ORIGIN AND EVOLUTIONARY HISTORY OF THE

Bee World 64(1) : 29-38 (1983)

ORIGIN AND EVOLUTIONARY HISTORY OF THE HONEYBEES APIS by THOMAS W. CULLINEY Department of Entomology, Cornell University, Ithaca, NY 14853, USA

Introduction The fossil record, in general, presents a severely limited and unrepresentative sample of past life. Only about 130 000 fossil species, representing less than 3% of the probab}e total number of organisms that have ever lived, have been described and named35 • This dearth of material is a consequence of the fossilization process: not all organisms have' an equal chance of becoming fossilized, and not all geological environments are equally favourable to the production of fossils. About 12 000 fossil insect species are known 35 , the oldest* being of Devonian age 14• 38 (the major divisions of geological time are presented in Table 1). The scarcity of fossil specimens, in this largest class of animals, reflects the fact that insects generally occupy habitats that are not conducive to their preservation as fossils 35 . But despite its inherent deficiencies, the fossil record does provide valuable information on the histories of certain insect groups; among them the bees. TABLE 1. Major divisions of geological time. Entries in the final column are in million years before the present.

Era

Period Quaternary

Cenozoic Mesozoic

Paleozoic Proterozoic (Precambrian)

Tertiary Cretaceous Jurassic Triassic Permian Carboniferous Upper Lower Devonian Silurian Ordovician Cambrian

Epoch

Began

Holocene Pleistocene Pliocene Miocene Oligocene Eocene Paleocene

0·011 2 10

27 3!]11 55 65 130

180 225 260 300

340 405 435 480 570

*Order Collembola. Although some doubt exists among authorities as to the true phylogenetic position of Collembola, the classification of Boudreaux2 includes the order within the class Insecta, and is accepted here.

30

Preservation of fossil bees has often been excellent48 • Many specimens have come to light, such as those embedded in amber, with important morphological characters well displayed, a circumstance permitting the determination of systematic and evolutionary relationships with some measure of confidence. The present article summarizes available evidence, from the fossil record and other sources, for the probable origin and evolution, in geological time, of one particular group of bees: members of the honeybee genus Apis. It represents a first attempt to bring together the sometimes ambiguous and conflicting findings from a rather scant literature on the subject, and from them to present a reasonably coherent and plausible picture of honeybee evolutionary history.

Origin of the Apoidea In a review of this kind, it is .useful first to present an outline of prevailing theory concerning the origin and evolution of the bees as a group. 'Theory' would seem the appropriate word, in light of the highly speculative nature of the subject31 • All bees belong to the superfamily Apoidea. The total number of living species in this group has been estimated to be of the order of 20 00025 ' 30 , divided into about 700 genera25 of 10, or possibly 11, families 33 . No other group of aculeates, or stinging Hymenoptera, has such a diversity of species 41 • On the basis of morphological similarities, it is generally accepted that the bees were derived as a monophyletic offshoot from the burrowing wasps of the superfamily Sphecoidea8 ' zs, 28 , 30 • No existing sphecoid wasps, however, can be identified with certainty as the ancestral group. The earliest bees may have arisen in the paleocontinent Gondwana, probably in its western region32 , the xeric interior of which has been suggested by Raven and Axelrod36 as the area of origin of the angiosperms, or flowering plants. Divergence from the sphecoid stock may have occurred as late as the middle Cretaceous 28 , 31 , 32 , a period during which angiosperms became the dominant vegetation36 . Recent fossil discoveries confirm the existence of sphecoids at that time 13 . Burnham3 has suggested that bees may have evolved even earlier, in response to the food source provided by the pteridophytes, or ferns, and were thus preadapted to serve as pollinators by the time the angiosperms made their appearance--becoming, in this capacity, the driving force behind the subsequent explosive adaptive radiation and success of this plant group. But in spite of the obvious affinity between living primitive bees and the sphecoid wasps, there are difficulties associated with the study of apoid phylogeny. The Cretaceous insect fauna as a whole is barely known6 , and this lack of an adequate fossil record has made it impossible to ascertain the exact ancestral phyletic line of the bees45 . In addition to relative primitivity of structure, biogeographical evidence indicates that the short-tongued families Colletidae and Halictidae are the two oldest, still extant groups of bees, dating possibly from the Cretaceous28 ' 31 , and presumably evolving in concert with the shallow-flowered angiosperms prevalent at that time. Colletids and halictids are· the only two families well represented in the Australian bee fauna. Moreover, Australia is the only continent in which most of the genera and nearly half of the named species of bees belong to the Colletidae29 . Few genera of this family occur in Eurasia and North America; genera are somewhat more numerous in South America and Africa. This family thus shows the same panaustral type of distribution seen among other

