Development and Reproduction

As in all insects that undergo complete metamorphosis, each bee passes through egg, larval, pupal, and adult stages (Fig. 4-1).

The haplodiploid system of sex determination has had a major influence on the evolution of the Hymenoptera. As in most Hymenoptera, eggs of bees that have been fertilized develop into females; those that are unfertilized develop into males. Sex is controlled by alleles at one or a few loci; heterozygosity at the sex-determining locus (or loci) produces females. Development without fertilization, i.e., with the haploid number of chromosomes, produces males, since heterozygosity is impossible. Inbreeding results in some diploid eggs that are homozygous at the sex-determining loci; diploid males are thus produced. Such males are ordinarily reproductively useless, for they tend to be short-lived (those of Apis are killed as larvae) and to have few sperm cells; moreover, they may produce triploid offspring that have no reproductive potential. Thus for practical purposes the sex-determining mechanism is haplodiploid.

When she mates, a female stores sperm cells in her spermatheca; she usually receives a lifetime supply. She can then control the sex of each egg by liberating or not liberating sperm cells from the spermatheca as the egg passes through the oviduct.

Because of this arrangement, the female (of species whose females are larger than males) is able to place female-producing eggs in large cells with more provisions, male-producing eggs in small cells. In Apis, the males of which are larger than the workers, male-producing cells are larger than worker-producing cells and presumably it is the cell size that stimulates the queen to fertilize or not to fertilize each egg. Moreover, among bees that construct cells in series in burrows, the female can place male-producing eggs in cells near the entrance, from which the resultant adults can escape without disturbing the slower-developing females. The number of eggs laid during her lifetime by a female bee varies from eight or fewer for some solitary species to more than a million for queens of some highly social species. Females of solitary bees give care and attention to their few offspring by nest-site selection, nest construction, brood-cell construction and provisioning, and determination of the appropriate sex of the individual offspring. Of course, it is such atttention to the well-being of offspring that makes possible the low reproductive potential of many solitary bees.

The eggs of nearly all bees are elongate and gently curved, whitish with a soft, membranous chorion ("shell") (Fig. 4-1a), usually laid on (or rarely, as in Lithur-gus, within) the food mass provided for larval consumption. In bees that feed the larvae progressively (Apis, Bom-bus, and most Allodapini), however, the eggs are laid with little or no associated food. Eggs are commonly of moderate size, but are much smaller in highly social bees, which lay many eggs per unit time, and in Allodapula (Al-lodapini), which lays eggs in batches, thus several eggs at about the same time. Eggs are also small in many clep-toparasitic bees (see Sec. 8) that hide their eggs in the brood cells of their hosts, often inserted into the walls of the cells; such eggs are often quite specialized in shape and may have an operculum through which the larva emerges (see Sec. 8). Conversely, eggs are very large in some subsocial or primitively eusocial bees like Braunsapis (Allo-dapini) and Xylocopa (Xylocopini). Indeed, the largest of all insect eggs are probably those of large species of Xylocopa, which may attain a length of 16.5 mm, about half the length of the bee's body. Iwata and Sakagami (1966) gave a comprehensive account of bee egg size relative to body size.

The late-embryonic development and hatching of eggs

Desarrollo Abeja
Figure 4-1. Stages in the life cycle of a leafcutter bee, Megachile brevisCresson. a, Egg; b-d, First stage, half-grown, and mature larvae; e, Pupa; f, Adult. From Michener, 1953b.

has proved to be variable among bees and probably relevant to bee phylogeny. Torchio, in various papers (e.g., 1986), has studied eggs of several different bee taxa immersed in paraffin oil to render the chorion transparent. Before hatching, the embryo rotates on its long axis, either 90° or 180°. In some bees (e.g., Nomadinae) the chorion at hatching is dissolved around the spiracles, then lengthwise between the spiracles; eventually, most of the chorion disappears. In others the chorion is split but otherwise remains intact.

