The Ants Chapter 8

CHAPTER 8. CASTE AND DIVISION OF LABOR

It is possible to distinguish two very general problems in the study of social insects, to which all other topics and theoretical reflection play a tributary role. The first is the origin of social behavior itself. Biologists are especially interested in the advanced state of eusociality, which characterizes all of the ants and a small percentage of aculeate wasps and bees. This evolutionary grade is defined as the combination of three features: care of the young by adults, overlap in generations, and a division of labor into reproductive and nonreproductive castes.

The last of the eusocial traits, the existence of a subordinate or even completely sterile worker caste, is the rarest of the three. It is also by far the most significant with reference to the further evolutionary potential of social life, for when individuals can be turned into specialized working machines, an intricate division of labor can be achieved and a complicated social organization becomes attainable even with a relatively simple repertory of individual behavior. It does not matter, to use a rough metaphor, if the separate pieces of a clock are simple in construction, so long as they can be shaped to serve particular roles and then fitted together into a working whole. You cannot construct a proper clock if every little piece must also keep some sort of time on its own. By the same token natural selection cannot readily assemble a complex colony if every member is designed to complete a reproductive life cycle of its own in the vertebrate manner.

This brings us to the second major problem in the study of social insects, which can be called strategic design, or, more fully, the strategic design of colonies. Once a sterile worker is in place, that is, once the equivalent of the less-than-independent levers and wheels of the clock can be manufactured, the important consideration becomes the best arrangement of castes and division of labor for the functioning and reproduction of the colony as a whole. The colony can be most effectively analyzed if it is treated as a factory within a fortress. Natural selection operates so as to favor colonies that contribute the largest number of mature colonies in the next generation, so that the number of workers per colony is only of incidental importance. In other words, the key measure is not how big, or strong, or aggressive a colony of a particular genotype can become but how many successful new colonies it generates. Hence the functioning of the workers in gathering energy and converting it into virgin queens and males is vital. This part of colony functioning constitutes the factory. But the colony is simultaneously a tempting target for predators. The brood and food stores are veritable treasure houses of protein, fat, and carbohydrates. As a consequence colonies must have an adequate defense system, which often takes the form of stings and poisonous secretions and even specialized soldier castes. This set of adaptations constitutes the fortress.

The ultimate currency in the equations of colony fitness is energy. The workers appear programmed to sweep the nest environs in such a way as to gain the maximum net energetic yield. Their size, diel rhythms, foraging geometry, recruitment techniques, and methods of food retrieval are the qualities most likely to be shaped by natural selection. But even as energy is being collected and distributed to the queen and brood, the colony is subject to predation and competition. A certain number of individuals must be sacrificed in periodic defenses of the colony and during the riskier steps of the daily foraging expeditions. The loss of energy required to replace them is entered on the debit side of the fitness ledger.

Colony design then becomes effectively a problem in economics. The more precise expression is ergonomics, to acknowledge that work and energy are the sole elements of calculation, and also that nothing resembling human transactions with credit and money is involved (Wilson, 1968; Oster and Wilson, 1978).

Caste, task, role
The core of any ergonomic (as well as any human economic) analysis is the prescription of a complete balance sheet, and to this end it is necessary to define as precisely as possible the agents entailed. The fundamental distinctions among individual workers in a colony are based on the actual tasks they perform and the various roles they play in accomplishing the functions of the colony as a whole. An example of the behavioral repertories of two physical castes is given in Table 8-1.

Lists of distinct behavioral acts are made from protracted observations of individuals, selected sets of individuals, or, the entire colony. If distinct physical and temporal groups can be distinguished, separate repertories for each are compiled. In the unlikely event that some of these arbitrarily defined categories prove to have identical repertories, they cannot be distinguished as separate castes --and the data concerning their repertories can be subsequently combined. The next step is to compute the relative frequencies of the acts and to fit them to standard distributions such as the lognormal Poisson or negative binomial. This method has been used with success by Fagen and Goldman (1977) to make estimates of total repertory size even before a complete catalog is actually compiled. An observer thus can obtain a measure of the adequacy of his sample size. For example, after 1,222 separate behavioral observations had been made on the minor worker caste of a colony of Pheidole dentata, 26 kinds of behavioral acts could be recognized; the latter constituted the known behavioral repertory of this caste. By fitting the frequency data (see Table 8-1) to a lognormal Poisson distribution, the actual number of kinds of behavioral acts was estimated to be 27, with a 95 percent confidence interval of (26, 28). The major workers were observed performing 8 kinds of behavioral acts; the true number was estimated to be 9, with a confidence interval of (8, 10).

As analyzed by Wilson and Fagen (1974) there are notable strengths and weaknesses in this method of tabulating behavioral repertories, which has gained wide usage in the study of behavior. One obvious advantage of the technique is that it improves unaided intuition without forcing any new, unsupportable assumptions on the analysis. Another is that the tabulation allows a more precise judgment of the point of diminishing return during ethological studies. That point comes surprisingly early in the case of the ants. A typical example is the study of worker behavior in Leptothorax curvispinosus conducted by Wilson and Fagen. After only 51 hours of observation, during which 1,962 separate acts were recorded, the mode of the frequency curve emerged and the estimated sample coverage attained was 99.95 percent. Thus the effort required to secure a nearly complete repertory is at least a full order of magnitude less than in the case of vertebrates, which typically consumes months or years of arduous field research. The result is that comparative behavioral studies have proceeded much more rapidly in ants and other insects.

The tractability of ant studies has a rationale of considerable biological interest. This is the small number of rare behavioral acts that exist relative to common acts (see Figure 8-1). In other words, whatever ants do they do rather frequently in comparison with vertebrates; few if any rare behaviors exist to surprise the investigator in the late stages of the study. It is possible that the small size of the ant brain precludes the storage of acts that are not used commonly or at least are not of crucial importance to the colony. This interpretation is consistent with the principle of parsimony in the evolution of ant communication systems, which we documented in Chapter 7. In briefest form, the concept of parsimony holds that a characteristic of ant behavior is the repeated use of the same communicative signals and responses in different contexts to achieve multiple purposes.

There are two disadvantages of the method which we do not regard as particularly serious. The first is the probability that the repertories and especially the frequency distributions change in different contexts. It remains for the biologist to define those contexts and to repeat the analysis within them. In the case of ants distinguishable contexts are not only finite but also probably quite limited in number. By far the greatest part of an ant's life is conducted in the homeostatic environment of the nest interior. Thus the lifetime sample coverage in the Pheidole dentata study, defined as the cumulative probability of all behavior for all contexts, was probably very high in spite of the fact that it was limited to one environment. We suggest that the following list might exhaust the remaining contexts for the worker caste: extended foraging periods and territorial patrolling and defense; major disturbances of the nest, including invasion by alien colonies, flooding, and overheating; emigration to a new nest site; and assisting during the initiation of nuptial flights on the part of the reproductive forms.

The second difficulty in repertory estimation is the arbitrariness of the definition of the behavioral act. One observer might see three distinct neuromuscular patterns where another sees only one. Thus “foraging” as defined in Table 8-1 could easily be broken down into several acts. This is essentially a problem of language, and different observers can solve it by a straightforward mapping procedure. One observer's acts a, b, and c will be recognized as comprising the second observer's act a; the first observer's act h will be seen as representing the second observer's acts m and n; and so forth. No great difficulty should occur when the same species is considered or closely related species are compared. Serious conceptual problems might exist, however, when an attempt is made to compare the size and frequency characteristics across radically different species.

The next step beyond the behavioral repertory is the construction of an ethogram, which incorporates not only the repertory of a caste but also the transition probabilities connecting individual acts and the time distributions spent in each act. When the ethogram also takes into account the interactions of parents and offspring, dominant and subordinate individuals, and other members of the society, the description is referred to as a sociogram. Ethograms can cover all of the repertory or certain well-defined portions of it. Such quantitative studies have been conducted on ants, honeybees, hermit crabs, mantis shrimps, and rhesus monkeys, with promising results (see reviews by Dingle, 1972; Wilson, 1975b: 194-200).

Figure 8-2 illustrates an imaginary example of an ethogram with role and castes delimited. For any individual, certain of the behavioral acts (ai) will be linked together by relatively high transition probabilities: in Pheidole dentata, for example, pupal licking is associated with high frequency to pupa carrying, egg licking, and egg transport; nest construction gives way with high probability to foraging outside the nest; and so on. A set of closely linked behavioral acts can be defined as a role, even if the acts are otherwise quite different. It is generally true, for example, that the act of grooming the queen is closely linked with the very different acts of regurgitating to the queen and removing freshly oviposited eggs. All of these responses can be considered part of the single role of queen care. We can define a caste as a group that specializes to some extent on one or more roles. Broadly characterized, a caste is any set of a particular morphological type, age group, or physiological state (such as inseminated versus barren) that performs specialized labor in the colony. A natural classification follows from this definition. A physical caste is distinguished not only by behavior but also by distinctive anatomical traits. A temporal caste, in contrast, is distinguished by age. A physiological caste is distinguished by a principal physiological state that is frequently but not necessarily linked to anatomy or age, such as insemination. Sometimes all of the workers together are referred to as a caste, as distinct from the queen, and subsets of workers are called subcastes.