31

primitive southern animal groups. Australia completely lacks families that are otherwise distributed world-wide, or nearly so, including the Andrenidae and Melittidae 29 • 32 . Such a distributional pattern suggests that the Colletidae and Halictidae existed in Australia early, when the continent was still connected by land to other continents28 , and that the subsequent isolation of this continent prevented the invasion and establishment of later-evolving bee families. Some support for this comes by way of the theory of plate tectonics, or continental drift. Africa and South America (comprising West Gondwana) are thought by geologists to have separated from Australia and Antarctica (East Gondwana) in Cretaceous times 34 . The proposed antiquity of the Colletidae and Halictidae, however, is not corroborated by any concrete evidence from the fossil record. No fossil coiletids have yet been found. Few halictids are represented as fossils, and all are in the subfamily Halictinae, the earliest dating from the Oligocene epoch of the Tertiary period 3 • 48 . The first records of fossil bees are from the Baltic amber of the Upper Eocene epoch26 • 48 (see also Kelner-Pillault 16), perhaps 40 million years old. Five families are represented: Andrenidae, Melittidae*, Megachilidae, Anthophoridae and Apidae, the family to which the honeybees belong48 • Social behaviour among the bees probably arose early in the Tertiary31 . Recent discoveries have established, in particular, the early development in the bees of eusociality, the highest expression of social behaviour. Among the Apidae, fossil meliponines (stingless bees) of the extant genus Trigona Jurine-some identified as workers--have been described from Baltic ambert as old as Upper Eocene age 15 • 17 as well as from amber of Oligocene and Miocene age from the New World42 • 44 (see also the review of fossil meliponines by Wille 43 ). Michener32 thought it likely that the meliponines had originated by Upper Cretaceous times, when Africa and South America were still joined or not yet widely separated, and that the present pantropical distribution of the group resulted largely from continental movements. Highly social behaviour has formerly been regarded as arising only once among the bees, all such bees having a highly eusocial ancesto~ 1 . Recent morphological and behavioural studies by Winston and Michener46 , however, may suggest that the social systems of the two highly social groups of bees, the meliponines and Apis (the two comprising the subfamily Apinae), evolved independently. These authors have interpreted their results as indicating an early and strong divergence of meliponines from the other apids, a divergence that is not contradicted by the fossil record, in which, as mentioned above, specimens of Trigona are found in strata lacking other apids of modern form. Winston and Michener46 have therefore concluded that highly eusocial behaviour evolved twice in the bees, similarities in social behaviour between meliponines and Apis apparently resulting from convergent evolution. They have proposed that the stingless bees be assigned to a separate subfamily, the Meliponinae.

*Subfamily Ctenoplectrinae. Michener and Greenberg33 have divided the Melittidae, excluding from it the Ctenoplectrinae, and raising this subfamily to family rank. tThese discoveries also establish the past existence in Europe of a group of bees now confined strictly to the tropics and subtropics.