Larvae ofbees are soft, whitish, legless grubs (Fig. 4-1b-d). In mass-provisioning bees, larvae typically lie on the upper surface of the food mass and eat what is below and in front of them, until the food is gone. They commonly grow rapidly, molting about four times as they do so. The shed skins are so insubstantial and hard to observe that for the great majority of bees the number of molts is uncertain. For the honey bee (Apis) there are five larval instars (four molts before molting into the pupal stage); and five is probably the most common number in published reports such as that of Lucas de Olivera (1960) for Melipona.. In some bees, e.g., most nonparasitic Apinae other than the corbiculate tribes (i.e., in the old An-thophoridae), the first stage remains largely within the chorion, leaving only four subsequent stages (Rozen, 1991b); such development is also prevalent in the Mega-chilidae. In the same population of Megachile rotundata (Fabricius) studied by Whitfield, Richards, and Kveder (1987), some individuals had four instars and others five. The first to third instars were almost alike in size in the two groups, but the terminal fourth instar was intermediate in size between the last two instars of five-stage larvae.

Markedly different young larvae are found in most cuckoo bees, i.e., cleptoparasitic bees. These are bees whose larvae feed on food stored for others; details are presented in Section 8. Young larvae of many such parasites have large sclerotized heads and long, curved, pointed jaws with which they kill the egg or larva of the host (Figs. 84-5, 91-6, 105-3). They then feed on the stored food and, after molting, attain the usual grublike form of bee larvae.

Other atypical larvae are those of allodapine bees, which live in a common space, rather than as a single larva per cell, and are mostly fed progressively. Especially in the last instar, they have diverse projections, tubercles, large hairs, and sometimes long antennae that probably serve for sensing the movements of one another and of adults, and obviously function for holding masses of food and retaining the larval positions in often vertical nest burrows (Fig. 90-6). Many of the projections are partly retracted when the insect is quiet, but when touched with a probe or otherwise disturbed, they are everted, probably by blood pressure.

It has been traditional to illustrate accounts of bee larvae (unfortunately, this is largely not true for adults). The works of Grandi (culminating in Grandi, 1961), Mich-ener (1953a), McGinley (1981), and numerous papers by Rozen provide drawings ofmature larvae of many species. Various other authors have illustrated one or a few larvae each. Comments on larval structures appear as needed later in the phylogenetic and systematic parts of this book. Unless otherwise specified, such statements always concern mature larvae or prepupae. Accounts of larvae are listed in a very useful catalogue by McGinley (1989), organized by family, subfamily, and tribe. It is therefore unnecessary except for particular cases to cite references to papers on larvae in this book, and such citations are mostly omitted to save space.

As in other aculeate Hymenoptera, the young larvae of bees have no connection between the midgut and the hindgut, so cannot defecate. This arrangement probably arose in internal parasitoid ancestors of aculeate Hy-menoptera, which would have killed their hosts prematurely if they had defecated into the host's body cavity. In some bees defecation does not begin until about the time that the food is gone; in others, probably as a derived condition, feces begin to be voided well before the food supply is exhausted. After defecation is complete the larva is smaller and often assumes either a straighter or a more curled form than earlier and becomes firmer; its skin is less delicate, and any projections or lobes it may have are commonly more conspicuous (Fig. 4-2). This last part of the last larval stage is called the prepupa or defecated larva; this stage is not shown in Figure 4-1. Most studies of larvae, e.g., those by Michener (1953a) and numerous studies by Rozen, are based on such larvae, because they are often available and have a rather standard form for each species; feeding larvae are so soft that their form frequently varies when preserved. Prepupae are often the stage that passes unfavorable seasons, or that survives in the cell for one to several years before development resumes. Houston (1991b), in Western Australia, recorded living although flaccid prepupae of Amegilla dawsoni (Rayment) up to ten years old; his attempts to break their diapause were not successful. Such long periods of developmental stasis probably serve as a risk-spreading strategy so that at least some individuals survive through long periods of dearth, the emergence of adults being somehow synchronized with the periodic blooming of vegetation. Even in nondesertic climates, individuals of some species remain in their cells as prepupae or sometimes as adults for long periods. Thus Fye (1965) reported that in a single population and even in a single nest of Osmia atriventris Cresson in Ontario, Canada, some individuals emerge in about one year, others in two years.