The term task is used to denote a particular sequence of acts that accomplishes a specific purpose, such as foraging or nest repair. Ordinarily a task is identical to a role or is composed of the subset of acts within a role, but it might conceivably consist of acts distributed across two or more roles. Finally, the division of labor by the allocation of tasks among various castes is often referred to as polyethism, a term apparently first employed by Weir (1958a,b). We further speak of physical caste polyethism as opposed to temporal caste polyethism.

Few studies have probed to the depth necessary to yield quantitative measures of castes and tasks. Wilson (1976c) recognized four worker subcastes of Pheidole dentata, comprising a unified age category in the major worker and 3 age categories in the minor worker. Together the castes perform a known total of 26 acts in undisturbed colonies, of which 23 can be classified as true social tasks. Similarly, a total of 29 tasks have been identified in the leafcutter ant Atta sexdens (Wilson, 1980a). These are performed by an estimated four physical castes, of which three are further subdivided into temporal castes to make a total of at least seven castes overall. The most thorough studies of labor division have been conducted on Lasius niger (Lenoir, 1979a,c) and on species of Leptothorax (Herbers, 1983; Herbers and Cunningham, 1983). These authors combined matrix analysis with methods of multivariate analysis to cluster the tasks into roles. Two or three roles, or “components” as they were called by Lenoir, could be recognized in Lasius. In the Leptothorax, the workers comprised three behavioral castes filling a total of four roles.

It will be useful at this point to introduce a short glossary of terms applied to castes that have gained at least moderate employment by myrmecologists. This is a difficult procedure, for two reasons. First, an extraordinary number of technical terms has been proposed. Many of them were suggested by William Morton Wheeler, who was not only a great entomologist but a classical scholar fluent in Greek with an inordinate fondness for neologisms. In 1907 he proposed a caste system based on anatomy with no fewer than 30 categories. He recognized pathological forms such as the phthisaner, a pupal male with appendage growth caused by an Orasema wasp larva; the pseudogyne, a worker-like form with swollen mesothorax in the genus Formica caused by the presence of lomechusine staphylinid beetles in the nest; and the pterergate, a worker ant with vestiges of wings. During his lifetime and especially in his last work on the subject in 1937, Wheeler believed he had found good reasons for multiplying and naming every qualitatively distinguishable form. On the one hand he considered the parasitogenic forms to be different enough and rare enough to fit comfortably into the system. More important, however, he believed (erroneously) that most nonparasitogenic castes arise by genetic mutations. He saw no fundamental difference between normal functional castes and true anomalies. All except the queen and typical males were basically anomalous forms to Wheeler, and he referred to his categories alternatively as castes, phases, and anomalies. In a reevaluation of Wheeler's system, Wilson (1953b) concluded that some of the names are superfluous, some are virtually synonymous with others, and some are no more than stages in an allometric progression. Over the years a substantial literature of teratology has accumulated on gynandromorphs and other developmental anomalies, some of which possess traits intermediate between normal castes, but there has been no inclination to recognize any of these forms as castes; descriptions and reviews have been provided variously by Wheeler (1937b), Novak (1948), Kusnezov (1951a), Buschinger and Stoewesand (1971), Wilson and Fagen (1974), Sokolowski and Wisniewski (1975), Peru (1984), and Taber and Francke (1986).

A second cause of ambiguity in classification is the dispute among leading students of the subject over whether castes should be defined primarily by role or by anatomy. In particular, Buschinger (1987b) has proposed that “queen” and “worker” be used to designate females with reproductive and nonreproductive roles, regardless of whether they differ anatomically in a particular species, while various other terms such as gynomorph and intermorph be used to denote the anatomical variants within these two principal categories. Peeters (1987a,b), in opposition, prefers a morphological definition of the castes “queen” and “worker," with the term “gamergate” being used for the relatively uncommon condition in which mated, completely worker-like forms have replaced the queen caste in “queenless” societies. The two positions are conceptually not far apart and can be semantically resolved.  Our opinion is that the classification should be kept somewhat loose, incorporating either anatomy or roles in a manner that maximizes convenience, precision, and clarity of expression.  It must be recognized that anatomy and reproductive role are related across the various ant species not on a one-to-one linkage but by a many-to-many linkage.  That is, anatomical workers often join the anatomical queens in reproduction although usually to a limited extent.  In such species the reproductive role can be said to be assumed by both anatomical castes. And queens in their turn assume many roles other than reproduction. Such many-to-many relationships are nearly universal among the anatomical worker subcastes and labor roles. It is also true that anatomically distinct (i.e., physical) castes are almost always biased toward certain roles, while individual roles are almost always filled preferentially by one anatomical caste or another in the case of polymorphic species. With these qualifications in mind, the following annotated glossary is the most efficient and for the most part reflects current usage (see also Figure 8-3).

1. Male. In the great majority of ant species, males (designated by the symbol ) fill no role in the colony that generated them, being content to receive food from their sisters while awaiting the nuptial flight that will end their lives. In such cases it is misleading to refer to them as a caste. In some species of Camponotus, the males are long-lived and serve as donors in food exchange within the colony. Hence they qualify marginally as castes. To take another, very different phenomenon, worker-like or “ergatomorphic” males occur in several genera (Hypoponera, Cardiocondyla, Formicoxenus, Technomyrmex). However, so far as known they do not contribute to colony labor.

2. Queen. Often designated by the symbol  (contrast with symbols for worker, to follow). In the broad sense, the principal female reproductive type, in other words any form anatomically distinguishable from the worker caste and responsible to a disproportionate extent for reproduction. In the narrow sense, employed in more technical literature on caste biology, the fully developed reproductive female, possessing a generalized hymenopterous thorax and functional but deciduous wings. The queen is sometimes referred to loosely as the “female” of the colony. The term gyne was used synonymously with queen by Wheeler (1907a). Brian (1957b) employed it to denote more specifically “a sexual female that is not socially a functional reproductive.” In recent years the word has gained wider usage in conformity with Wheeler's original meaning. It is employed most consistently as a neutral expression, to cover any reproductive female whether virgin or inseminated, laying or infertile. In these writings, “queen” then denotes a functioning gyne. In a few species such as the primitive Australian Nothomyrmecia macrops, the wings are reduced in size and probably nonfunctional (Figure 8-4). Such individuals are designated micropterous queens (or micropterous females) in the literature. Occasionally, queens are exceptionally small, even smaller than the workers in some dimensions. Such microgynes, as they are called, are usually social parasites. Examples are found in the South American myrmicine Pheidole microgyna (Wilson, 1984c), the parasitic and microgynous form of the European Myrmica rubra complex (Pearson, 1981), and members of the North American Formica microgyna group (Wheeler, 1910a; Creighton, 1950). Microgynes coexist in the same colonies with normal, “macrogynous” queens, in the arboreal Pseudomyrmex veneficus (Janzen, 1973b) and an arboreal Australian species of Polyrhachis subgenus Cyrtomyrma (Bellas and Hölldobler, 1985; see Figure 8-5).

3. Worker. Often represented by the symbols  or. The ordinarily sterile female, possessing reduced ovarioles (or none at all) and a greatly simplified thorax, the nota of which typically consist of no more than a single sclerite each (Tulloch, 1935). Even when ovarioles are present, the workers usually lack spermathecae in which sperm can be stored. Hence when they become reproductive they cannot produce daughters except by thelytokous parthenogenesis--an uncommon event in ants generally (Crozier, 1975; Buschinger and Winter, 1978; Choe, 1988; Bourke, 1988). The disparity between the reproductive apparatus of workers and queens varies considerably among ant species. In Nothomyrmecia macrops, a very primitive ant, workers possess four to seven ovarioles and queens eight to ten (Hölldobler and Taylor, 1983). In Leptothorax nylanderi only two ovarioles are found in workers and eight in queens (Plateaux, 1970; Figure 8-6), while in Formica polyctena workers have four to six ovarioles as against 90 and 270 in queens (Otto, 1958, 1962; Figure 8-7). On the other hand in some species of Rhytidoponera whose mated workers have replaced the queen as the functional egglayers, there is no significant difference between the ovaries of reproductives and those of non-reproductives. However, only inseminated workers appear to lay eggs (Peeters, 1987b). The queen of Eciton hamatum has approximately 4600 ovarioles (Hagan, 1954), and that of Eciton burchellii has at least twice as many (Whelden, 1963; Schneirla, 1971). In some other species, such as the members of Pheidole and Solenopsis, workers possess no ovarioles at all (Wilson, 1971). The worker caste is often subdivided into additional castes, or subcastes, as follows:

4. Minor, media, major. Castes in a size-variable worker series are designated according to ascending size as minor, media, or major workers. In some species the media subcaste mostly or entirely drops out, and the minor and majors are easily distinguished as two frequency distributions with distinct modes. In this case, the symbol  designates the major, and the symbol   usually designates the minor. When their function is partly or wholly fighting on behalf of the colony, the majors are often referred to as soldiers.