32

Ancestral lineage of Apis Most of the known fossil apids belong to the tribe Apini48 , a fortunate situation for us, given the vicissitudes of the fossilization process, that allows some insight into the evolutionary development of the genus Apis. The main characteristics of modern Apini, today represented by Apis alone, are believed to have evolved by Upper Oligocene times 26 • 47 . Manning26 , and Zeuner and Manning 48 , have placed all primitive Apini in the extinct Eocene genus Electrapis Cockerell, specimens of which have been found in the Baltic amber. Repeated finds of individuals grouped together in the same amber specimen strongly suggest that this genus contained species that were social23 , although Zeuner47 has concluded that they could hardly have had a social life higher than that of the primitively eusocial bumble bees. Electrapis is considered to be in the line directly ancestral to Apis26 • 27 • 48 , with E. meliponoides (Buttel-Reepen), in particular, ancestral to both the meliponines and more recent apines48 . The phyletic position of Electrapis is not without its ambiguities, however, and the above determination has not been accepted by all authorities on bee taxonomy. Kelner-Pillault 18 concluded that Electrapis possessed too many of the characters of primitive apids to be regarded as the direct ancestor of Apis. Maa24 felt certain that the genus was not of the Apini, and possibly not of the subfamily Apinae. The rate of evolutionary change in the lineage leading to Apis was apparently rapid. This is indicated not only in the fossil record, which depicts a large change in external morphology in apines between the Upper Eocene and Upper (%:gocene, a span of perhaps not more than 10 million years 26 • 47 , but also in comparative biochemical studies of living apoids4 • 5 . Results of recent investigations into the composition of proteins, obtained from A. mellifera L. and from bees of the same and other families, have shown a greater degree of amino acid substitution in A. mellifera compared to that in the other bees, suggesting a more rapid protein evolutionary rate in the honeybee lineage than in other bee groups. Such rapid protein evolution, it has been proposed4 • 5 , may have resulted from selective pressures accompanying the development of eusociality in the honeybee line. (A correlation between insect social behaviour and rapid evolution at the anatomical level has been suggested by Michener28 .) On the basis of morphological evidence, a long period of relative stasis in honeybee evolution has reigned since Miocene times26 • 47 ; fossil Apis all appear closely related to each other and to modern species 47 • 48 .

The rise of Apis True honeybees of the genus Apis probably arose in the Old World early in the Oligocene (Fig. 1), and were likely already eusocial before the end of that epoch, as indicated in the resemblance of fossil forms to modern worker bees in the structure of the legs, tongue, and abdomen37 • 47 . The known Oligocene, Miocene, and Quaternary Apini are all' represented solely by this genus48 • Deodikar9 and Deodikar et al. 10a, 11 have postulated that, since the natural geographical distribution of Apis shows its greatest diversity in India and adjacent areas, these regions probably constitute the centre of its origin and early evolution. Michener32 has lent some support to this argument by pointing out that, while the origin of the Apinae (now considered to contain only Apis46 ) is obscure, the

33

Fig. 1. An early honeybee (Apis henshawi Ckll) from the Oligocene of Germany. Photo courtesy of Frank M. Carpenter.

subfamily's distribution is centred in the Oriental region. Before European settlement, Apis was not found anywhere in the Western Hemisphere, Australia, or the Pacific except on continental islands such as Japan, Formosa, the Philippines and Indonesia31 . An early account of some fossil honeybees was given in Armbruster 1 . Maa24 listed various species of 'Apis', which he considered of doubtful validity, from the Oligocene and Miocene of Europe. He assigned these to two extinct genera: Synapis Cockerell, comprising Oligocene specimens, and Hauffapis Armbruster, containing the Miocene fossils (Table 2). These genera were said to resemble closely, in their morphology, the giant honeybee A. dorsata F. (considered by Maa to be the most primitive living apine), Synapis being definitely more primitive than Hauffapis. These classifications were modified and elaborated by Zeuner and Manning48 , who consigned Synapis to sub generic rank and placed Hauffapis into synonymy with the subgenus Apis (Table 2). The now widespread species A. mellifera is believed to have originated in the African tropics or subtropics sometime around the end of the Tertiary, migrating to colder climates later, but prior to its association with man45 . According to Michener (quoted in Wilson45 ), the early distribution of this species probably included the whole of Africa, all but northernmost Europe, and western Asia. Specimens (said not to differ in any essential point from present-day forms) have been found in East African copal, a fossil resin similar to amber, of Pleistocene age 48 . Cockerelf made mention of specimens in amber reported from Yarmouth, England, but expressed doubts as to their true geographical origin and possible Pliocene age, speculating that the fossils might have