An account of delayed emergence as risk-spreading behavior in a desert bee, Macrotera portalis (Timberlake), was given by Danforth (1999b); see also Minckley, Cane, and Kervin (2000). An account of possible risk-spreading behavior in Hylaeus grossus Cresson, by construction of most cells in different places rather than assembled in one or few nests as do related forms, is by Michener and Brooks (2003).

Mature larvae of many bees spin cocoons, usually at about the time of larval defecation, much as is the case in sphecoid wasps. The cocoons are made of a framework of silk fibers in a matrix that is produced as a liquid and then solidifies around the fibers; the cocoon commonly consists of two to several separable layers. Various groups of bees, including most short-tongued bees, have lost cocoon-spinning behavior and often are protected instead by the cell lining secreted by the mother bee. Cocoon spinning sometimes varies with the generation. Thus in Microthurge corumbae (Cockerell), even in the mild cli

Figure 4-2. Change of a mature larva to a prepupa shown by last larval stadium of Neffapis longilongua Ruz. a, Pre-defecating larva; b, Postdefe-cating larva or prepupa. (The abdominal segments are numbered.) From Rozen and Ruz, 1995.

Pre Defecating

Figure 4-2. Change of a mature larva to a prepupa shown by last larval stadium of Neffapis longilongua Ruz. a, Pre-defecating larva; b, Postdefe-cating larva or prepupa. (The abdominal segments are numbered.) From Rozen and Ruz, 1995.

mate of the state of Sao Paulo, Brazil, the cocoons of the overwintering generation are firm and two-layered but those of the other generation consist of a single layer of silk (Mello and Garofalo, 1986). Similar observations were made in California by Rozen (1993a) on Spheco-dosoma dicksoni (Timberlake), in which larvae in one-layered cocoons pupated without diapausing, whereas those in two-layered cocoons overwintered as prepupae. In other cases, in a single population, some individuals make cocoons and others do not. Thus in Exomalopsis nitens Cockerell, those that do not make cocoons pupate and eclose promptly, but those that make cocoons diapause and overwinter (Rozen and Snelling, 1986).

When conditions are appropriate, pupation occurs; for all eusocial species and many others this means soon after larval feeding, defecation, and prepupal formation are completed. In other species pupation occurs only after a long prepupal stage. Pupae are relatively delicate, and their development proceeds rapidly; among bees the pupa is never the stage that survives long unfavorable periods. Because they are delicate and usually available for short seasons only, fewer pupae than larvae have been preserved and described. Pupal characters are partly those of the adults, but pupae do have some distinctive and useful characters of their own (see Michener, 1954a). Most conspicuous are various spines, completely absent in adults, that provide spaces in which the long hairs of the adults develop. Probably as a secondary development, long spines of adults, like the front coxal spines ofvarious bees, arise within pupal spines.

Adults finally appear, leave their nests, fly to flowers and mate, and, if females, according to species, either return to their nests or construct new nests elsewhere. Many bees have rather short adult lives of only a few weeks. Some, however, pass unfavorable seasons as adults; if such periods are included, the adult life becomes rather long. For example, in most species of Andrena, pupation and adult maturation occur in the late summer or fall, but the resulting adults remain in their cells throughout the winter, leaving their cells and coming out of the ground in the spring or summer to mate and construct new nests. In most Halictinae, however, although pupation of reproductives likewise occurs in late summer or autumn, the resulting adults emerge, leave the nest, visit autumn flowers for nectar, and mate. The males soon die, but the females dig hibernaculae (blind burrows), de novo or inside the old nest, for the winter. A few bees live long, relatively active adult lives. These include the queens of eusocial species and probably most females of the Xylocopinae and some solitary Halictinae. Among the Xylocopinae, a female Japanese Ceratina in captivity is known to have laid eggs in three different summer seasons, although only one was laid in the last summer (for summary, see Mich-ener, 1985b, 1990d). Females of some solitary Laioglos-sum (Halictinae), especially in unfavorable climates (only a few sunny days per summer month, as in Dartmoor,

England) provision a few cells, stop by midsummer, and provision a few more cells the following year (Field, 1996). Like the variably long inactivity of prepupae described above, this may be a risk-spreading strategy.