5. Ergatogyne. A reproductive form anatomically intermediate between the worker and the queen. A variety of relatively informal terms have been used to denote the intermediates. These terms range from “apterous females” (Bolton, 1986b), and “gynomorph” or “gynomorphic workers,” “ergatomorph” or “ergatomorphic queens,” and “intermorphs” (Buschinger and Winter, 1976). We are inclined to favor a bipartite classification suggested to us by Christian Peeters (personal communication). It makes a distinction between intercastes, which are forms that are intermediate in anatomy between workers and queens, commonly lack a spermatheca (and hence are incapable of mating), and occur in conjunction with typical workers and queens; and ergatoid queens, which are also intermediate in anatomy but possess spermathecae and typically replace the ordinary queen caste as the female reproductive.

Intercastes as just defined occur most commonly in social parasites of the leptothoracine genera Formicoxenus, Harpagoxenus, and Protomognathus (see Figure 8-53), but they also occur in some free-living species of Leptothorax and Monomorium. They give the impression of arising from a failure of endocrine regulation in the differentiation of queens and workers. In the most detailed study to date, Plateaux (1970) showed that there is a continuous anatomical progression in intercastes of the free-living Leptothorax nylanderi, manifested in body size, ocelli, segmentation of the thorax, number of ovarioles, the spermatheca, and elsewhere. While the character states are strongly concordant in the workers and queens, they vary independently of one another in the intercastes. For example, the thorax and gaster do not increase in size in a well coordinated manner, and some individuals occur that combine large ovaries with worker-like thoraces. Intercastes of most of the species, such as Harpagoxenus canadensis, Leptothorax nylanderi, and Protomognathus americanus, lack spermathecae. On the other hand, the intercastes of Formicoxenus species and Harpagoxenus sublaevis do have spermathecae and hence often mate and lay eggs.

Ergatoid queens, on the other hand, replace the typical queen entirely and are not connected to the worker caste by a graded series. This second, truly functional type of ergatogyne is especially common in the primitive genus Myrmecia and in several genera of the subfamily Ponerinae. Haskins and Haskins (1955) have pointed out that the tendency is partly correlated with the habit of queens of primitive ants to forage for food outside the nest during colony founding. In higher ants claustral founding is the rule, and queens usually must rear their first brood entirely on the reserves contained in their own fat bodies and degenerating flight muscles. Hence fully differentiated queens are a necessity when colonies are founded claustrally. Ergatoid queens nevertheless do occur in some free-living higher ants. They are the rule, for example, in the aberrant dolichoderine genus Leptomyrmex (Wheeler, 1934a) and in the legionary cerapachyines (a tribe of the Ponerinae) and dorylines (Wilson, 1958e). They occur in Aphaenogaster phalangium of Central America and Blepharidatta brasiliensis (Wilson, unpublished). They are common in species of the Old World Monomorium salomonis group, where a graded series on the queen-worker gradient can be found among various species but not within species (Bolton, 1986b; see Figure 8-8). Ergatoid queens are also the sole form of reproductive in a high percentage of the endemic species of New Caledonia, belonging to such phylogenetically advanced genera as Monomorium (= Chelaner), Lordomyrma, Prodicroaspis, and Promeranoplus (Wilson, 1971). New Caledonia is an old, very isolated island, and ergatogyny in its ants corresponds to the flightless state found so commonly among the endemic species of birds and insects on oceanic islands. Where ergatoid and micropterous queens have replaced true queens in higher species, it seems likely that either workers accompany the reproductives during colony founding, or else the reproductives revert to foraging on their own during colony founding. Supporting evidence of the former alteration has been adduced in the case of Monomorium (= Chelaner) (Briese, 1983). Many ergatoid queens show a divergent trend away from the queen-worker gradient in that the development of the gaster and postpetiole outpaces the development of the thorax and head. Such variants possess a gaster that approaches (or surpasses) in size that of the typical queen, while the thorax and head are more typically worker-like.

6. Gamergates. A growing number of ponerine ants has been discovered in which the queen caste is replaced by reproductives that are anatomically indistinguishable from the worker caste. The species in this category include Diacamma rugosum (Wheeler and Chapman, 1922; Fukumoto, 1983; Moffett, 1986h), Dinoponera grandis (Haskins and Zahl, 1971), Leptogenys schwabi (Peeters, 1987a), Ophthalmopone berthoudi (Peeters and Crewe, 1984, 1985), Pachycondyla krugeri (Peeters and Crewe, 1986b), Platythyrea schultzei (Peeters, 1987a), and several species of Rhytidoponera (Haskins and Whelden, 1965; Ward, 1981a,b, 1983a,b; Peeters, 1987b). The only examples known from the Myrmicinae are apparently a few species belonging to the South American Megalomyrmex leoninus group (Brandão, 1987). Peeters has suggested the term gamergate for such inseminated workers, which seems a useful and clarifying step. It is the one case known to us of a true physiological caste, in which a particular physiological state (insemination and enhanced oogenesis) rather than anatomy or age distinguish a labor group. On the other hand, it may be pushing the term too far to include the reproductive workers of Pristomyrmex pungens, which are not fertilized and produce females by parthenogenesis. In this extreme, aberrant case the colony can be said to lack a physical caste system (Itow et al., 1984; Tsuji and Itô, 1986). On the other hand, Pristomyrmex pungens have a typical age caste system: young workers work inside the nest and lay eggs, while older workers have reduced ovaries and tend to work outside the nest (K. Tsuji, personal communication).

7. Dichthadiiform ergatogyne. The dichthadiiform female is the extreme stage of the phylogenetic trend toward enlargement of the gaster in the ergatogyne, and it is usually recognized as a distinct category. In fact, it is just an aberrant queen and is never accompanied by ordinary queens. The total size of the female is greatly increased, the gaster is huge, and the postpetiole is expanded to the extent that it has come secondarily to resemble the first gastric segment (see Figure 8-9). In addition, the head is broadened and rounded, the mandibles are often falcate, and the petiole is commonly bilaterally cornulate. Dichthadiiform females are limited to ants with a legionary mode of life. The extreme development is seen in the subfamilies Dorylinae, Ecitoninae, and Leptanillinae and the ponerine genus Onychomyrmex (Wilson, 1958e; see Figure 8-10). An intermediate stage in the evolution of this form occurs in the ergatogynes of the ponerine Acanthostichus quadratus and species of the ponerine genus Simopelta (Gotwald and Brown, 1966). All of these phyletic lines, both intermediate and advanced, evidently evolved their dichthadiiform form independently.

Temporal castes. We now take up a literally different dimension in caste formation. A temporal caste is a set of individuals distinguished both by behavior and by age. It is thus wholly different from physical castes, which are marked by some anatomical feature, and physiological castes, which may in a few cases be distinguished by insemination or some other principal physiological feature alone, in a manner unrelated to anatomy and age. In Pheidole dentata, for example, one temporal caste consists of the youngest workers, from the moment of emergence from the pupa to about two days into adult life. These individuals care preferentially for the queen, eggs, and young larvae. The second temporal caste, which tends to care for medium-sized larvae, extends to about the sixteenth day of adult life. The third temporal caste, which prefers nest work and foraging to a greater extent, consists of still older workers (Wilson, 1976c).

Adaptive demography
A key principle of caste evolution is the adaptive nature of colony demography (Wilson, 1968; Oster and Wilson, 1978). Ordinary demography, of the kind found in nonsocial organisms, in social vertebrates, and in more primitively social insects such as subsocial wasps and bees, is a function of the individual parameters of growth, reproduction, and death. A large amount of documentation from free-living and laboratory populations supports the general belief that growth and natality schedules are direct adaptations shaped by natural selection at the level of the individual (Krebs and Davies, 1981). On the other hand, the size and age structure of the population as a whole are epiphenomena, in the sense that they reflect the individual-level adaptations but do not constitute adaptations in their own right. Thus a sharply tapered age distribution in any species of fishes and birds results from a high birth rate and a high mortality schedule throughout the life span, but in itself does not contribute to the survival of the population or the individual members. The exact reverse is the case of the eusocial insect colony defined as a population. The demography, not its causal parameters, is directly adaptive. The workers are for the most part sterile; their birth and death schedules have meaning only with reference to the survival and reproduction of the queen. Hence the unit of selection is the colony as a whole. The traits of the colony are the larger features of demography, the age and size-frequency distributions. What matters are such higher-level traits as the number of very large adults available to serve as soldiers, the number of small young adults functioning as nurses, and so on through the entire caste roster and behavioral repertory. Each species has a characteristic age-size frequency distribution, and the evidence is strong that this colony-wide trait is not an epiphenomenon, but has been shaped by natural selection, constituting a direct adaptation (see Figure 8-11).

