Original article

Fossil honey bees and evolution in the genus Apis(Hymenoptera: Apidae)

Michael S. Engel

Department of Entomology, Comstock Hall, Cornell University, Ithaca, NY 14853, USA

(Received 22 August 1997; accepted 12 December 1997)

Abstract - A partial revision is provided for some of the more well-known fossil honey beespecies. Apis henshawi is diagnosed, the holotype described, and a complete taxonomichistory presented. The following names are newly synonymized under A. henshawi:A. henshawi dormiens and A. aquisextana. A new species, A. vetustus sp. n., is recognizedfrom Oligocene strata. Synapis petrefacta is officially transferred into the genus Apis (newcombination) and A. fota and A. shandongica are placed into synonymy with A. miocenica(new synonymies). The authorship of A. melisuga is discussed and the name considered to bea nomen dubium. A phylogeny is proposed for Apis which incorporates the known fossilspecies and evolution in the genus discussed. No honey bees are known from before theOligocene. © Inra/DIB/AGIB/Elsevier, Paris

Apis / Apoidea / Cenozoic / paleontology / phylogeny / taxonomy

1. INTRODUCTION

The honey bees (genus Apis L.) are themost well recognized of all insects. Owingto the important role honey bees play inagriculture, it is not surprising that theyshould factor so heavily in our mythology,art and religion. It is surprising, however,that the systematics of such a small andimportant group should be so confused.Four to twenty-four species have been

recognized at one time or another, and thegenus has been diced into as many as three

genera [3, 20]. As the group is currentlyclassified there are six species, with someauthors according distinctive populationsof the giant honey bee (Apis dorsata F.)or the Asian honey bee (A. cerana F.) spe-cific status [21, 38]. Although the taxo-nomy of these species is in need of mono-graphic study and the taxonomic historiesof all species have been compiled by the

Present address: 1503 Rosewood Terrace Drive, Ballwin, MO 63021, USA

author, the focus of the present work issimply to clarify the taxonomy of someof the known fossil honey bees.

The first fossil species of the genus wasdescribed as A. henshawi by Cockerell [6].Although previous fossils had been pro-posed as species of Apis, Cockerell’s wasthe first correctly assigned to the genus.By the time of Zeuner and Manning’s [42]monograph on the fossil bees of the world,17 fossil honey bee species or subspecieshad been proposed (not including thoselater removed to other genera). Four spe-cies have been added since 1976 by otherworkers [2, 15, 43, 44]. Table I summa-rizes the currently recognized species ofApis along with their geographical and geo-logical distribution. Of the living species,only A. mellifera L., has been found in thefossil record from Pleistocene copal [42].Stauffer [35] reports a fossilized honey

comb from the Malay Peninsula of earlyQuaternary age which is probably the pro-duct of, or a close precursor of, A. cerana(Stauffer assigns the comb to A. javanaEnderlein, a junior synonym of A. cerana).

The holotype of the most famous of thefossil honey bees, A. henshawi (figure 1),is located in the Museum of ComparativeZoölogy, Harvard University. This speci-men, along with the others in that collec-tion, are among the finest. Many of thefiner details of the bees are flawlessly pre-served in the specimens (e.g. figure 8depicts the pollen press of A. henshawi).Due to the inadequacy of the descriptionsprovided by Zeuner and Manning [42] intheir revision, and to the usual splitting ofspecies based on minor size differencesin the absence of diagnosable characters bythese authors, a more detailed treatmentof the fossil bees is required. New des-

criptions for the fossil honey bees in theMuseum of Comparative Zoölogy are pro-vided below along with an attempt to cleanup some of the taxonomic difficulties thathave crept into the genus.

2. MATERIALS AND METHODS

All measurements were made using an ocu-lar micrometer on a WILD-M5a microscopeand should be considered approximate. The fol-lowing abbreviations are used in the remainderof the text: F, flagellomere; MCZ, Museum ofComparative Zoölogy; S, sternum; T, tergum.

3. SYSTEMATICS

3.1 Apis henshawi Cockerell(Figures 1-3, 5-6, 8 and 11)Apis (Synapis) henshawi Cockerell,

1907, Entomologist, London, 40, 229.

Apis dormitans Cockerell, 1907 (nonHeyden, 1862), Entomologist, London,40, 228.

Apis oligocenica Meunier, 1915, Zt.Deut. Geol. Ges., Berlin, 67, 210.

Synapis kaschkei Statz, 1931, Wiss.Mitt. Ver. Nat-Heimatik, Köln, 1, 50.

Apis henshawi dormiens Zeuner andManning, 1976, Bull. Brit. Mus. Nat. Hist.(Geol), 27, 241. Nomen novum pro Apisdormitans Cockerell, 1907. New syno-nymy.

