Dual Origin of Highly Social Behavior Among Bees (Hymenoptera/Apidae/Phylogeny) MARK L

Proc. Natl. Acad. Sci. USA Vol. 74, No. 3, pp. 1135-1137, March 1977 Evolution Dual origin of highly social behavior among bees (Hymenoptera/Apidae/phylogeny) MARK L. WINSTON AND CHARLES D. MICHENER Department of Entomology, University of Kansas, Lawrence, Kans. 66045 Contributed by Charles D. Michener, December 27,1976

ABSTRACT A study of behavior and structure indicates the corbicula from the distal end of the tibia in Apis (Apini) (3, that highly eusocial behavior arose twice in the bees-i.e., in 4), Bomibs (Bombini) (5), Melipona and Trigona (Meliponini), the stingless bees (Meliponinae) and in the honeybees (Apinae). and Euglossa and Euplusia (Euglossini) (observations by the Morphological features demonstrate the distinctiveness of these two groups and the relationship of the latter to bumblebees authors). This method of loading the corbicula with pollen, (Bombini) and orchid bees (Euglossini) The social behaviors of presumably characteristic of all of the nonparasitic Apidae, is the stingless bees and honeybees, while more or less equally quite different from the scopa-loading movements of other bees elaborate, are so different as to support their independent ori- and is therefore a distinctive feature of the Apidae. gins. The primitive apids, along with the related Xylocopinae The Meliponinae have retained a relatively small, slender, (in the Anthophoridae), appear to have had the potential for hind basitarsus, like that of most other bees. There is no auricle arasocial, subsocial, an primitively eusocial behavior and (Fig. 2) for pressing pollen upward into the corbicula. As in from such forms the two highly eusocial groups arose. other apids the apex of the tibia is usually equipped with a comb It has often been thought that highly social behavior arose only of stiff bristles (b) but this comb or rastellum is often not well- once among bees, all such bees having a common, highly formed. In addition, nearly all stingless bees have a penicillum eusocial ancestor (1). The development of such behavior, (c, one or more short rows of long curved bristles on the outer probably the most elaborate of any invertebrate, is remarkable side of the apex of the tibia), a structure unique to the Melipo- enough; independent parallel development of two highly ninae. Stingless bees transfer pollen from the middle leg to the eusocial systems would be even more noteworthy. The purpose hind leg of the same side by pulling the former through the of this paper is to report evidence that the social systems of the space between the penicillum and the base of the hind basi- two highly social groups of bees evolved independently. tarsus. Because of the curvature of the penicillum, such a The highly eusocial bees are those that live in large perennial movement apparently pushes pollen up into the corbicula colonies with morphologically different queen and worker (observations of Trigona pallida by the authors). castes. Lone individuals are unable to survive and establish The other apids are united by several common, derived colonies, which therefore multiply by swarming. Elaborate morphological and behavioral characters. The base of the hind chemical and physical communication coordinates swarming basitarsus is expanded posteriorly to form an auricle (d), a individuals, recruits foragers to food and other resources, reg- surface opposable to the apex of the tibia, forming the pollen ulates production of the two female castes and presumably of press which pushes pollen proximally into the corbicula, at least the sexes, and performs other coordinating functions within in Apis and Bombus. A well-formed row of bristles, the ras- colonies (1). tellum (b), extends across the apex of the tibia on the inner There are only two major taxonomic groups of highly eusocial surface, and at least in these two genera serves to comb pollen bees, both in the family Apidae: (i) the stingless honeybees of off the opposite hind leg (3-5), so that pollen collected on one the tropics and (if) the true honeybees. Because of their com- side of the body is carried in the corbicula of the opposite side. mon character of highly eusocial behavior, as well as certain Such transfer of pollen from one side of the body to the other morphological characteristics, the tribes Meliponini (stingless is not known to be characteristic of any other bees. bees) and Apini (honeybees, all in the genus Apis) have been The maxilla of stingless bees also appears primitive relative united in the subfamily Apinae and separated from the other to that of other