Solitary versus Social Life

Many works treat aspects of behavior of diverse kinds of bees. Specialized papers are cited throughout this book; some more general treatments are the books by Friese (1923), with its interesting colored plates of nests of European bees; Iwata (1976), with its review of previous work on the behavior of bees and other Hymenoptera; and O'Toole and Raw (1991), which offers readable accounts and fine illustrations of bees worldwide. A major aspect of behavior involves intraspecific interactions, i.e., social behavior in a broad sense. Courtship and mating are treated briefly in Section 4. Here we consider colonial behavior—its origin as well as its loss.

Some female bees are solitary; others live in colonies. A solitary bee constructs her own nest and provides food for her offspring; she has no help from other bees and usually dies or leaves before the maturation of her offspring. Sometimes such a female feeds and cares for her offspring rather than merely storing food for them; such a relationship is called subsocial.

A colony consists of two or more adult females, irrespective of their social relationships, living in a single nest. Frequently the females constituting a colony can be divided into (1) one to many workers, which do most or all of the foraging, brood care, guarding, etc., and are often unmated; and (2) one queen, who does most or all of the egg laying and is usually mated. The queen is often, and in some species always, larger than her workers, but sometimes the difference is only in mean size. In some social halictines, the largest females have extraordinarily large heads, often with toothed genae or other cephalic modifications probably resulting from allometry.

For many people, bees are thought of as honey-producing social insects living in perennial colonies, each of which consists of a queen and her many daughter workers. This is indeed the way oflife for the honey bees (genus Apis) and the stingless honey bees (Trigona, Melipona, etc.) of the tropics. Queens and workers in these cases are morphologically very different, and the queen is unable to live alone (e.g., she never forages); nor do workers alone form viable colonies (they cannot mate and therefore cannot produce female offspring). These are the highly eu-social bees. Such bees always live in colonies, and new colonies are established socially, by groups or swarms. Only two tribes, the Apini and the Meliponini (family Apidae), consist of such bees.

Most bumble bees (Bombini) and many sweat bees (Halictinae) and carpenter bees and their relatives (Xylo-copinae) may live in small colonies, mostly started by single females working as solitary individuals performing all necessary functions of nest construction, foraging, provisioning cells or feeding larvae progressively, and laying eggs. Later, on the emergence of daughters, colonial life may arise, including division of labor between the nest foundress (queen) and workers. These are primitively eu-social colonies. Queens and workers are essentially alike morphologically, although often differing in size; they differ more distinctly in physiology and behavior. Such colonies usually break down with production of repro-

ductives; thus the colonies are obligately temporary rather than potentially permanent like those ofhighly eu-social bees.

Since in primitively eusocial bees the individual that becomes the queen cannot always be recogized until she has workers, the word gyne has been introduced for both potential queens and functional queens. The word is most frequently used for females that will or may become queens (Michener, 1974a), but have not yet done so. Thus it is proper to say that a gyne establishes her nest by herself in the spring, and becomes a queen when the colony develops.

Both permanent honey bee colonies and temporary bumble bee or halictine colonies are called eusocial, meaning that they have division of labor (egg-layer vs. foragers) among cooperating adult females of two generations, mothers and daughters. Such a definition is adequate for most bees; there is currently much discussion of modifying the definition of "eusocial" and relevant terms to make them useful across the board for all groups of social animals or, alternatively, eliminating them in favor of a system of terms that addresses the social levels among diverse animal species as well as the variability within species (see Crespi and Yanaga, 1995; Gadagkar, 1995; Sherman et al., 1995; Costa and Fitzgerald, 1996; and Wcislo, 1997a).

Not all bees that live in colonies are eusocial. Sometimes a small colony consists of females of the same generation, probably often sisters, that show division of labor, with a principal egg-layer or queen and one or more principal foragers or workers. Such colonies, called semi-social, may not be worth distinguishing from primitively eusocial colonies. As noted below, they often arise when the queen of a primitively eusocial colony dies and her daughters carry on, one of them commonly mating and becoming the principal egg-layer or replacement queen.

Some bee colonies lack division of labor or castes: all colony members behave similarly. Some such colonies are communal; two or more females use the same nest, but each makes and provisions her own cells and lays an egg in each of them. In most or all species that have communal colonies, other individuals in the same populations nest alone, and are truly solitary. Thus colonial life is facultative. A possible precursor of communal behavior arises when a nest burrow, abandoned by its original occupant, is then occupied by another bee of the same species (Neff and Rozen, 1995). Such behavior is rarely reported, because without marked bees, one does not know of it. A condition that appears to promote communal behavior is very hard soil or other substrate, because it is much easier to join other bees in a preexisting nest than to excavate a new nest starting at the surface (Michener and Rettenmeyer, 1956; Bennett and Breed, 1985).

