is justified in searching for unusual circumstances that have promoted its deviant form of evolution.

Endangered populations. Population extinction rates are likely to be highest in rare or locally distributed species. In ants and other social hymenopterans, in which the males are derived from unfertilized eggs, the effective size of the population of colonies (Ñ in the parlance of population genetics; see Li, 1955) is

[(4.5Nt)/Nc](MQ/1+2M)

where

Nt is the total number of adult individuals, of all castes, in the population of colonies;

Nc is the average number of adult individuals per colony;

Q is the average number of queens contributing offspring to individual colonies;

M is the average number of males that fertilized each queen (these individuals no longer need be living).

Ñ is the equivalent of the number of breeding individuals in an idealized nonsocial population with equal numbers of males and females, and it provides an exact measure for the estimate of inbreeding, gene loss through random drift, and probability of extinction. In ants as in nonsocial organisms the effective breeding size will be exactly equal to the term given if breeding is panmictic, that is, completely random among the reproductive individuals, and less than the term if it is not panmictic (Wilson, 1963, 1971).

Examination of this formula shows that the most efficient means of enlarging effective population size is by increasing the number of queens. Merely adding a single additional queen to a monogynous colony system, for example, has the effect of doubling the effective population size. And to double the population size will enormously increase the mean survival time of the populations under a wide range of environmental conditions and demographic constraints (MacArthur and Wilson, 1967). Consequently polygyny alone might "rescue" rare populations from quick extinction. Put another way, group selection could establish polygyny in systems of populations small enough to be subject to frequent extinction. If there are multiple rare species or rare populations belonging to the same species, those containing polygynous colonies would be more likely to survive than others composed exclusively of monogynous colonies.

The effective population size of some ant species is indeed very low. In the Erebomyrma urichi population occupying Trinidad's Oropouche Cave in 1961, it was estimated not to exceed 400 (Wilson, 1962d). The population of Lasius minutus at Hidden Lake, Michigan, nested in only 700 mounds during the 1950s. Since a single colony occupied an average of about 4.4 mounds (Kannowski, 1959a,b), the population could be estimated to contain approximately 160 colonies and an effective population size as low as 320 outside the reproductive season. The extreme rarity of many social parasites, coupled with patchy distributions, is well known to myrmecologists. A typical example is Manica parasitica, recorded only from nests of Manica bradleyi on top of Polly Dome, Yosemite National Park, California, and apparently absent from immediately surrounding areas (Creighton, 1934; Wilson, 1963). A second population has been discovered in the Stanislaus National Park of California by G. C. and J. Wheeler (1968). Chamberlin (in Wheeler, 1910a) found Formicoxenus (= Symmyrmica) chamberlini only “in several parts of a ten-acre field" near Salt Lake City, Utah, in 1902, and only three colonies were located there. After an intensive search eighty years later Buschinger and Francoeur (1983) rediscovered a sparse population in the same area.  The extreme parasite Teleutomyrmex schneideri''  has one population apparently limited to the east side of the isolated Saas-Fee Valley of Switzerland, between 1,800 and 2,300 meters elevation (Kutter, 1950a); a second local population has been discovered near Briançon in the French Alps (Collingwood, 1956).

A second means of enlarging the effective population size, which might be favored by group selection (or more precisely, interdemic selection) is the reduction in the average colony size, which increases the number of colonies for a fixed total number of individual ants. Still another is the promotion of outbreeding, by such mechanisms as the appearance of the male before the reproductive females in individual colonies (protandry), fully developed nuptial flights that carry the reproductive forms away from the natal nests, and the synchronization of nuptial flights to bring together males and females from different colonies at the time of mating.

Have in fact the rare species taken these steps? From

the evidence presented in Table 6-1, it can be seen that a significantly higher number of such species have multiple queens in comparison with related species. The inference that can be drawn is that selection is strong enough at the level of entire populations of colonies (as opposed to individual colonies), due to the danger of extinction through small population size, to force polygyny on the colonies. But the inference is weak since polygyny also occurs in many ant species that are abundant and widespread.

To summarize, one circumstance by which polygyny might have arisen in ants is by group selection acting on rare species, the category in which interdemic selection is generally most likely to be potent. However, an alternative explanation for polygyny in rare species is available: because of the small number of individuals, associated queens might be more closely related than is the case in larger, more typical populations. Hence, as originally suggested for Formica rufa by Williams and Williams (1957), altruistic cooperation among queens would be favored due to sister-group selection. At the present time there is no clear way to decide between these two competing hypotheses.