apids. In Meliponinae, a well-developed process two tribes in the Apidae, the Bombini (bumblebees) and the (Fig. 3) extends from the basal end of the stipes to the sub- Euglossini (orchid bees) (2) (Fig. 1A). However, morphological mentum; this process is lost (e) in other apids. Certain other studies and an evaluation of their social behavior suggest early long-tongued bees, including many genera in the closely related differentiation as well as strong divergence of the stingless bees Xylocopinae (family Anthophoridae; best developed in Cera- from the remaining Apidae. tina, Braunsapis, and Xylocp) as well as in the Megachilidae, have a similar process. The Apidae probably arose from a xy- locopine-like ancestor (6) having a stipital process; its loss is thus LINES OF DESCENT a derived character of the Apinae-Bombinae line. The heavily sclerotized subgaleal sclerite (Fig. 3) of meliponines, similar to Fig. 1B is a cladistic hypothesis for the Apidae. The principal that of Xylocop and Lestis in the Xylocopinae, also retains the structures suggesting that the Meliponinae is the sister group probable primitive condition for Apidae, with a strong trian- to all the other apids are in the pollen-handling apparatus on gular projection at each end. The subgaleal sclerite of the Ap- the hind legs and in the maxilla. These and other characters are inae-Bombinae is generally lightly sclerotized and straight (f), lettered (in parentheses) below and the positions at which they again seemingly a common derived character for that group. arose are indicated by the same letters in Fig. 1B. Within the Apidae the reduced stigma of the forewing (g) The Apidae are characterized by the presence of a corbicula is another derived common character of the Apinae-Bombinae. or pollen basket (a) on the outer surface of each hind tibia of Moderate-sized stigmas are widespread among the families of females (at least workers), a structure that serves to carry pollen bees and appear to be ancestral, but reduction also is common and nest-building materials (Fig. 2). Pollen is pushed up into and, like the loss of maxillary processes and sclerotization, is less 1135 Downloaded by guest on October 2, 2021 1136 Evolution: Winston and Michener Proc. Natl. Acad. Sci. USA 74 (1977)

Bombinae Euglossini Bombini

Meliponinae, k Apinae qq 0 n * Ed B A API DAE ANTHOPHORIDAE b Xylocopinae

~a E *..*.MB x A FIG. 1. Dendrograms showing old and new classifications of the FIG. 3. Inner views of maxillae of Apidae. Left. Apinae, Apis Apidae. A. Old phylogenetic diagram, with initials of the subfamilies mellifera. Right. Meliponinae, Trigona pallida. and tribes shown in B. B.Proposed cladistic pattern. Shading indicates highly eusocial groups. Small letters indicate the segments of the on the outer mandibular surfaces (1) (Michener and Fraser, cladogram in which the characters discussed arose (see text). unpublished data). meaningful for cladistics than the development of the basitarsal DIFFERENTIATION OF MELIPONINAE auricle and associated features. Early divergence of the Meliponinae from the other apid Additional differences among the apid subfamilies support the groups is at least not contradicted by fossils, because in the Baltic distinctiveness of the Meliponinae and justify our decision to Amber (Eocene) there is a modern meliponine genus (Trigona) recognize it as a subfamily separate from the Apinae. The sting, whereas the other apids do not appear in modern form (7). One well-developed in all other apids and most other bees, is reduced of us (C.D.M.) has recently examined the type of the amber and does not function as a sting in stingless bees (m). Tergal and fossil Electrapis (Roussyana) proava (Menge); it has an auricle sternal apodemes are reduced in meliponines, possibly as a re- and the hind tibial spurs are reduced or absent (only one and sult of reduced abdominal musculature in nonstinging bees (n). very short in the typical subgenus Electrapis) so that it would Wax glands are dorsal in meliponines, ventral in Apis, and seem to be an apine in spite of being superficially Trlgona-like. dorsal and ventral in Bombus (8), suggesting divergence of the Its wing venation, however, is Bombus-like, without the derived Apinae and the Meliponinae. The wing venation of stingless characters found in Apis such as the unusual elongation of the bees, unlike that of other apids, is reduced (o), with a large marginal and submarginal cells (h). stigma and few hamuli. Internal structures such as the pro- Derived characters common to both tribes of Bombinae and, ventriculus, rectal pads (9), and ovarioles (1), also support our