-~ 34

TABLE 2. Two alternative classifications of fossil honeybees (tribe Apini). Specimen Matl- 4

Zeuner & Manning48

'Apis' proava Menge

Electrapis proava (Menge) 'Apis' aquitaniensis de Rillyb Apis (Synapis) cuenoti Theobald 'Apis' dormitans Heydenb Apis (Synapis) henshawi henshawi Ckll

Eocene'

Prussia, Germany

Oligocene

Aix-en-Provence, France

Oligocene

France

Oligo-Miocene

Rott, Germany

Oligo-Miocene

Rott, Germany

Apis (Synapis) henshawi dormiens subsp. nov. Apis (Synapis; henshawi kaschkei (Statz) Apis (Apis) melisuga (Handlirsch) Apis catanensis Roussyc Apis (Apis) armbrusteri armbrusteri Zeunerd Apis (Apis) armbrusteri scharmanni (Armbruster) Apis (Apis) armbrusteri scheeri (Armbruster) Apis (Apis) armbrusteri scheuthlei (Armbruster) Apis (Apis) mellifera L.

Oligo-Miocene

Rot!, Germany

Oligo-Miocene

Rott, Germany

Miocene

Gabbro, Italy

Miocene Upper Miocene

Catania, Sicily Swabia, Germany

Upper Miocene

Germany

Upper Miocene

Germany

Upper Miocene

Germany

Pleistocene'

Yarmouth, England•; East Africa'

'Apis' ( =Synapis?) aquitaniensis de Rilly 'Apis' ( =Synapis?) cuenoti Theobald Synapis dormitans (Heyden) 'Apis' oligocenica Meunier ( =Synapis henshawi (Ckll)) Synapis kaschkei Statz

'Apis' ( = Hauffapis?) armbrusteri Zeuner Hauffapis scharmanni Armbruster Hauffapis scheeri Armbruster Hauffapis scheuthlei Armbruster 'Apis mellifera' L. ( =Synapis?)

Age

Distribution

•Age given in Zeuner and Manning48 bPosition regarded as uncertain by Zeuner and Manning48 cNo description given dA group of 17 individuals was found in limestone deposits, evidently part of an ancient swarm •Location given in Maa24 fr_ocation given in Zeuner and Manning48

come from Africa. A fossilized comb, judged by its cell size to be that of A. mellifera or an immediate ancestor, b'as recently come to light in Malaysia 39 • It has been estimated to be of late Tertiary or early Quaternary age. Polyploidy has been implicated as the ultimate mechanism in the origin of the genus Apis47 . Although speciation by means of polyploidy has been generally considered to be rare in animals, other than those displaying parthenogenesis or hermaphroditism, there is evidence to suggest that it has occurred rather frequently, and has been an important evolutionary factor, within the Apoidea. An estimated 65% of known species of bees are believed to be either polyploid or of polyploid origin21 . In particular, past studies have suggested a polyploid origin for A. mellifera 10a,ll,l 9 , 20 • 21 . In 1966 cytological investigations of the dwarf honeybee A. flo rea F., a species generally considered to exhibit the greatest number of ancestral characters of the genus 22 • 31 , showed a diploid chromosome number of 1610 • This was taken to suggest a polyploid constitution for both A. mellifera and the Asian honeybee A. cerana F., both of which possess a diploid complement of 32,