An examination of Table 6-1 shows that decrease in colony size, another means of raising effective population size, in fact does not occur among the rare species. Furthermore, the data show no evidence of an increase in exogamy, the tendency of the sexual forms to mate with members of other colonies. Quite the contrary; the rare species have reduced the level of exogamy. Mating among members of the same colony, which has the effect of turning the colony into something resembling a self-fertilizing hermaphrodite, has long been recognized by myrmecologists as a trait of the rarest, parasitic species. The males are often apterous or subapterous, mating takes place in or near the nest, and the fecundated, winged queens then either disperse in search of new host colonies or else return to the old. Whether intracolonial mating characterizes other categories of rare species is an open question. Since the trait must cause a decrease in the effective breeding size of the population, just the reverse of what purely logical considerations concerning population size alone dictate, it is necessary to consider other possible advantages of such a design feature. At least one can be deduced: intracolonial mating certainly eliminates the loss of virgin reproductives normally occurring during dispersal and insures that the queens will be inseminated, however scarce the species. This advantage can easily outweigh disadvantages from inbreeding. Passing from random mating to perfect inbreeding reduces the effective breeding size by only half, a deficit that can be balanced merely by doubling the average number of nest queens. The exact extent of true brother-sister mating is unknown. Because of the additional trait of polygyny in these same species, the offspring of several matings probably breed with each other as a matter of course. In fact, Wesson (1939) did find that the queens and males of Protomognathus (= Harpagoxenus) americanus prefer to mate with unrelated individuals. It is even conceivable that parasitic species are less “adelphogamous” than previously assumed since it has not been established with certainty that true brothers and sisters within polygynous colonies really mate with each other at all. In polygynous colonies the opposite may be true.

Specialized nest sites. A much stronger correlation exists between polygyny and the manner in which colonies occupy nest sites. Truly polygynous species, most or all whose colonies contain multiple inseminated queens, fall into one or the other of three sets characterized by very different adaptation syndromes. (1) The first type is specialized on exceptionally short-lived nest sites. Such species are opportunistic in the sense employed by ecologists--they occupy local sites that are too small or unstable to support entire large colonies with life cycles and behavioral patterns dependent on monogyny. (2) The second type is specialized on nest sites that are scarce, evidently conferring advantages on queens willing to group together in lasting associations. (3) The third type is specialized on habitats--entire habitats as opposed merely to nest sites--that are long-lived, patchily distributed and extensive enough to support large populations. The three forms of specialization are not mutually exclusive; some ant species, for example Iridomyrmex humilis and Pheidole megacephala, possess features of the first and third types.

Consider first the class of opportunistic nesters. Colonies of Tapinoma melanocephalum, Tapinoma sessile, Paratrechina bourbonica, and Paratrechina longicornis often occupy tufts of dead grass, plant stems, temporary cavities beneath detritus in urban environments, and other local sites that sometimes remain habitable for only a few days or weeks. For example, colony fragments of Tapinoma sessile observed by Smallwood (1982) moved an average of every 12.9 days. Some species of Cardiocondyla excavate shallow tunnels and chambers in patches of soil in such places as the edges of palm trunks, sidewalks, and street gutters. Leptothorax curvispinosus typically nests in confined and relatively unstable preformed cavities in acorns, hickory nuts, galls, stems, and twigs. Lasius sakagamii favors unstable river banks, sandy and sparsely vegetated areas that are frequently flooded (Yamauchi et al., 1981). On the rocky islets of the Gulf of Finland, Formica truncorum occupies flimsy nest sites in which temperature varies in an unreliable manner (Rosengren et al., 1985). Colonies of Monomorium pharaonis and Tapinoma melanocephalum  go so far as to invade houses to occupy cracks in walls, the lining of instrument cases, spaces in piles of discarded clothing, between leaves of books, and similarly unlikely microhabitats. Colonies of these species are characterized by extreme vagility--a readiness to move when only slightly disturbed and the ability swiftly to discover new sites and to organize emigrations. Their colonies are also typically broken into subunits that occupy different nest sites and exchange individuals back and forth along odor trails. Colonies of opportunistic nesters bud, disperse, and fuse again, as documented in Tapinoma erraticum by Dubuc and Meudec (1984) and various species of Leptothorax  by Buschinger (1974a), Möglich (1978), Alloway et al. (1982), and Stuart (1985b). We suggest that it is the latter quality that gives polygyny a premium in opportunistic nesting and ties it closely to polydomy, the occupation of multiple nest sites. Because of the inevitable frequent fragmentation of the colonies, subunits probably lose contact with one another for long periods of time and occasionally forever. Having enough reproductive females to service most or all of the subunits means that the colony as a whole can exploit the rapidly fluctuating environment in which it lives. Other kinds of ants are not fragmented in this manner, and consequently a single queen suffices as the colony progenitrix.