justifying their cladistic union, include large size, robust form reclassification. In addition, an interesting behavioral feature (i), papillate distal wing membranes (j), loss of jugal lobes of of the Meliponinae (at least Trigona) is that pollen gathered by and more than the usual number of grooves the fore basitarsi is brushed off onto backward-directed hairs the hind wings (k), of the thoracic venter (p), where it is picked up by the middle legs for transfer to the hind legs (Michener and Winston, un- corbicula published data). In other bees, pollen is transferred directly from the front legs to the middle legs. The major previously used character associating the stingless bees with Apis is the lack of hind tibial spurs (q) (2); it is not. difficult to imagine independent loss of these structures. The same is true for partial loss in both groups of the mandibular grooves and ridges found in other bees (Michener and Fraser, unpublished data). Furthermore, the small to moderate size of Meliponinae and Apinae, compared to the large Bombinae, as well as the superficial resemblance of Melipona to Apis, give the impression that these groups are related. Other characters previously used to unite Apis and the meliponines in a single subfamily (2), such as the length and shape of certain wing veins, have been examined and appear variable and unim- portant. ORIGINS OF SOCIAL BEHAVIOR According to the lines of descent within the Apidae proposed here, there are two possible theories on origin of highly eusocial FIG. 2. Hind tibiae and basitarsi of Apidae. Left. Apinae, Apis behavior within the family. The first is that such behavior arose mellifera. Right. Meliponinae, Trigona pallida. only once, ancestral apids being highly eusocial. The Bombinae, Downloaded by guest on October 2, 2021 Evolution: Winston and Michener Proc. Natl. Acad. Sci. USA 74 (1977) 1137

including the primitively eusocial Bombus and the solitary to (1, 14), may also be important for social interactions. Food parasocial (sense of Michener, ref. 1) euglossines, would tlhs storage in the nest for adult use, which affects the flow of ma- have lost complex, highly eusocial behavior'.' Reversion from terial among members of a colony, is another social trait unique highly eusocial behavior is unlikely, however, in view of the to the Apidae and the Xylocopinae (Allodape, Allodapula, interdependence of castes and inviability of lone bees (1). Braunsapis, and Xylocopa) (6, 14, 15). The corbicula of apids, It therefore seems that highly eusocial behavior evolved twice which can carry not only pollen but material for nest con- in the bees, with similarities in social behavior between Apis struction, might have been a preadaptation for constructing the and the meliponines arising independently. The social biology large nests of eusocial bees. of the two groups supports this view (1, 10). For instance, al- Thus, in a series of behavioral features (as well as in certain though both groups reproduce by swarming, the mechanisms morphological features-stipital process, subgaleal sclerite), are quite different. Meliponine workers fly out from the pa- xylocopines demonstrate similarity to the Apidae. The behav- rental colony, find a new site, and gradually prepare a new nest, ioral features listed above are impressive because they are de- using materials from the old nest. Only when the new nest is rived attributes, common to some members of the two groups ready does a young queen join workers in the new nest, leaving (six tribes and subfamilies) but lacking in the remaining 32 the old queen behind in the original nest. In Apis, on the con- tribes and subfamilies of nonparasitc bees. The common an- trary, it is the old queen which departs with some of the cestor of Xylocopinae and Apidae must have had the potential workers, leaving a new queen in the old nest. Swarms leave the for developing parasocial, subsocial, and primitively eusocial old colony without having found or prepared a new nest site; behavior, all of which are found in both Xylocopinae and Ap- they remain in an exposed cluster while scout bees locate a idae, and ultimately also the highly eusocial behavior which suitable nesting site. appeared independently in the Meliponinae and Apinae. Apis and meliponines have also evolved sophisticated mechanisms of recruitment to food sources, but again the We are indebted to Dr. Rudolf Jander, University of Kansas, whose mechanisms of recruitment seem to be convergent rather than studies of leg structures and movements led him to conclude that the monophyletic. In Apis, communication concerning distance meliponines are markedly