A little-used additional term is quasisocial. It applies to the relatively rare case in which a few females occupying a nest cooperate in building and provisioning cells, but different individuals (as opposed to a single queen)

lay eggs in cells as they are completed. That is, all the females have functional ovaries, mate, and can lay eggs. This may not be the terminal or most developed social state for any species of bees, but at times some colonies exhibit this condition.

When one opens a nest containing a small colony of bees, it is often impossible to recognize the relationships among the adult female inhabitants. The colony might be communal, quasisocial, or semisocial. Only observations and dissections will clarify the situation. Such colonies can be called parasocial, a noncommittal umbrella term used for a colony whose members are of a single generation and interact in any of the three ways indicated or in some as yet unrecognized way. At first, primitively euso-cial colonies may look like parasocial colonies, but one individual, the queen (mother), is older, more worn, and sometimes larger than the others, which are workers (daughters). The queen commonly has enlarged ovaries and sperm cells in the spermatheca; workers usually do not.

Because many species pass through ontogenetic stages of sociality or are extremely variable in this regard, terms like "eusocial" should be applied to colonies, not species, except when dealing with permanently highly social forms like Apis and the Meliponini. For example, a nest may contain a single female, a gyne who has provided for and is protecting her immature progeny in a subsocial relationship. After emergence of the first adult workers, however, the nest contains a eusocial colony. There are species of Halictinae that have eusocial colonies in warmer climates but are solitary in cold climates (Eickwort et al., 1996). A single population may consist of some individuals functioning like solitary bees while others are eusocial, as observed in a New York population of Halictus rubicundus (Christ) (Yanega, 1988, 1989). In most Allodapini and some Ceratinini (in the Xylo-copinae), although nests harboring colonies of two or more cooperating adult females exist, most nests contain a lone adult, rearing her young subsocially without benefit of a worker or other adult associate (Michener, 1990b). In the nests containing two or more adults, one is often the principal layer, thus a queen, and the others (or one of them), principal foragers and often unmated, and thus workers. Later, if the queen dies, one of the workers may become a queen; the result is a semisocial colony of sisters. But if several or all of the sisters become reproductive, the result is a quasisocial colony. Of course there are sometimes intergradations or mixtures. In such bees eusocial and other social relationships have arisen even though most individuals of the species never experience cooperative behavior among adult females.

The terminology summarized above is not always helpful; I introduce it here because some of the terms are often found in the literature and are used later in this book. A case in which the terminology ("communal," "semisocial," etc.) is not useful is found in the autumnal colonies of Exoneura bicolor Smith in Australia (Melna and Schwarz, 1994). The bees in such colonies can be divided into four classes, according to their activities. Yet there is no reproductive activity at this time; thus there is no queenlike or workerlike division of labor, but rather division along other lines. It may be that in the Allodap-

ini, whenever two or more adults nest together, some sort of division of labor ensues.

Many kinds of bees that nest in the ground construct numerous nests in limited areas; a patch of earth, a path, or an earthen bank may be peppered with their holes (Fig. 5-1). Such groupings of individual nests are called aggregations. Each burrow may be made and inhabited by one female or may contain some sort of small colony (Fig. 52). Some aggregations doubtless result from the availability of local patches of suitable soil, but often the bees choose to aggregate in only part of an extensive area that appears uniform. Sometimes, gregarious behavior seems to be a response to the presence of other bees or bee nests—thus a social phenomenon; see Michener (1974a). In other cases bees may be returning to the site of their own emergence or "birth." In the literature, aggregations are sometimes called "colonies." I think it is best to avoid this usage and to limit the word "colony" as indicated above.

The above is a brief account of a large topic, the social diversity found among bees. Additional information and sources can be found in Michener, 1974a, 1985b, 1990c, d. The great abundance of the highly social forms (honey bees, stingless bees) almost wherever they occur suggests that such sociality itself is an enormous advantage in the presumed competition with other bees. The great body of literature on the theory of eusocial behavior of insects mostly addresses in one way or another the problem of how it is possible for attributes like those of workers to evolve and be passed on from generation to generation, even though they decrease the probability of their bearer's leaving progeny. Briefly expressed, an individual's overall

Figure 5-1. Part of an aggregation of nests made by females of Trigonopedia oligotricha Moure. The holes were in a vertical bank near Rio de Janeiro, Brazil. From Michener and Lange, 1958c.
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Figure 5-2. Part of an aggregation of nests, each containing a eusocial colony of Halictus hesperus Smith, in Panama. The tumuli at the nest entrances make the site conspicuous. Photo by R. W. Brooks.