The second class of polygynous nesters was recently defined by Herbers (1986a,b) and has only a single known example, the small North American myrmicine Leptothorax longispinosus. The species prefers hollow acorns and other preformed cavities on the ground, sites that are usually in short supply. Herbers found that the percentage of colonies that are secondarily polygynous increases with the local density of colonies, and she was able to exclude nest site fragility as a potent factor.

The third major class of fully polygynous ant species contains only a few species, but they include the great majority of examples that have been both well studied and do not qualify as opportunistic nesters. Thus, most fully polygynous species whose natural history is known to us are accounted for by the simple dichotomous classification proposed here. The habitats favored by species in the second category are first of all patchily distributed; they have distinctive qualities and are more or less isolated from each other. They are also extensive enough to support substantial populations of ants. Hence propagules of species that are specially adapted for such places encounter a potential bonanza when they succeed in colonizing one. The habitats are also relatively long-lived, giving a premium to the type of slow but thorough occupation made possible by polygyny and budding.

For example, the Allegheny mound-builder Formica exsectoides typically occupies persistent grassy or heath-like clearings. Such habitats are relatively scarce and patchily distributed, and many are fully occupied by dense unicolonial populations of Formica exsectoides. The “microgyna” form of Myrmica ruginodis (which is almost certainly a distinct species in its own right; see Pearson, 1981) shows a similar preference for scattered, very stable open habitats in England, some of which are known to have persisted at the same localities for as long as 200 years. The typical, or “macrogyna” form, which is haplometrotic and monogynous, favors less stable but more widespread habitats (Brian and Brian, 1955). Pseudomyrmex veneficus is specialized to occupy species of swollen-thorn Acacia  that grow for long periods of time in areas of slow floristic succession. Because the acacias are able to expand into extensive thorn forests, the Pseudomyrmex veneficus colonies have the opportunity to build large unicolonial populations over a period of many years. Single populations may contain 20 million or more workers, rivaling Dorylus ants for the possession of the largest ant "colonies" in the world (Janzen, 1973b). Both are exceeded easily, however, by Formica yessensis, one supercolony of which in Hokkaido was estimated to contain 306 million workers and 1,080,000 queens (Higashi and Yamauchi, 1979; Higashi, 1983). "Tramp" species, those ants distributed widely by human commerce and living in close association with man, are typically polygynous. In a sense they can be said to have been preadapted for patchy but persistent and species-poor habitats created within man-made environments. Some of the best known species comprise unicolonial populations and spread largely or entirely by budding off of groups of workers accompanied on foot by inseminated queens. Examples include Monomorium pharaonis, Pheidole megacephala, Iridomyrmex humilis, and Wasmannia auropunctata.

The isolated-habitat specialists, as distinguished from the nest-site opportunists, are species that have difficulty locating their preferred habitats, but once having found a suitable place, are opposed by relatively less competition from colonies of their own or other ant species. Thus it is to the advantage of the founding colony to spread out as a continuous unicolonial population, occupying all of the habitable nest sites and foraging areas. An example involving the Argentine ant Iridomyrmex humilis is shown in Figure 6-2. In contrast, most other ant species have no trouble finding a suitable habitat, but such places are typically already saturated with other ant colonies. The best strategy of these ants is to send out large numbers of flying queens capable of founding new colonies independently. A tiny fraction of the propagules will locate some of the rare nest sites and foraging areas left unfilled; the colonies they produce will not find it profitable to try to spread outward through the surrounding occupied territories by budding in the unicolonial manner.

The full life cycle of unicolonial populations remains to be worked out in detail, although details of the structure and secular changes over a period of up to a few years have been studied in the huge colonies of Formica lugubris in Switzerland by Cherix (1980), Formica polyctena  in the Netherlands by Mabelis (1986), and Formica aquilonia  in the Soviet Union by Zakharov et al. (1983). A map of part of the Formica lugubris

colony is presented in Figure 6-3. Among the interesting variables to be studied as functions of the age and condition of the populations are the queen:worker ratios and the behavior of queens during nuptial flights. Scherba (1961) reported that most of the queens of Formica opaciventris, a North American mound-building, unicolonial species, mate within a few meters of their nest of origin and return at once, while a small minority, originating entirely from mounds near the edge of the population, fly out of sight in a direction away from the population. A very similar pattern occurs in at least one of its European equivalents, Formica polyctena, the life cycle of which was presented in Chapter 3 (see also Gösswald and Schmidt, 1960). We predict that in the early stages of population growth, the queen:worker ratio will start high (immediately following independent nest founding by one or more newly inseminated queens, usually by adoption of an alien host species), drop to a steady state as the population comes to saturate the habitat, then rise again as the habitat quality declines and a higher premium is placed on dispersal away from the habitat. It also seems likely that a fraction of the queens engaging in dispersal flights will increase when the habitat is saturated, and increase still more as the habitat declines.