Apis aquisextana Nel, Martínez-Del-clòs, Arillo, and Peñalver, 1996, in Arilloet al., 1996, Bull. Soc. Entomol. France,101, 60. New synonymy.

3.1.1. Diagnosis

Basal vein gently curved and slightlydistad cu-a by 1.5 times vein width. Innerangle of third submarginal cell between2r-m and M nearly orthogonal, much grea-ter than 45°; cell slightly broader on ante-rior border than posterior border. Distalabscissa of vein M in hind wing present.

3.1.2. Description

Holotype (obverse and reverse impres-sions): total body length 15.4 mm; totalforewing length 7.7 mm. Head length3.28 mm. Mandibles broader at apex thanbase (apical width 0.56 mm; basal width0.36 mm; length 1.26 mm), without teeth;distinct dorso-longitudinal carina on innersurface. Mouthparts long. Combinedlength of scape and pedicel 1.28 mm;length of flagellum 2.84 mm; F1-9 eachabout as long as wide, individual lengths0.28 mm; F10 longer than wide, length0.32 mm. Vertex with long, simple hairs.Hairs of compound eye long. Diameter ofmedian ocellus 0.24 mm. Mesoscutum

apparently without pubescence; scutellumwith long hairs. Claws bifid. Basal veingently curved, distad cu-a by 1.5 timesvein width (figures 5 and 11); stigmalength 0.38 mm, width 0.14 mm; anteriorborder of first submarginal cell along Rs0.3 mm in length; length of anterior borderof second submarginal cell 0.24 mm, pos-terior border 1.38 mm; length of anteriorborder of third submarginal cell 0.92 mm,posterior border 0.9 mm, inner posteriorangle between 2r-m and M nearly ortho-gonal; marginal cell long and bluntlyrounded at apex, length 3.12 mm, width0.4 mm. Hind wing with distal abscissaof vein M present, M gently curved. Scat-tered hairs on T5-6; pubescence not appa-rent on preceding terga or sterna; stinglength 1.8 mm, length of ramus 0.54 mm.

Legs of reverse counterpart more finelypreserved than obverse. Fore femur length1.76 mm; tibia length 1.24 mm; basitarsuslength 1.2 mm. Hind tibia length 2.76 mm,width at apex 0.92 mm; corbicula evident,without hairs except along outer margins(base of setae faintly evident); basitarsuslength 1.8 mm, width 1 mm; pollen pressbarely visible, setal rows on basitarsus notapparent.

Clypeus pale brown, remainder of headdark brown. Scape and pedicel dark

brown, flagellum dark brown. Mesosomadark brown. Legs dark brown except tar-someres 2-5 pale brown; claws pale brownexcept apical halves dark brown. T1-2dark brown; remaining terga progressi-vely paler; sterna pale brown.

Specimen Nr 7513: Total body length15.1 mm. Head width 3.52 mm. Combined

length of scape and pedicel 1.24 mm; F1-9each about as long as wide; F10 longerthan wide; flagellum length 2.24 mm.Long eye hairs apparent on left compoundeye. Mesosoma with hairs evident onleft side. Tegula oval. Fore tibia length1.62 mm; basitarsus length 1.18 mm. Hindtibia length 3.24 mm, width at apex 0.76 mm;corbicula without hairs except on borders;hind basitarsus length 1.92 mm, width 0.8mm, with at least 8 setal comb rows evi-

dent; pollen press apparent and well deve-loped (figure 8). Basal vein distad cu-a by1.5 times vein width; stigma length 0.42 mm,width 0.12 mm; marginal cell of indeter-minate length (distal portion missing),0.36 mm wide. Hind wing with distal abs-cissa of vein M present, M gently curved.Scattered hairs evident on T6 and lateral

margins of T5. Sting length 1.76 mm,ramus length 0.72 mm.

Head and mesosoma dark brown to

black. Antennae brown. Legs light brown.T1 and T6 dark brown; T2 brown on basalhalf, apical half pale; T3 brown with api-cal margin pale; T4 with apical third pale;T5 brown with pale median patch.

3.1.3. Material

Holotype: worker female, MCZ Nr6316 (figure 1) and reverse of holotype(figure 2). Oligocene, Rott, Germany.Additional specimens: worker female,MCZ Nr 7513 (figure 3), Oligocene, Rott,Germany; holotype for subspecies A. hen-shawi dormiens, here considered a juniorsynonym of A. henshawi henshawi.