or inclusive fitness consists of (1) its direct fitness (its number of offspring and their contributions to subsequent generations; i.e., the fitness resulting from its own actions) and (2) an indirect effect resulting from its influence on the fitness of other individuals, weighted by its coefficient of relatedness to those individuals. Association of two individuals (x and y) should be favored by selection if x experiences no decrease in direct individual fitness that is not more than offset by an increased fitness received indirectly through the actions ofy. A worker bee, a daughter of a queen, is closely related to the queen; and the queen's other offspring are genetically similar to the worker. The worker's individual fitness is zero if she produces no offspring, but the proliferation of genes like those of the worker is promoted by the benefits for the queen and her colony provided by the worker. And because of the haplodiploid sex-determination system in Hymenoptera, relationships between full sisters are closer than are mother-daughter relationships. Therefore a group of sisters (workers) may increase their inclusive fitness more by caring for their sisters, younger offspring of their mother, than by producing their own offspring. They thus gain in fitness by staying with their mother (the queen). This situation, resulting from haplodiploidy, is presumably a partial explanation of the frequency of evolution of eusociality in the Hymenoptera, compared to its rarity in other animals.

One must also observe, however, that associates in colonies are not always closely enough related to satisfy such thinking, perhaps because of multiple mating by gy-nes, or the formation of colonies by not necessarily related individuals from the general population. There must also be, then, additional factors that can promote colony formation. These are ecological factors, namely, mutualism, including such behavior as defense against natural enemies (Lin and Michener, 1972), cooperative nest construction, and continued protection of a mother's young offspring in spite of her death. Although behavioral studies (e.g., nest switching among communal nests) long ago suggested low coefficients of relationship among communal colony members, DNA fingerprinting makes such investigations easier and far more decisive. A recent study, containing relevant references to earlier works, is that of Macrotera texana (Cresson) (Panurginae). It showed that in this commonly communal bee, relationships among colony members did not differ significantly from relationships among non-nestmates of the same population (Danforth, Neff, and Barretto-Ko, 1996).

The terms explained above for various social levels among bees were often thought of as reflecting a possible evolutionary sequence of species from solitary to eusocial. Thus a parasocial sequence consisted of solitary, communal, semisocial, and eusocial species and a subsocial sequence consisted of solitary, subsocial, and eusocial species. It now seems probable that eusociality has often arisen directly from solitary antecedents (Michener, 1985b). Communal behavior is an alternative way of living together that does not usually lead to eusociality, according to Danforth, Neff, and Barretto-Ko (1996).

One caution is important in considering these matters: in haplodiploid insects like the Hymenoptera, the conditions for the origin of social behavior may differ from the requirements for the survival, maintenance, and subsequent evolution of social behavior. The expression "the evolution of social behavior" can include both, a fact that in the past has resulted in substantial confusion.

A review of the literature on the origins and evolution of sociality is beyond the scope of this book. Starr (1979) and Andersson (1984) provided comprehensive reviews. Radchenko (1993) gave a useful list of the many publications on social behavior in the Halictinae, a group that is particularly critical for evaluating theories about social behavior because of the many origins and losses of euso-ciality that have occurred in this subfamily. Packer (1991) and Richards (1994) have examined the distribution of sociality on phylogenies of the halictines Lasioglossum (Evylaeus) and Halictus, respectively; see also Packer, 1997. Valuable recent papers on the social evolution of the augochlorine bee Augochlorella are those of U. G. Mueller (see Mueller, 1997). See also Wcislo and Gonzalez (2006).

Clearly, there is no ready answer to the often-asked question about the number of times that eusocial behavior has arisen in the course of bee evolution. If each population of many species can become either more or less social, ranging from always social at the season of maximal activity to never social, the number of origins becomes both unknowable and useless. It is the wrong question. Nonetheless, there are interesting phylogenetic aspects to the occurrence of eusociality. So far as I know, it is never found in most bee families, although communal behavior occurs at least occasionally in nearly all families. Evidently, the Halictidae (especially Halictinae) and the Xylocopinae (especially Allodapini) have special potentials for repeated evolution of eusocial behavior. But even within these groups, there is much variation in the frequency of eusocial colonies, as shown by the efforts (cited above) to plot sociality on phylogenies. An interesting example is in the halictine subgenus Lasioglossum s. str., most species of which are consistently solitary. Packer (1997), however, cites meager evidence that one species, L. aegyptellum(Strand), can be eusocial; if this interpretation is correct, eusociality in this species is believed to be a recent evolutionary development in a clade of basically solitary species. Phylogenetic analysis of certain Lasioglossum species by Danforth, Conway, and Ji (2003), based on nucleotide sequences of three genes (one mitochondrial, two nuclear), indicated a single origin of eusociality within the genus but six reversals, i.e., changes from eusocial to solitary. Thus losses of sociality may be much more frequent than origins of sociality.

Questions about the origins of eusocial behavior are usually asked with the assumption that evolution is from solitary to eusocial. Certainly among bees as a whole this has been true. But there may be many cases in which species of primitively eusocial clades like those of many of the Halictinae have evolved to become solitary. Packer (1997) and his associates, when plotting behavior on cladograms, have discovered diverse cases of this kind; see also Wcislo and Danforth (1997).

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