Thus in a curious fashion the extreme polygynous species have evolved unicolonial populations as a means for trading dispersibility for potential colony immortality. Where competitive pressure is less, the species can afford to gamble on great longevity. The colonies can be fused into single units, and newly mated queens can more safely return to the parental nests. And since colonies are on the average longer lived, fewer empty nest sites will be available at any given time, making the dissemination of queens away from the parental nests less profitable. The results will be a dual pressure for the unicolonial species to suspend claustral nest founding altogether. The adoption of unicolonialism, with its increased degree of inbreeding and reliance on budding as the principal means of reproduction is an evolutionary step that parallels the adoption of apomixis and vegetative reproduction in nonsocial organisms. Both permit the rapid growth of population in habitats that are relatively free of competing ants but sparsely distributed.

An interesting phenomenon for which no explanation yet exists is the frequent coexistence of pairs of closely related species, one of which is monogynous and the other polygynous. Examples include the “macrogyna” and “microgyna” forms of Myrmica ruginodis, probably at least a few other European species of Myrmica (Pearson, 1981), the acacia ant Pseudomyrmex veneficus  and an undescribed polygynous sibling form in Mexico (Janzen, 1973b), two apparent species placed under Crematogaster minutissima  (Wilson, unpublished), Dorymyrmex insanus  and Dorymyrmex  flavopectus  (Nickerson et al., 1975), Formica incerta and Formica nitidiventris  (Talbot, 1948), and two apparently distinct species of Formica neorufibarbis  in the White Mountains of New Hampshire (Wilson, 1971). A similar duality appears to exist in Formica “rufa,” which apparently consists of two sibling species, one strictly monogynous and the other polygynous (Kutter, 1977). It is also possible for at least the rough equivalents of monogynous and polygynous strains to occur as genetic polymorphs within the same species, as in the "A" and "B" colony types of Rhytidoponera confusa and Rhytidoponera chalybaea  in Australia (Ward, 1983a,b).

Variable food supply. A third principal clue to the origin of polygyny, as well as mixed strategies among and within species with respect to the number of queens, has been provided by Briese (1983) in his study of an Australian species of Monomorium (= Chelaner) belonging to the rothsteini  group. He followed two colonies over a two-year period in a semi-arid saltbush steppe in New South Wales. One, containing winged queens capable of flight, started new colonies by the conventional means of nuptial flights followed by claustral nest founding. The other, containing brachypterous (short-winged) queens unable to fly, started new colonies by fission. The brachypterous queens were either adopted back into the natal nest or escorted to new nest sites by their worker sisters. Both procedures led to polygyny with brachypterous queens. Flights by the normal-winged queens occurred after a favorable period of substantial rainfall that increased the food supply, principally seeds. Fission by brachypterous females followed a drought and reduced food supply (Figure 6-4). Briese considered the two kinds of colonies to belong to the same species, and their founding methods to constitute alternative responses of a mixed strategy:

When conditions are favourable, the production of fully alate queens, with sufficient body reserves to raise a first brood by themselves, would allow a colony to extend its genetic material over a much wider area with maximised chances of successful establishment. When stress is very severe queen production may cease altogether. However, under conditions of less severe food stress, the mode of colony foundation might alter, and brachypterous queens with less body reserves be produced. During colony foundation, these would be accompanied by groups of worker ants which act as food gatherers to support the initial brood. Such daughter colonies would remain in the same, relatively favourable area, still capable of supporting a colony, rather than facing the risk of failure through the alternative mode of random dispersal to areas of unknown favourability.

The attractiveness of Briese's hypothesis is that it can be tested, regardless of whether the two queen morphs represent different species or variants of the same species. Further studies of this and other species can judge whether there is indeed a propensity of ants to evolve fission in areas of wide and erratic fluctuations in climate, such as occur in the arid Australian interior. Furthermore, it can be determined whether species that are truly polyethic with response to the two strategies favor fission during hard times.