A striking example of adaptive demography is provided by developmental changes in the caste system of the leafcutter ant Atta cephalotes (Wilson, 1983b). Beginning colonies, started by a single queen from her own body reserves, have a nearly uniform size-frequency distribution across a relatively narrow head-width range of 0.8-1.6 mm. The key to the arrangement is that workers in the span 0.8-1.0 mm are required as gardeners of the symbiotic fungus on which the colony depends, while workers with head widths of 1.6 mm are the smallest that can cut vegetation of average toughness. This range also embraces the worker size groups most involved in brood care. Thus, remarkably, the queen produces about the maximum number of individuals which together can perform all of the essential colony tasks. As the colony continues growing, the worker size variation broadens in both directions, to head width 0.7 mm or slightly less at the lower end to over 5.0 mm at the upper end, and the frequency distribution becomes more sharply peaked and strongly skewed to the larger size classes (see Figures 8-12 and 8-13).

A more physiological question immediately arises from the observed sociogenesis (colony ontogeny) of Atta: which is more important in determining the size-frequency distribution, the size of the colony or its age? In order to learn the answer, Wilson selected four colonies 3-4 years old and with about 10,000 workers and reduced the population of each to 236 workers, giving them a size-frequency distribution characteristic of natural young colonies of the same size collected in Costa Rica. The worker pupae produced at the end of the first brood cycle possessed a size-frequency distribution like that of small, young colonies rather than larger, older ones. Thus colony size and indirectly the amount of food produced are more important than age.

The Atta example is just an extreme case of what appears at least on the surface to be programmed colony demography among ant species. However, the physiological control mechanisms remain almost entirely unexplored. The “rejuvenation” effect in Atta cephalotes indicates that a feedback loop of some kind is involved, as opposed to an irreversible maturation of the size-frequency distribution; but its nature has not been investigated.

The ontogeny of the physical caste system has also been traced in the red imported fire ant Solenopsis invicta, as illustrated in Figure 8-14. In this species the first adult generation of workers consists entirely of “nanitics” or “minims,” with head widths about 0.50 mm. These individuals, as Porter and Tschinkel (1986) have demonstrated experimentally, are more effective as a group in rearing the second generation of adults, but less efficient energetically on an individual basis than the slightly larger “minor” workers. When the population grows by the addition of the second and later broods, it is to be expected on the basis of ergonomic selection at the colony level that the minims will be quickly replaced by minors and still larger workers. Just such a transition actually occurs, as shown in Figure 8-14. Subsequent field studies by Tschinkel (1988a) revealed that as the fire ant colonies grew, they changed from a monomorphic to a polymorphic worker force. The production of larger, major workers causes the overall size-frequency curve to become skewed in the manner just illustrated (Figure 8-9) for Atta. The skewed distributions are actually bimodal. They consist of two slightly overlapping normal distributions, a narrow one defined as the minor workers and a much broader one defined as the major workers. The “media” workers have no clear developmental definition and are simply individuals in the zone of overlap between the minor and major frequency curves. In full-sized colonies, the majors make up about 35 percent of the total worker force and 68 percent of its biomass.

It is evident that each ant species possesses a particular programmed ontogeny in the ratios of its subcastes (size-frequency distribution). In other words, the ratios are species-specific and hence genetically prescribed. Even differences encountered among colonies of the same species may have a partial genetic basis, as suggested by laboratory studies conducted on the North American myrmicine ant Pheidole dentata by Johnston and Wilson (1985). The worker force of colonies of Pheidole dentata, like those of other species of Pheidole, is divided into two discrete castes: small-headed minor workers, which conduct most of the quotidian tasks of the colony, and large-headed major workers, which are specialized for defense (see Table 8-1 and Figure 8-20). In natural populations of Pheidole dentata in northern Florida, majors make up between 5 and more than 50 percent of the worker force. The higher figures are rare and almost certainly pathological, and the great majority of colonies in the field and laboratory maintain a representation of majors between 5 and 15 percent. When Johnston and Wilson altered laboratory colonies displaying this latter range of variation to a uniform percentage of 5 percent and then allowed them to grow freely, the colonies changed to the original rank ordering and in most cases not far from their original subcaste percentages. Wheeler and Nijhout (1984) have shown that excess numbers of majors in Pheidole bicarinata ( vinelandica) colonies inhibit further production of majors in a manner that restores the species-characteristic ratio. The inhibition is evidently due to a pheromone that affects the endocrine system of presumptive soldiers. It seems likely that a similar mechanism operates in Pheidole dentata, and that the variation in ratios among colonies arises from genetic differences in major pheromone production, sensitivity to the pheromone, or both. The result is potentially important for an understanding of the evolution of caste ratios, since genetic variation in any trait is a prerequisite for its modification through time.

To summarize, there appears to be a species average or “norm” in caste ratios around which individual colonies vary due to both genetic and environmental differences. The environmental factors most important to the variance have only begun to be explored. For example, it is a common observation that majors of ant species live longer than minors, so that when the queen dies or ceases oviposition for long periods of time the major/minor ratio rises. It also increases above ordinary levels when the colony is starved or desiccated, because larger ants withstand such stress longer than their nestmates. The differential is commonly observed in the laboratory and has been documented explicitly in Camponotus and Formica by Kondoh (1977). In Veromessor pergandei, a seed-harvesting myrmicine living in the deserts of the southwestern United States, there is an annual cycle in average worker size. Smaller workers appear in the foraging force as a result of the wintertime “triple crunch” caused by a reduced seed crop, shorter suitable foraging time, and the added expense of production of reproductive forms (Rissing, 1987). In a reverse trend, major workers of the fire ant Solenopsis invicta become relatively most common in the late winter and early spring, probably due to their lower mortality under adverse conditions (Markin and Dillier, 1971). Such unusual fluctuations may well be just epiphenomena, that is, “noise” in the system of no adaptive significance to the colonies.

The evolution of physical castes
In ants the diversification of the female castes is based mostly on allometry. During larval development, the imaginal discs (patches of undifferentiated tissue destined to be transformed into adult organs at the pupal state) grow at different rates, a process that swiftly accelerates during pupal development (Brian, 1957a, 1979a; Schneirla et al., 1968). The principal result of differential growth rate in the imaginal discs is that various organs end up with different sizes relative to one another according to how large the individual is at the termination of the larval period. That is, the final adult size determines how much overall growth the various organs have attained. Thus, if the disc destined to transform into part of the head is growing faster than the disc destined to transform into part of the thorax, it will finish proportionately larger in an ant that attains a larger overall size. In short, big ants will have proportionally even bigger heads. If each disc grows exponentially, and if the disc growth rates do not change much in the course of development, the sizes of two parts will be related by a simple power law: log y = log b + a log x, or, equivalently, y = bxa where y and x are linear measures of the two body parts and a and b are fitted constants the values of which depend on the nature of the measurement taken. This simple relation is referred to as allometry or heterogonic growth. Its study in ants and other organisms was pioneered by Julian Huxley (1932) and has been reviewed extensively by Gould (1966). On a double logarithmic plot the curve is a straight line. Its slope a is determined by the rate of divergence of the two body parts with increasing total size and can be referred to as the allometric constant. If a is equal to unity, no divergence takes place with an overall increase in size; the growth is then referred to as isometric. The greater the departure of a from unity, the more striking the differential growth. Skellam, Brian, and Proctor (1959) found that in Myrmica rubra the imaginal discs of the wings and legs actually grow in this elementary fashion during development of adult queens and males. The organs predictably conform to the basic allometry equation in their final adult form.

It is possible to produce a wide array of deviations from elementary allometric growth by simply speeding or slowing the growth rates of different discs according to different time schedules. Further complexity can be introduced by making the rates dependent on the total size of the larva reached by certain ages. This last effect is crucial in the determination of the queen and worker castes in Myrmica, as documented by M. V. Brian. It also occurs during the differentiation of the worker caste of the Eciton army ants, as discovered by Tafuri (1955). These modifications are crucial for the discretization of physical castes within the adult instar of ants, a process that will now be examined in some detail.