i

I

35 a doubling of chromosome number being presumed to be the prime factor in the divergence of these two species from A. flo rea, or from an ancestor common to the three. (Michener31 has considered it probable that an ancestral Apis species gave rise to two main phyletic lines: one leading to A. florea, the other to the remaining three living species of the genus. The latter line evidently divided again, one branch giving rise to an ancestor of dorsata, and the other to a common ancestor of cerana and mellifera.) Furthermore, cytogenetic studies of A. cerana by Deodikar et al. 10a confirmed the close phylogenetic affinity between this species and A. mellifera. These results and additional supporting evidence, including the observation that mellifera workers will tend a cerana queen, and the close resemblance between A. mellifera and some Himalayan forms of A. cerana, have prompted Deodikar9 • lOa,u and Kerr and Laidlaw (1956) 20 to suggest that mellifera and cerana might be merged into a single species. However, more recent cytological studies by Fahrenhorst 13 a, employing refined techniques, have invalidated the earlier karyotypic results, and revealed a diploid number of 32 in A. florea. A polyploid origin for A. mellifera, in particular, must thus be discounted, although the role of polyploidy in the origin of the honeybee genus remains plausible 47 • The development in A. mellifera of three European races: a northwestern 'black' race (A. m. mellifera), a southeastern 'grey' race (A. m. carnica), and an Italian 'yellow' race (A. m. ligustica), is believed to have resulted from events occurring during the last glaciation in the late Pleistocene, when conditions made it impossible for honeybees to survive in central Europe 12 . The then-existing population presumably became fragmented, and survived only in three mutually isolated southern areas: one in Spain and southern France, one in Italy, and one in the Balkan peninsula. In these refugia, the three distinct races evolved. As the glaciers were retreating around 10 000 years ago, the western and eastern races were apparently able to re-invade central Europe, but remained separated from each other, and from the Italian race, by the barrier produced by the Alps.

Conclusions Although, by its very nature, it cannot establish with any certainty an exact time of origin, the fossil record does give a reasonable approximation of the antiquity of the genus Apis, revealing a history of this group spanning perhaps as many as 35 million years. There is some evidence, albeit from an undeniably incomplete source, that-if classificatory schemes of fossil forms are valid (Table 2)-the genus, from an origin and radiation early in the Tertiary, has suffered some decline in diversity over succeeding epochs to the comparative paucity of the four (or three?) species existing at the present time. Global climate was generally mild throughout the Tertiar~ 4 , and conditions prevailing during that period may have favoured a greater diversity of honeybee species. The coming of the ice age at the beginning of the Quaternary may have brought about the extinction of a number of these earlier kinds, and led to the rise of species possessing behavioural adaptations suited to the colder climatic conditions. (The species A. dorsata and A. flo rea, that build their comb in the open, and are considered more primitive and similar to the ancestral type than the other living honeybees, are today restricted to regions within the Old World tropics, while A. mellifera ranges well into cold temperate zones.) There is

36 also the possibility, as Zeuner47 has speculated, that the capacity to produce numerous closely related species, as shown in many genera of solitary bees, may have become lost in Apis as a consequence of the evolutionary stability resulting from the development of eusociality. A. mellifera is, by all indications, a relative newcomer on the apine evolutionary scene, its apparent point of origin on the geological time scale predating that of another social animal, Homo, by only a slight interval. In light of this, it is perhaps fitting that the two, honeybee and man, arising within such a short time of each other on their respective phylogenetic trees, should come to establish such a close relationship, one that has been growing and improving at least since the Stone Age 40 , and that may prove to be a significant factor in the future evolution of this honeybee species.

Acknowledgements I wish to thank Professors Roger A. Morse and George C. Eickwort for reviewing an earlier draft of the manuscript. Dr. Eickwort's comments and references to recent papers on new developments in bee systematics are especially appreciated. I also thank Professor Frank M. Carpenter, Harvard University, for the photograph reproduced in Fig. 1.

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WILLE, A.; CHANDLER, L. (1964) A new stingless bee from the Tertiary amber of the Dominican Republic (Hymenoptera: Meliponini). Revta Bioi. trap. (Costa Rica) 12(2) : 187-195 . WILSON, E. 0. (1971) The insect societies. Cambridge, MA : Belknap Press of Harvard University Press WINSTON, M. L.; MicHENER, C. D. (1977) Dual origin of highly social behavior among bees. Proc. natn. Acad. Sci. U.S.A. 74(3) : 1135-1137 ZEUNER, F. E. (1951) A discussion of time-rates in evolution. Proc. Linn. Soc. Land. 162 : 124-130 ZEUNER, F. E.; MANNING, F. J. (1976) A monograph on fossil bees (Hymenoptera: Apoidea). Bull. Brit. Mus. (Nat. Hist.), Geol. 27(3) : 151-268