Gyny and species diversity
Having reviewed the possible ecological prime movers that lead to monogyny or polygyny, let us now briefly consider some of the broader implications of variation in the number of queens. Monogyny is closely associated with colony distinctness. Each colony occupies a separate nest site, and its workers either avoid or attack the members of other colonies they encounter during foraging. The loss of territorial boundaries in the case of highly polygynous, unicolonial species changes the rules drastically. Unicolonial species are notable for their high local abundance and the degree to which they appear to dominate the environment. Introduced populations of Pheidole megacephala, Wasmannia auropunctata, and Iridomyrmex humilis extirpate many other kinds of ants, although it is not known whether species occurring within the native ranges of the unicolonial ants have evolved competitive resistance to the point of being able to coexist. Habitats containing populations of Formica exsectoides have notably sparse ant faunas, and the related Formica exsecta  and Formica opaciventris  are known to exclude some other territorial ants, including other species of Formica, by aggression (Scherba, 1964; Pisarski, 1972). The same is true of Formica aquilonia and Formica polyctena, the “large-scale conquerors” of the Formica rufa group in Europe (Rosengren and Pamilo, 1983). It is not known to what extent the general occurrence of unicolonial species in species-poor habitats is a cause and to what extent it is an effect. The matter can be put as a question: have the unicolonial ants simply adapted to habitats that were species-poor in the first place, or does the formation of supercolonies provide them with a decisive competitive edge in habitats that would otherwise be species-rich? This problem seems eminently tractable to field analysis (see Chapter 11).

It is possible that gyny and the nature of territoriality also affect the patterns of species diversity and quite possibly the mechanism of speciation itself. Local faunas consisting of multicolonial ant populations, which comprise in turn chiefly monogynous and oligogynous colonies, seem to be more susceptible to increases in within-habitat species diversity, for three reasons. First, as previously noted, they appear to suppress other ant species less severely than do unicolonial populations, permitting the buildup of larger numbers of coexisting species. Second, because the colonies are much smaller in size, multicolonial species are able to specialize more on nest sites and food. For example, a colony of one species might do well with a single hollow stem, while a colony of another species is able to occupy the space beneath a nearby stone. Other species can be differentiated according to food, some preying exclusively on small arthropods, others mostly tending scale insects, and so forth. The relatively huge populations of unicolonial species cannot afford a narrowing of their niche. In order to survive they must remain broad generalists, which brings them into competition with a large number of specialists as well as other generalists.

The third reason why multicolonial species can be expected to exhibit higher within-habitat diversity is more subtle. Many studies have shown that colonies of ants are hostile to a degree inversely proportional to the degree of similarity to their competitors. That is, they are most aggressive to other colonies of the same species, somewhat less to other species in the genus, and least of all to forms that not only belong to other genera but differ strongly in size and behavior. This being the case, within-habitat diversity can be expected to be enhanced by the divergence of species odors between closely related species. Suppose that two newly formed, cognate species have arisen by genetic divergence during geographical isolation, and have recently come into contact along the boundaries of their respective geographical ranges. Suppose further that the species are sufficiently divergent in ecological requirements so that neither would exclude the other by means of nonaggressive preemption of resources. Yet the two forms are likely to remain in separate geographical ranges so long as their species odors are too similar, causing interspecific territorial exclusion to be as strong as intraspecific exclusion. The two species can penetrate one another's range only if one or both undergoes a divergence in the species-specific components of the colony odor. This would be a form of character displacement comparable to the divergence of identifying songs by which territorial bird species penetrate one another's ranges (Murray, 1971). The result is an increase in the within-habitat species diversity.

The penetration of territories belonging to alien monogynous species is made easier by the very fact that territorial colonies repel one another so effectively--to the extent that colonies are overdispersed in their statistical pattern of distribution. In many kinds of ants, such as members of the genus Pogonomyrmex, this pattern is geometrically very regular and is maintained by high levels of intercolonial aggression (Hölldobler, 1974, 1976a). If colonies of other species are different enough in species specific components of the colony odor to escape such aggressive response, and if they are also distinct enough in their foraging habitats not to be replaced through competitive exclusion, they might easily slip into nest sites located between those of the resident species.

In an earlier analysis (Hölldobler and Wilson, 1977b), we hypothesized that the degree of odor specificity associated with monogyny and intercolony territoriality lends itself to interspecific recognition, the reduction of interspecific territorial aggression by means of that recognition, and an increase in numbers of species that can coexist in the same habitat. Many polygynous ant species, and particularly those that are unicolonial, have surrendered some of this discriminatory power. As a result they remain aggressive toward a broader range of species, and it is not surprising to find very few unicolonial species occupying the same habitat, as well as an overall decrease in species diversity. Although it is theoretically possible for unicolonial ant species to build up between-habitat diversity by means of specialization on habitats as opposed to niches within habitats, very little appears to have occurred in nature--quite possibly due to the preemption of most kinds of habitats by monogynous, multicolonial ant species.