Wilson (1953b) demonstrated that the allometry equation, or relatively simple modifications of it, can be applied almost universally to continuous variation in the hard parts of ants. The comparative study of allometry has proved fruitful in tracing the evolution of castes. Polymorphism, as this research has led us to understand it, embraces three variable characters in the adult females within colonies of any species: size variation, shape variation due to allometric growth at the time of adult formation, and the frequency distribution of different sized workers. A physical caste system (or polymorphism as it is also frequently called) is defined as growth occurring over a sufficient range to produce individuals of distinctly different sizes, body proportions, or both. Where polymorphism exists, it has always been found to be closely linked to division of labor.

By comparing a large fraction of the more than 10,000 living ant species, it has been possible to infer five major steps in the evolution of physical castes (Wilson, 1953b):

(1) Monomorphism. The workers of the normal mature colony display isometry (with a log-log curve slope of approximately 1.0) and very limited size variability. A plot of their size-frequency distribution is symmetrical and has only a single mode. In other words, the properties of variation are not basically different from those in a typical random collection for nonsocial insects. The worker castes of most ant genera and species are monomorphic. Also, within the majority of genera and higher taxonomic groups monomorphism is evidently the primitive state.

(2) Monophasic allometry. The relative growth is nonisometric, meaning that the allometric constant a is greater or less than unity to a subjectively noticeable degree. In the most elementary form of monophasic allometry, and hence of worker polymorphism generally, feeble nonisometric variation is displayed over a short span of size variation; this variation in turn is grouped around a single mode with possible skewing in the direction of the major caste. A more advanced stage, involving an increased variation in size together with an apparent bimodal size-frequency distribution, is exemplified by the fire ant Solenopsis invicta (Figure 8-15). The two modal groups are still overlapping, and hence the majors and minors are connected by intermediate-sized workers, or “medias.”

(3) Diphasic allometry. The allometric regression line, when plotted on a double logarithmic scale “breaks” and consists of two segments of different slopes that meet at an intermediate point. In the several species known to possess this condition, including the leafcutter ant Atta texana (Wilson, 1953), African driver ant [[Dorylus nigricans (Hollingsworth, 1960), and carpenter ant Camponotus sericeiventris'' (Busher et al., 1985), the size-frequency curve is bimodal. Also, the saddle between the two frequency modes falls just above the bend in the allometry curve.  Diphasic allometry permits the stabilization of the body form in the small caste while providing for the production of a markedly divergent major caste by means of a relatively small increase in size.  The lower segment of the relative growth curve is nearly isometric, so that individuals falling within a large segment of the size range are nearly uniform in structure; but the upper segment leading to the major caste is strongly nonisometric, with the result that a modest increase in size yields a new morphological type.

(4) Triphasic and tetraphasic allometry. The allometric line breaks at two points and consists of three straight segments. The two terminal segments, representing the minor and major castes respectively, deviate only slightly from isometry while the middle segment, encompassing the media caste, has a very steep slope. The effect of triphasic allometry is the stabilization of body proportions in the minor and major castes. An example from the weaver ant genus Oecophylla is presented in Figures 8-16 and 8-17. Baroni Urbani (1976b) has reported a case of tetraphasic allometry in the antennal length of the West African ant Camponotus maculatus. The curve resembles that of triphasic species except that in the largest size classes a high degree of allometry is resumed. The biological significance of this extreme pattern is wholly unknown.

(5) Complete dimorphism. Two morphologically very distinct size groups exist, separated by a gap in which no intermediates occur. Each class is either isometric or non-isometric, but the allometric regression curves are not aligned, a condition suggesting that complete dimorphism can arise directly from triphasic allometry. Examples include most queen-worker differences in ants. They also include minor-major divisions in no fewer than eight phylogenetically scattered genera: the myrmicines Acanthomyrmex, Oligomyrmex, Pheidole, and Zacryptocerus; the aneuretine Aneuretus; the dolichoderine Zatapinoma; and the formicines Camponotus (subgenera Colobopsis and Tanaemyrmex) and Pseudolasius (Plate 7).

By arranging species of ants along a gradient from what appear to be the simplest to the most advanced systems, worker castes can be found that display virtually every conceivable step in a transition from perfect monomorphism to a complete dimorphism (see Figure 8-18). Certain large taxonomic groups, such as the subfamilies Myrmicinae and Formicinae, embrace the entire evolutionary sequence within themselves. The evolution has thus occurred repeatedly within multiple phyletic lines in the ants and produced a remarkable degree of convergence between the lines.

Of the three principal qualities of polymorphism (size variation, allometry, and size frequency), the size-frequency distribution has been subject to the stricter and more notable convergence. When individual colonies of a given species show a slight increase in size variance, the frequency curve is almost always skewed toward the larger size classes. When the intracolonial size variance is still greater, the frequency curve is bimodal. In at least one species of army ant with extreme size variation, data published by Topoff (1971) and da Silva (1972) show the existence of three size modes. Three modes may occur in the extremely polymorphic myrmicine Pheidologeton diversus (Moffett, 1987b). Otherwise enlarged intracolonial size variation is typically associated with bimodality, with the large workers being less common. In weaver ants of the genus Oecophylla, the reverse is true: the majors are more common than the minors, and they fill most of the labor roles of the colony. This unusual form of polymorphism has existed since at least as far back as Miocene times, as shown by Wilson and Taylor (1964). These authors describe the extinct species Oecophylla leakeyi from a colony fragment that had been preserved intact, including even pupae and packets of larvae. With this extraordinary material, the only fossil insect colony found to date, it was possible to measure allometry and size frequency and compare these traits with those of the modern species.

The ways by which ant species create castes out of the adult instar are few. It is reasonable to ask how a colony limited to simple skewing and a maximum of two or three modes is able to produce castes in proportions that match the frequencies of numerous environmental contingencies. The answer appears to be that the evolutionary sequence unfolds within narrow physiological constraints. Species can only improve their situation to the extent of increasing the intracolonial size range and arranging something close to the optimum numbers of majors, minors, and medias. Physical caste systems, in a word, are coarse-tuned rather than fine-tuned (Oster and Wilson, 1978).

Temporal castes
The adult workers of almost all kinds of social insects change roles as they grow older, ordinarily progressing from nurse to forager. Each species has its own distinctive pattern of temporal polyethism, and in many the behavioral changes are accompanied by patterned shifts in the activity of exocrine glands. For example, as honeybee workers shift during a two-week period from a preoccupation with brood care and nest work to an emphasis on foraging, the activity of the hypopharyngeal and wax glands declines somewhat while that of the labial glands increases. For the purposes of ergonomic analysis it is useful to consider different age groups as constituting distinct temporal castes (Wilson, 1968). Just as a species may manipulate its own developmental biology in the course of evolution to produce optimum ratios of physical castes, it can adjust the program of role change during adult life to approach optimum ratios of temporal castes.

Two extreme alternatives are open to a species in the process of evolving temporal castes. These are represented in Figure 8-19. The aging period depicted is that which occurs from the moment of the worker's eclosion from the pupal skin to the moment of its death by senescence. The division of the life span into six periods in this imaginary example is arbitrary. The worker undergoes physiological change with age such that its responsiveness to various environmental stimuli changes. For example, suppose that T1 is the responsiveness to a misplaced egg: the curve indicates that when the worker is very young (age I) it is likely both to be in the vicinity of the egg and to react by picking the egg up and putting it on an egg pile. Its location and/or behavioral responsiveness change as it ages in such a way that its probability of response to the contingency drops off rapidly after ages I or II. Such age-dependent responsiveness has been abundantly documented in ants (Topoff et al., 1972; Cammaerts-Tricot, 1974b; Jaisson, 1975; Topoff and Mirenda, 1978; MacKay, 1983b).

Let us now consider the possibilities. In the upper diagram of Figure 8-20, labeled Model 1, the response curves to four contingencies (T1 through T4) are all out of phase. The curve of response to T1 (misplaced egg) is different from the curve of response to T2 (say, a hungry larva), and so on. As a result, the ensemble of age groups, represented on the right-hand side by the frequency distribution of workers in different age groups that attend to task T1, is different from that attending to T2, and so on. As the number of contingencies is increased, and their response curves are all made discordant, there will be one age-group ensemble for each task. Let us now define an age-group ensemble as a temporal caste. In the extreme case represented in Model 1 there is a caste for each task. However, the distinction between age-group ensembles will be blurred as more tasks are added. The overlap in the age-group frequency curves is so extensive that after ten or so contingencies are added, the system becomes effectively continuous. For this reason we suggest that such an arrangement be called a continuous caste system.

The approach to continuity in Model 1 is marked by complexity and subtlety. The evolving ant species can easily adjust the programming to individual worker responsiveness to attain discordance that in turn yields one caste specialized for each task. Thus, only a relatively elementary alteration in physiology is needed to produce a complex caste system.