dissimilar from bombines and apines and We also useful and direction of nectar, pollen, and other resources is by means who thereby stimulated the present study. acknowledge discussions with Dr. Alvaro Universidad de Costa Rica. This of the well-known dance language as well as by food odors. Wille, paper was made possible by National Science Foundation Grant GB Meliponines, however, lack comparable dances, relying instead 37301. on a variety of behaviors, including social facilitation, odor trails, and leading foragers part or all of the way to food sources 1. Michener, C. D. (1974) The Social Behavior of the Bees (Harvard (1, 11). The suggestion that such leading is homologous to the University Press, Cambridge, Mass.) straight run of the Apis dance, which is primitively toward the 2. Michener, C. D. (1944) "Comparative external morphology, food source (1, 12), has never been very convincing, partly phylogeny, and a classification of the bees (Hymenoptera)," Bull. because primitive meliponines do not show such behavior. Am. Mus. Nat. Hist. 82,151-326. Other differences in social biology also point to a diphyletic 3. Hodges, D. (1952) The Pollen Load of the Honeybee (Bee Re- origin of highly eusocial behavior within the Apidae. Apis search Assn., Ltd., London). workers feed their larve progressively while meliponines close 4. Snodgrass, R. E. (1956) Anatomy of the Honey Bee (Cornell cells with newly laid eggs and enough food for complete larval University Press, Ithaca, N.Y.). development. Apis queens are produced by feeding a special 5. Sladen, F. W. L. (1912) The Humble Bee (Macmillan & Co., Ltd., to caste determination in London). secretion, royal jelly, larvae, while 6. Michener, C. D. (1972) "Direct food transferring behavior in meliponines is primarily due to quantity of food, although there bees," J. Kans. Entomol. Soc. 45, 373-376. is partial genetic caste determination in the genus Melipona. 7. Zeuner, F. E. & Manning, F. J. (1976) "A monograph on fossil Excess gynes of Apis are killed by the queen; in meliponines, bees (Hymenoptera: Apoidea)," Bull. Br. Mus. (Nat. Hist.) Geol. they are killed by the workers (1). Finally, there are substantial 27,149-270, pls. I-IV. differences in nest architecture between the two groups (1, 13). 8. Cruz Landim, C. da (1963) "Evolution of the wax and scent Meliponines construct food storage pots that are very different glands of the Apinae (Hymenoptera: Apidae)," J. N.Y. Entomol. from brood-rearing cells and commonly surround the brood Soc. 71, 2-13. chamber with involucral layers of soft wax and resin. Apis 9. Cruz Landim, C. da & Rodrigues, L. (1967) "Comparative and of the builds one type of cell for both worker-rearing and food storage, anatomy histology alimentary canal of adult Apinae," J. Apic. Res. 6,17-28. and the brood area lacks involucral layers. In addition, Apis cells 10. Sakagami, S. F. (1971) "Ethosoziologischer vergleich zwischen are long-lasting and reused, while meliponine cells are torn honigbienen und stachellosen Bienen," Z. Tierpsychol. 28, down after a single use. 337-50. If highly eusocial behavior arose twice in the bees, what type 11. Lindauer, M. (1967) "Recent advances in bee communication of social organization might ancestral apids have shown? and orientation," Annu. Rev. Entomol. 12, 439-470. Primitive apids might conceivably have had behavior ranging 12. Kerr, W. E. & Esch, H. (1965) "Comunicagio entre as abelhas from solitary to primitively eusocial, but certain traits of social sociais Brasileiras e sua contribuigio para o entendimento da sua behavior are unique to the Apidae and Xylocopinae among all evolugao," Cienc. Cult. (Sdo Paulo) 17,529-538. the bees, suggesting that the ancestral apid had traits pread- 13. Wille, A. & Michener, C. D. (1973) "The nest architecture of apting it to eusocial behavior. Liquid food transfer between stingless bees with special reference to those of Costa Rica (Hy- menoptera: Apidae)," Rev. Biol. Trop. (Costa Rica) 21 (Suppl. adults, found only in Apis, meliponines, Bombus (rarely), and 1), 1-279. Xylocopinae (Xylocapa, Exoneura, and Braunsapis), may have 14. Michener, C. D. (1971) "Biologies of African allodapine bees been a prerequisite for the evolution of the extensive commu- (Hymenoptera, Xylocopinae)," Bull. Am. Mus. Nat. Hist. 145, nication among adults of eusocial species (6). Progressive 219-302. feeding of larvae, found only in Apis, Bombus (with little direct 15. Rau, P. (1933) Jungle Bees and Wasps of Barro Colorado Island adult-larva contact, however), and most allodapine Xylocopinae (publ. by author, Kirkwood, Mo.). Downloaded by guest on October 2, 2021