The male-female interactions among bees are diverse; they must have evolved to maximize access of males to receptive females and of females to available males. The mating system clearly plays a major role in evolution. Reviews are by Alcock et al. (1978) and Eickwort and Ginsberg (1980); the following account lists only a few examples selected from a considerable literature. Many male bees course over and around flowers or nesting sites, pouncing on females. In other species females go to particular types of vegetation having nothing to do with food or nests and males course over the leaves, pouncing on females when they have a chance. In these cases mating occurs quickly, lasting from a few seconds to a minute or two, and one's impression is that the female has no choice; the male grasps her with legs and often mandibles and mates in spite of apparent struggles. The male, however, may be quite choosy. In Lasioglossum zephyrum (Smith), to judge largely by laboratory results, males over the nesting area pounce on small dark objects including females of their own species, in the presence of the odor of such females, but do so primarily when stimulated by unfamiliar female odor, thus presumably discriminating against female nestmates, close relatives of nestmates, and perhaps females with whom they have already mated (Michener and Smith, 1987). Such behavior should promote outbreeding. Conversely, it would seem, males are believed to fly usually over the part of the nesting area where they were reared; they do not course over the whole nesting aggregation (Mich-ener, 1990c). Such behavior should promote frequent inbreeding, since males would often encounter relatives, yet they appear to discriminate against their sisters. The result should be some optimum level of inbreeding.

In communal nests of Andrena scotia Perkins (as A. ja-cobi Perkins) studied in Sweden, over 70 percent of the females mated within the nests with male nestmates (Pax-ton and Tengo, 1996; Paxton et al., 2000). Such behavior, with its potential for inbreeding, may be common in communal bees. Given the rarity with which one sees mating in most species of bees, it may be that mating in nests is also common in some solitary species. In species that have several sex-determining loci, inbreeding may not be particularly disadvantageous, because deleterious genes tend to be eliminated by the haploid-male system.

In some bees, females tend to mate only once. Males in such species attempt to mate with freshly emerged young females, even digging into the ground to meet them, as in Centrispallida Fox (Alcock, 1989) or Colletes cunicular-ius (Linnaeus) (Cane and Tengo, 1981). In other species females mate repeatedly. The behavior of males suggests that there is sperm precedence such that sperm received from the last mating preferentially fertilize the next egg. Males either (1) mate again and again with whatever females they can capture, as in Dianthidium curvatum (Smith) (Michener and Michener, 1999), or (2) remain in copula for long periods with females as they go about their foraging and other activities, thus preventing the females from mating with other males (many Panurginae, personal observation).

In Colletes cunicularius (Linnaeus), Lasioglossum zephyrum (Smith), Centris pallida Fox, and many others, female-produced pheromones seem to stimulate or attract males, but in Xylocopa varipuncta Patton a male-produced pheromone attracts females to mating sites (Alcock and Smith, 1987). Some male Bombus scent-mark a path that they then visit repeatedly for females (Haas, 1949). In other species of Bombus, those with large-eyed males, the males wait on high perches and dash out to passing objects including Bombus females (Alcock and Alcock, 1983). Although playing a role in all cases, vision is no doubt especially important also in other bees with large-eyed males, such as Apis mellifera Linnaeus, the males of which fly in certain congregating areas and mate with females that come to those areas; see also the comments on mating swarms of large-eyed males in Section 28.

Most male bees can mate more than once, but in Meliponini and Apini the male genitalia or at least the en-dophallus is torn away in mating, so that after the male mates he soon dies.