Next consider the alternative option, depicted in the lower half of Figure 8-20. Here various of the response curves are concordant, or at least approximately so. As a result the same statistical ensemble of workers attends to more than one task. As the number of tasks increases, the number of castes does not keep pace; conceivably it could remain low, say corresponding to as few as 2 or 3 distinct ensembles. Thus, the species has chosen to operate with a discrete caste system--comprising relatively few, easily recognized age-group ensembles. The evolutionary process leading to such a system can be called “behavioral discretization” (Wilson, 1976c). It can operate through physiological alterations as potentially simple as those that yield continuous caste systems.

Few studies of temporal polyethism have been designed in a way that permits a consideration of the hypothesis of discretization. An analysis of the ant Pheidole dentata by Wilson (1976c) showed that the system has been discretized. Virtually all of the 26 behavioral acts recorded in the minor worker caste can be divided according to three age periods in which they are performed approximately in concert (see Figures 8-20 and 8-21). Data presented by Higashi (1974) on the Japanese wood ant Formica yessensis indicate that temporal castes have also been discretized in this species, but the behavioral categories followed through time were too few to be certain.

The observed discretization in Pheidole dentata appears to represent an adaptation that increases spatial efficiency. It is obviously more efficient for a particular ant grooming a larva to regurgitate to it as well. Similarly, a worker standing “guard” at the nest entrance can be expected to be especially prone to excavate soil when the entrance is buried. The other juxtapositions in the Pheidole dentata repertory make equal sense when the spatial arrangement of the colony as a whole is considered. The queen, eggs, first instar larvae (microlarvae), and pupae are typically clustered together and apart from the older larvae, although the positions are being constantly shifted, and pupae are often segregated for varying periods of time well away from other immature stages. Thus, the A-ensemble of workers can nicely care for all of these groups, moving from egg to pupa to queen with a minimum of travel. The mean free path of a patrolling worker is minimized by such versatility so that the least amounts of time and energy are consumed. It makes equal sense for A workers to assist the eclosion of adults from pupae, since pupae are already under their care.

It will be of interest to learn to what extent and by which patterns the temporal polyethism of other species of social insects has been discretized. Calabi et al. (1983) found the phenomenon lacking in the Asian Pheidole hortensis; in other words, the caste system is continuous. While it is too early to put the matter on a sound empirical basis, we suspect that the recognizable age ensembles--that is, temporal castes--will prove to be related functionally to nest architecture. Species with complex nest structure, which provide a wider array of housekeeping tasks, and the opportunity for a more precise distribution of brood stages into chambers with differing microclimates, can be expected to have more temporal castes than those with relatively simple structures. For example, leafcutter ants of the genus Atta, which construct elaborate chambers for the gardening of symbiotic fungi, are expected to possess a correspondingly complex system of temporal polyethism. The patterns of temporal polyethism may be related to the dietary specialization of the species and the external environment of its nests. An ant species that forages widely outside the nest for small particles of food, while simultaneously defending its nest entrances from frequent attacks by predators, is likely to have an unusually discrete polyethic division at the end of worker life. The C age ensemble of Pheidole dentata represents just such a case. Finally, the more dispersed the tasks for which temporal castes are specialized, the more likely is the labor to be discretized.

To the extent that temporal castes are discretized, all of the castes of a species can be counted. Pheidole dentata, for example, has five adult castes: three temporal stages of the minor worker, a major worker (which has only one temporal stage), and the queen. The male does not occupy any known labor role. The larva might provide gluconeogenesis or some other metabolic service and hence constitute a sixth caste, but this possibility remains uninvestigated in Pheidole. There is every reason to suspect that the modest temporal caste system of Pheidole dentata is typical for the majority of ant species.

More generally, the total characterization of an insect society appears more feasible than it did only a few years ago. It is likely that the number of physical and temporal castes will not exceed 10 in ants and 20 in termites. The categories of behavior recorded in individual physical castes of ants have so far ranged between 20 and 42, with a broad overlap of categories among castes and a total species repertory probably not much exceeding 50 (Oster and Wilson, 1978). Moreover, the smaller the size of the worker characterizing a species, the smaller the behavioral repertory of the species. The largest ants have a repertory size somewhat more than 1.5 times that of the smallest ants (Cole, 1985). The number of categories of signals used in communication, mostly chemical, is likely to fall between 10 and 20 (Wilson, 1971).

The study of the relation of age and behavior in ants has proceeded slowly because it is a technically difficult task. A few authors, including Otto (1958) and Lenoir (1979c), have simply marked and followed individual ants through portions of their lives. This brute-force procedure, while unassailably accurate, is also very tedious. Other investigators have sought short-cuts that allow the rapid estimation of the ages of masses of workers engaged in particular tasks. In other words, instead of piecing together many individual trajectories and from those data inferring the age bias among workers generally with reference to particular tasks, the reverse is accomplished with approximately the same results: the age bias among the bulk of the workers is ascertained, and from this information “typical” individual repertories are inferred. An age marker used most commonly is the darkening color of workers as they age. In Pheidole dentata, for example, newly eclosed adult minor workers are uniformly clear yellow; after 2 days the gaster darkens to a contrasting yellowish brown; when the ant reaches about a week in age the head also darkens to contrast with the middle of the body; and so on until after about 16 days the body is nearly uniformly dark brown (Wilson, 1976c). A closely similar series has been effectively employed for Myrmica by Weir (1958a,b) and by Cammaerts (1974b). In the Neotropical cryptobiotic ant Basiceros manni we recognized four stages in coloration and cumulative body deposits that were correlated with age and hence useful in the study of temporal division of labor (Wilson and Hölldobler, 1986).

Another kind of marker altogether, employed by Higashi (1974) in his studies of Formica yessensis, is the degree of mandible wear. The three apical teeth of the masticatory border are needle-sharp in newly eclosed workers and gradually wear down through the course of adult life.

A third widely used marker is the condition of the ovaries, which typically reach maximal development early in the adult stage and gradually atrophy as the ants age and undertake work away from the brood chambers (Figure 8-22). In Formica sanguinea, for example, yolk deposition commences about the tenth day of adult life and reaches a maximum between the 26th and 35th days (Billen, 1982a). Oogenesis by the young workers either produces trophic eggs that are fed to the queen and larvae, or viable eggs that almost always develop into males. The progression of ovarian development has been used in other studies of the division of labor in Formica by Otto (1958), Kneitz (1964b, 1969), Hohorst (1972), and Möglich and Hölldobler (1974), and in Oecophylla by Hölldobler (1983). These authors have all noted the close correspondence between the position of the ants in the nest and the state of their ovaries.

Each of these methods of age estimation is subject to considerable error due to individual differences among the workers and fluctuations in the colony environment. But if large samples of workers are taken, at least the main course of age polyethism can be charted. Its reliability increases when the colonies are maintained under controlled laboratory conditions and the marker calibrated by following marked workers through the early part of their lives.

The technical advance most needed in studies of temporal division of labor is a physiological or biochemical “clock,” one that changes steadily as the ant grows older and is subject to minimal error due to environmental covariance. One candidate is the density of particles in the cytoplasm of oenocytes (Buschinger, 1967; Ehrhardt, 1970). In Pheidole dentata it increases at a seemingly steady rate (Wilson, unpublished). Another is the accretion of daily rings in the endocuticle, a process that works well in the honeybee for up to 11 days and less reliably thereafter (Menzel et al., 1969). Endocuticular rings occur in the harvester ant Pogonomyrmex badius but have not been calibrated (Wilson, unpublished).

Case histories
Temporal polyethism, in other words division of labor by age, is far more prevalent in ants than caste polyethism (the more easily recognizable division of labor correlated with anatomical differences). Only a single species, Amblyopone pallipes, is known that lacks temporal polyethism altogether. All of the remaining studies to date display some variation on “typical” age polyethism, in which young workers devote themselves to brood care and other forms of labor inside the nest, while older workers tend to travel outside the nest for nest construction, defense, and foraging. Ants, as the German investigators have succinctly put it, pass from Innendienst (inside work) to Aussendienst (outside work). In contrast, only a minority of genera of ants contain one or more polymorphic species, in other words species in which the workers are divided into two or more physical subcastes. Of the 297 living genera recognized during the preparation of this book (Table 2-2), only 46 or 15 percent contain at least some polymorphic species. These taxa are listed in Table 8-2, along with the small number of genera whose caste systems are unknown. One of the remarkable features of the phylogenetic distribution revealed by this tabulation is the scarcity of physical worker subcastes within the large and relatively primitive subfamily Ponerinae. Only a single genus (Megaponera), out of 58 known living ponerine genera, or 2 percent of the total, is known to be polymorphic. According to Breed and Harrison (1988) another case might be the giant Neotropical ponerine Paraponera clavata, where worker variation appears to be mildly allometric and the size-frequency distribution of mature colonies is unimodal and skewed to the right. While the sizes of workers performing different tasks overlap widely, there is a statistical association between size and task performance. Large workers function more often as guards and foragers. One other ponerine genus, Aenictogiton, is of unknown status with respect to caste.

Most of the studies of caste and division of labor conducted to the present time are listed in Table 8-3. It is informative to compare this compilation with Table 2-2, which contains all of the living genera, and Table 8-2, which lists the genera known to display polymorphism; and then to note that almost all ant species probably have some form of division of labor, even if just based on age. It will then be obvious that while a large amount of information is now at our disposal, it applies to only a small fraction of genera and species. The exploration of caste and division of labor in ants is in an early stage, and many surprises surely lie ahead.

The best way to encompass existing knowledge of division of labor is to compare several grades of complexity across the entire range of the living ants. A well-studied example of weak polymorphism correlated with polyethism has been provided by Brandão (1978) for Formica perpilosa. This American montane species displays weak polymorphism of a kind widespread in ants. There is a modest size variation within the worker caste of individual colonies, accompanied by a slight but distinct allometry in which the bodies grow more robust and the heads broader relative to length with an overall increase in size. Medium-sized workers have the broadest repertories, covering all of the quotidian tasks of brood and queen care, nest work, and foraging. The smallest workers are very similar in overall behavior while performing slightly fewer acts. The largest workers, in contrast, constitute a true “major” caste specialized for liquid food storage. They engage in few other social acts. Overall, Formica perpilosa closely parallels caste and division of labor in the species of Proformica, a formicine genus found in dry habitats in Europe and Asia that also possesses weak polymorphism and a major subcaste specialized for food storage (Figure 8-23). The similarity is almost certainly due to convergent evolution.

In almost all species for which differences in size have been found to be correlated with division of labor, the size variation is also distinctly allometric. In addition to this first rule of caste evolution we encounter a second rule: monomorphic ant species rarely divide labor according to size. More precisely, the greater the combined amounts of size variation and allometry, the more pronounced the division of labor. Considerable size variation often occurs, but unless it is accompanied by allometry strong enough to be clear-cut by casual inspection, it is not correlated with marked role differences (Wilson, 1971; Herbers et al., 1985). No deviation is known from the first rule relating polymorphism to division of labor. However, one exception has been discovered to the second rule. Leptothorax longispinosus is a typically monomorphic species, yet the large workers forage more than the smaller ones, a foreshadowing of the division of labor characterizing the most simply allometric ant species (Herbers and Cunningham, 1983). In contrast, the monomorphic Leptothorax ambiguus, when subjected to the same form of analysis, evinced no sign of size bias in behavior. Herbers (1983) suggested that the difference between the two species might be due to the greater size variation that occurs within colonies of Leptothorax longispinosus. Another exception is the formicine honey ant Myrmecocystus mimicus, where Hölldobler found that larger workers are significantly more engaged in tournament behavior than smaller workers.

Successive grades in the early evolution of polymorphism and division of labor is nicely demonstrated among species of fire ants. The more primitive pattern of Solenopsis invicta is typical of almost all of the fire ant species, which comprise the subgenus Solenopsis of Solenopsis (as opposed to the thief ants, which comprise the subgenus Diplorhoptrum). The allometry of Solenopsis invicta is very slight (see Figures 8-15 and 8-24). The majors have heads that are only somewhat shorter, broader, and more quadrate with reference to the remainder of the body. The behavioral differences are also modest, since the majors perform the same tasks as the minors with the exception of caring for the eggs and young larvae. Workers in these larger size classes simply handle pieces of brood, prey, and soil particles that are correspondingly larger in size. Hence transport and nest excavation appear to be enhanced by the polymorphism, although that subjective impression has not yet been put to a quantitative test. The more important point is that Solenopsis geminata has added something entirely new. Allometry is steep, so that the larger medias and majors are grotesque creatures possessing massive heads and blunt, toothless mandibles. These two features together contribute to a substantial increase in the crushing power of the ants. Wilson (1978) was able to show that the largest workers were in fact specialized for milling seeds, the majors so much so that they have become restricted to the smallest behavioral repertory thus far recorded in the social insects--milling and self-grooming. Solenopsis geminata has undergone this striking revision in its caste system and division of labor as part of its trend toward granivory, which is the most extensive known among the fire ant species.

Fire ants illustrate a further principle in the division of labor, which can be summarized under the expression alloethism: the regular and disproportionate change in behavior in a particular category of behavior as a function of size of the workers (Wilson, 1978). Alloethism parallels allometry, or the regular and disproportionate change in one anatomical dimension relative to other dimensions as a function of worker size. In both species in which sufficiently detailed measurements have been taken, the fire ant Solenopsis geminata and the leafcutter Atta sexdens, the curves were found to possess steeper slopes than the corresponding allometric curves of the anatomical structures employed in the behavior (Wilson, 1978, 1980a). Put succinctly, alloethism amplifies allometry. Part of the fire ant pattern is illustrated in Figure 8-25.

Passing to the opposite extreme, let us next consider one of the most advanced grades of caste and division of labor discovered so far in ants, that of Pheidologeton diversus of southeast Asia. Colonies of this “marauder ant” contain hundreds of thousands of workers and conduct wide-ranging raids to collect insects and a variety of vegetable materials. The workers display only a moderate amount of allometry, which is largely confined to the proportions of the head. But their size variation is the greatest ever recorded within single ant colonies: a full tenfold range in head width and a 500-fold range in dry weight (see Figure 8-26). The size-frequency distribution of the workers is trimodal. Superimposed on this pattern are the following four size-related roles.

Minors (head widths less than 0.8 mm) conduct most of the tasks of the colony, including brood care, much of the foraging, construction of the nest and trail arcades, and defense.

Medias (head widths 1.0-2.6 mm) assist the minors in foraging and construction.

Majors (head widths greater than 2.6 mm) hoist obstructions and smooth the surface of the trails.

Repletes are medias and majors that remain in the nest and acquire food until their abdomens are swollen; they share this stored food with other members of the colony.

The medias and majors act as the colony bulldozers. They move obstructions on the trails too large for their small nestmates to handle, pack the soil with their massive heads, and chew through the tougher fibers of fruit and the more massive appendages of captured prey. In addition to the physical castes, Moffett has distinguished two temporal castes in the small workers that conform to the usual pattern in ants. That is, the youngest workers associate more with the brood, while older workers presumably expand their repertory to fill the entire range of tasks. In addition, exceptionally dark-colored, hence old or wounded workers are disproportionately represented among the workers guarding the trails. The caste system of Pheidologeton diversus, when combined with its large colony size and ability to field a large army of workers, has enabled it to utilize an extraordinary wide variety of foods.

Precisely the opposite dietary adaptation has been achieved by the equally complex system of the leafcutter ants in the genus Atta, illustrated in Figure 8-27. Like Pheidologeton, Atta generates a broad array of physical types by combining extreme size variation with moderate allometry. In Atta sexdens, the head width varies eightfold and the dry weight 200-fold from the smallest minors to the huge majors; the polymorphism thus runs a close second to Pheidologeton diversus. However, the Atta caste diversity is not directed at broadening the diet of the ants, as in Pheidologeton, but at narrowing it severely. Colonies of Atta subsist entirely on the sap of plants and a symbiotic fungus they grow on fragments of vegetation. Atta and its sister genus Acromyrmex are unique in the Animal Kingdom in their ability to utilize freshly cut leaves and other vegetation for the rearing of fungus. Their unusual caste system has made the adaptation possible.

The fungus-growing ants of the ant tribe Attini, to which Atta belongs, are of unusual interest in biology because (to cite a familiar metaphor) they alone among the ants have achieved the transition from a hunter-gatherer to an agricultural existence. But this major shift did not require an elaborate caste system. The great majority of attine genera and species are monomorphic, including the presumably most primitive forms belonging to Cyphomyrmex. The complex caste system and division of labor of Atta represent a much narrower, more idiosyncratic adaptation to the collecting of fresh vegetation as a novel form of fungal substrate. Most of the monomorphic attines such as Cyphomyrmex utilize decaying vegetation, insect remains, or insect excrement, all of which are materials ready-made for fungal growth. Fresh leaves and petals, in contrast, require a whole series of special operations before they can be converted into substrate. They must first be cut down, then chopped into fine pieces, next chewed and treated with enzymes, and finally incorporated into the garden comb. Beyond the harvesting process, the fungus must also be provided constant care after it sprouts on the substratum.