Males in many species of bees in diverse families have enlarged and modified legs, especially the hind legs (see Sec. 28), or broad heads with long, widely separated mandibles. These are features that help in holding females for mating, and may be best developed in large males. Many males of Megachile have elaborately enlarged, flattened, pale, fringed front tarsi (Fig. 84-19). Wittmann and Blochtein (1995) found epidermal glands in the front basitarsi; at mating these tarsi hold the female's antennae, or cover her eyes. This behavior and gland product are presumably associated with successful mating or mate choice.

Large-headed males occur especially in some An-drenidae—both Andreninae and Panurginae—and in some Halictinae. Large heads appear to be characteristic of the largest individuals of certain species, no doubt as an allometric phenomenon. In two remarkable examples, one an American Macrotera (Panurginae) (Danforth, 1991b) and the other an Australian Lasioglossum (Chilal-ictus) (Halictinae) (Kukuk and Schwarz, 1988; Kukuk, 1997), the large-headed males (Figs. 4-3, 58-3, 58-4) have relatively short wings and are flightless nest inhabitants in communal colonies. The large-headed males also have large mandibles and fight to the death when more than one is present in a nest. Smaller males of each species have normal-sized wings and fly. Great size variation among males and macrocephaly may be most frequent in, or even limited to, communal species. Unlike most male bees that leave the nest permanently and mate elsewhere, short-winged males mate with females of their own colony. Thus such a male is often the last to mate with a female before she lays an egg.

In some other bees the male mating strategy also varies greatly with body size. Large males usually fly about the nesting sites, finding young females as they emerge from the ground or even digging them out of the ground, presumably guided by odor. Small males seek females on flowers or in vegetation near the nesting area. Such dual behavior is documented for Centris pallida Fox (Alcock, 1989) in the Centridini, and for Habropoda depressa (Fowler) (Barthell and Daly, 1995) and Amegilla dawsoni (Rayment) (Alcock, 1996), both in the Anthophorini.

Figure 4-3. Male morphs of Lasioglossum (Chilalictus) hemichal-ceum (Cockerell) from Australia. a, Ordinary male; b, c, Heads of same; d, Large, flightless male; e, Head of same. From Houston, 1970.

Such behavior seems akin to that of Anthidium manica-tum (Linnaeus), in which large males have mating territories that include flowers visited by females (Severing-haus, Kurtak, and Eickwort, 1981), whereas small ones are not territorial, and to that of certain Hylaeus (Alcock and Houston, 1996), in which large males with a strong ridge or tubercle on S3 are territorial whereas small ones with reduced ventral armature or none are not territorial. The ventral armature is apparently used to grasp an adversary against the thoracic venter by curling the meta-soma.

An interesting and widespread feature in Hymenop-tera is the prevalence of yellow (or white) coloration on the faces of males. If a black species has any pale coloration at all, it will be on the face (usually the clypeus) of males. Species with other yellow markings almost always have more yellow on the face of the male than on that of the female, although on the rest of the body yel

Figure 4-3. Male morphs of Lasioglossum (Chilalictus) hemichal-ceum (Cockerell) from Australia. a, Ordinary male; b, c, Heads of same; d, Large, flightless male; e, Head of same. From Houston, 1970.

low markings often do not differ greatly between the sexes. Groups like Megachile that lack yellow integumen-tal markings frequently have dense yellow or white hairs on the face of the male, but not on that of the female. In mating attempts males usually approach females from above or behind, so that neither sex has good views of the face of the other. Therefore I do not suppose that the male's yellow face markings have to do with male-female recognition or mating. Rather, I suppose that they are involved in male-male interactions, when males face one another in disputes of various sorts. Sometimes, males of closely related species, such as Xylocopa virginica (Linnaeus) and californica Cresson, differ in that one (in this case virginica) has yellow on the face but the other does not. Someone should study the male-male interactions in such species pairs. Presumably, male behavior linked to yellow male faces is found in thousands of species of Hy-menoptera.

Obviously, the variety of mating systems in bees de serves further study, both because of its interest for bee evolution and for evolutionary theory. Moreover, because of the frequency of morphological or chromatic correlates, mating systems and such correlates are important for systematists.

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