The Atta workers organize the gardening operation in the form of an assembly line, which is illustrated in Figures 8-28 and 8-29 (see also Plates 9 to 11). Tough vegetation can be cut only by workers with head widths of 1.6 mm or greater. The most frequent size group among foragers consists of workers with head widths 2.0 to 2.2 mm. At the opposite end of the line, the care of the delicate fungal hyphae requires very small workers, and this task is filled within the nests by workers with head widths predominantly 0.8 mm. The intervening steps in gardening are conducted by workers of graded intermediate size. After the foraging medias drop the pieces of vegetation onto the floor of a nest chamber, they are picked up by workers of a slightly smaller size, who clip them into fragments about one to two millimeters across. Within minutes, still smaller ants take over, crush and mold the fragments into moist pellets and carefully insert them into a mass of similar material. The resulting “comb” ranges in size from a clenched fist to a human head and is riddled with channels. Resembling a gray cleaning sponge, it is light and fluffy and crumbles under slight pressure. On its surface the fungus spreads out like a frost, sinking its hyphae into the leaf paste to digest the abundant cellulose and proteins held there in partial solution.

The remainder of the gardening cycle proceeds. Worker ants even smaller than those just described pluck loose strands of the fungus from places of dense growth and plant them onto the newly constructed surfaces. Finally, the very smallest--and most abundant--workers patrol the beds of fungal strands, delicately probing them with their antennae, licking their surfaces clean and plucking out the spores and hyphae of alien species of mold. These colony dwarfs are able to travel through the narrowest channels deep within the garden masses. From time to time they pull loose tufts of fungal strands resembling miniature stalked cabbage heads and carry them out to feed their larger nestmates.

Although the assembly line of fungal cultivation is the core of caste and division of labor in the leafcutter colony, it is far from the entire story. The defense of the colony is also organized to some extent according to size. All of the size groups attack intruders, but in addition there is a true soldier caste. Among the scurrying ants can be seen a few extremely large majors. Their sharp mandibles are powered by massive adductor muscles that fill the swollen, five-millimeter-wide head capsules. Working like miniature wire clippers, these specialists chop enemy insects into pieces and easily slice through the skin of vertebrate intruders. The giants are especially adept at repelling large enemies. When entomologists digging into a nest grow careless, their hands become nicked all over as if pulled through a thorn bush.

When brood care, nest construction, and other tasks are added, the ants perform a total of 22 such social functions. The workers of Atta sexdens fall into four size groups defined by the clusters of these tasks on which they specialize, together with size. These four physical castes can be characterized respectively as gardeners-nurses, within-nest generalists, foragers-excavators, and defenders. As shown in Figure 8-30, this analysis starts with the drawing of polyethism curves, or size-frequency curves of the workers engaged in each of the 22 tasks in turn. The polyethism curves are then clustered to define the roles. Three of the four physical castes recognized in this fashion have also been shown to pass through changes of behavior with aging, allowing the discrimination of two temporal castes in each. The total number of castes recognizable in Atta sexdens, physical plus temporal, is therefore seven (Wilson, 1980a).

The absolute commitment of the Atta worker caste to the social life of the species is reflected by its intricate polyethism. It is also underscored by the distinctive patterns of size-related variation in the exocrine glands and body spines. In every instance where the function of an organ is known, the organ proves to be maximally developed in the size classes that specialize on the tasks served by the organ (see Figure 8-31). Hence the pronotal spines, taken as representative of armament over the entire body, are proportionately longest in the size classes (with head widths 1.6-2.6 mm) that spend the most time foraging outside the nest and hence are exposed most frequently to danger from predators and competitor ants. The same size classes do most of the trail-laying, and sure enough, they have the proportionately largest poison glands, the source of the trail pheromone. The postpharyngeal gland is the source of larval food in species of ants that have been studied in this respect, and it turns out that in Atta sexdens the postpharyngeal gland is largest in the smallest size class, with head widths 0.6 to 1.2 mm; these workers are the ones that feed larvae by regurgitation. The mandibular gland is known to produce the alarm substances citral and 5-methyl-3-heptanone in species of Atta, including, at least in the case of the methylheptanone, Atta sexdens (Blum et al., 1968a). As expected, this paired organ is proportionately most massive in the largest size classes of Atta sexdens, which are specialized for colony defense. The consistency of correlation suggests that proportionate size alone might be used in the future as a first clue concerning the roles of previously unstudied or experimentally less tractable organs. For example, it can be predicted that secretions of the labial and hypopharyngeal glands in Atta sexdens function in brood care or fungus gardening, while those of the Dufour's gland are used either in defense or alarm communication. The technique can also be used to infer the roles of sensory organs. Jaisson (1972c), for example, reports that the sensilla ampulacea and sensilla coeloconica of the antennae vary according to worker size in Atta laevigata. This important aspect of sensory physiology awaits closer study.

Although caste and division of labor in Atta are very complex in comparison with other ant systems, they are still derived from surprisingly elementary processes of increased size variation, allometry, and alloethism. This important point is made graphic by Figure 8-32, in which the properties of the true Atta sexdens system are compared with those of an imaginary, more complex arrangement that could be generated by only slightly more elaborate rules. Ant species in general and Atta sexdens in particular have thus been remarkably restrained in the elaboration of their castes. They have relied on a single rule of deformation to create physical castes, which translates into a single allometric curve for any pair of specified dimensions such as head width versus pronotal width or, as illustrated in Figure 8-31, exocrine gland size versus pronotal width. The Atta could have created a more complex and precise array of castes by programming an early divergence of developing larval lines along with differing allometry among those lines at pupation, producing the effect illustrated in the upper diagram of Figure 8-32. But neither the Atta nor to our knowledge any of the many kinds of polymorphic ants have ever done so.

Behavior follows similarly elementary rules. The polyethism curves presented in Figure 8-30 are all of relatively simple form. They are unimodal and show only limited amounts of skewing. These properties suggest the existence of underlying alloethism functions of fundamental simplicity: for each behavior, a monotonic rise of responsiveness to a peak along the size range is followed by a monotonic decline.

To summarize, even though Atta sexdens possesses one of the most complicated caste systems found in the ants, it has not evolved anywhere close to the conceivable (and we believe evolutionarily attainable) limit. There are far more tasks than castes: by the first crude estimate seven castes cover a total of between 20 and 30 tasks. Furthermore, one can discern another important phenomenon in Atta sexdens that constrains the elaboration of castes: polyethism has evolved further than polymorphism.  As we showed in the case of the fire ant [[Solenopsis geminata, the alloethic curves rise and descend more steeply than the size-frequency distributions and they are generally steeper than the allometric curves drawn from any selected pair of physical measurements.  Consequently, ensembles specialized on particular tasks are more differentiated by behavior than by age or anatomy.  In the course of evolution, Atta'' created its division of labor primarily by greatly expanding the size variation of the workers, while adding a moderate amount of allometry and a relatively much greater amount of alloethism.

Specialization by majors: defense
It is remarkable that the anatomically more deviant major workers of various ant species have arisen in evolution solely as specialists for one or the other of three primary tasks: defense, milling (chewing and comminution) of seeds, and food storage (by the extreme distension of the crop to create repletes). In cases of advanced polymorphism, especially complete dimorphism where intermediates have dropped out and the majors and minor workers have begun to evolve allometric patterns of their own, the greatest modifications in the major caste are found in the head and mandibles. The majors often look like members of an entirely different species.

The dominant role of majors, first noted by Westwood (1838) and since repeatedly confirmed, is defense of the nest and food. The majors, or “soldiers” as they are properly designated, are adapted to one or the other four basic fighting techniques: shearing, piercing, blocking and bouncing. Each will now be briefly characterized.

(1) Shearing. The mandibles are large but otherwise typical, the head is massive and cordate, and the soldiers are adept at cutting the integument and clipping off the appendages of enemy arthropods. Examples are found in Pheidole (Figure 8-3), Pheidologeton (Figure 8-26), Atta (Figure 8-28), Oligomyrmex, Aneuretus, Zatapinoma, Camponotus (Figure 8-18), and a few other genera of diverse relationships. Wheeler, in his essay “The physiognomy of insects” (1927), pointed out that the peculiar head shape of this form of soldier is simply due to an enlargement of the adductor muscles of the mandibles, which imparts greater cutting or crushing power to the mandibles.

(2) Piercing. The mandibles are pointed and sickle-shaped or hook-shaped. Soldiers of the most highly evolved army ants (Dorylus and Eciton) often line up along the flanks of the moving columns, the heads facing outward and mandibles gaping. An identical guard posture is assumed around nest entrances by the saber-jawed soldiers of the formicine Cataglyphis bombycina in the Sahara Desert (Délye, 1957). These formidable looking individuals rush at any moving object when the nest is disturbed. They seldom engage in other tasks. Contrary to an earlier suggestion by Felix Santschi, Délye found that the Cataglyphis soldiers are not well suited for carting particles during the excavation of nests.