3.1.4. Preservation

The holotype and its counterpart arepreserved in profile (figures 1 and 2). Themouthparts are faintly evident and exten-ded below the head. The mandibles are

spread with the antennae extended paral-lel to the face just in front of them. Thehead is slightly turned so that the front ofthe face is seen obliquely. The holotypehas the wings extended away form thebody at an acute angle. The distal veinsare only faintly preserved, except theconnections of 1 m-cu and 2m-cu with the

submarginal cells are not visible. The fore-wings and hind wings are overlaid andvenation of the hind wing can be piecedtogether through the forewings. The basalportions of the legs are not preserved;however the tarsi and fragments of thelegs are evident below the body. Speci-men Nr 7513 is preserved with the dor-sum exposed (figure 3). The head is com-pressed dorso-ventrally with the leftantenna extended just in front of and awayfrom the head. The wings are extendedaway from the body to the sides with thevenation incompletely preserved, althoughthe venation is stronger in this specimenthan in any of the others (figure 6). Theleft hind leg sits along the side of the abdo-men and is turned so that the tibia-basi-tarsus junction is clear (figure 8).

3.1.5. Remarks

Zeuner and Manning [42] state that thebasal vein of A. henshawi is confluent with

cu-a, a comment which is clearly erro-neous when the holotype is examined(figures 5 and 11). This character was usedto distinguish between A. henshawi hen-shawi and their own A. henshawi dormienswhich they described as having the basalvein slightly distad of cu-a. Likewise, theabsence of eye hairs was used as a dia-

gnostic feature of A. henshawi dormiens(the presence of such hairs is a synapo-morphy of Apis), while in fact their spe-

cimen shows long eye hairs preserved onat least the left compound eye. In whole,both specimens have identical venation(figures 5 and 6) and structural characters,therefore the recognition of two subspe-cific forms is superfluous.

More recently, the errors discussedabove led Arillo et al. [2] to distinguish anew species of fossil Apis on the basis ofthis character. These authors distinguishedtheir species, A. aquisextana, by theslightly distal position of the basal vein.Their species is, in fact, no different fromA. henshawi and it is unfortunate that theconfusion begun by Zeuner and Manning[42] should mislead later workers. Indefense of Zeuner and Manning’s work,however, it must be noted that both ofthese authors had passed away many yearsbefore the final publication of their work(Professor Zeuner in 1963 and Dr Man-ning in 1966). Thus several errors, ofwhich only time and their unfortunatedeaths are to blame, may have accruedduring the intervening period.

Additional confusion stems from thefact that Arillo et al. [2] have failed to usevalid family-group names for bees. Forexample, these authors use the namesRophitidae and Sphecodinae in place ofHalictidae and Halictinae, and cite Miche-ner [23] for the usage. In actuality, Miche-ner [23] states clearly, even in his shortabstract, that the previous two names arenot to be used. Michener [24] later peti-tioned the International Commission on

Zoological Nomenclature for the correctusage of these names and the Commis-sion passed an opinion in agreement [18].Thus, the family-group names used byArillo et al. [2] are invalid and should notbe followed.

Lastly, Théobald’s [36] species A. cue-noti may also be a junior synonym of A. hen-shawi. However, far too little informationis available on this species to place it herewith confidence.

3.2. Apis vetustus Engel, new species

(Figures 4, 7 and 12)

3.2.1. Diagnosis

Basal vein linear, confluent with cu-a.Inner angle of third submarginal cell be-tween 2r-m and M nearly orthogonal,much greater than 45°; cell broader alongposterior border than anterior border. VeinM of hind wing gently curved.

3.2.2. Description

Total body length 15.9 mm; forewinglength 7.28 mm. Head length 2.72 mm,width 3.56 mm. Hypostoma length 1.72 mm,width 0.88 mm. Pubescence of head andmesosoma not apparent. Mesosoma width4.84 mm. Fore coxa wider than long; tro-chanter slightly longer than wide; remain-der of fore leg missing. Mid-coxa twiceas long as wide; trochanter and femur notpreserved; tibia length 1.76 mm; basitarsuslength 1.6 mm. Hind legs not preserved.Basal vein straight, confluent with cu-a(figures 7 and 12); stigma length 0.36 mm,width 0.14 mm; anterior border of first

submarginal cell along Rs 0.34 mm long;length of anterior border of second sub-marginal cell 0.28 mm, posterior border1.28 mm; length of anterior border of thirdsubmarginal cell 0.9 mm, posterior bor-der 0.98 mm, inner angle between 2r-mand M nearly orthogonal; marginal celllong and rounded at apex, length 1.56 mm,width 0.2 mm. Vein M of hind winggently curved, distal portion not preser-ved. Hairs not visible on apical sterna andlateral margins of T5.

Head and mesosoma dark brown.

Legs dark brown except tarsomeres 2-5light brown; claw dark brown. Sternapale brown except apical sternum darkbrown; lateral margins of terga darkbrown.

3.2.3. Type material

Holotype: worker female, MCZ Nr7514 (previously a paratype specimen forA. henshawi dormiens), Oligocene, Ger-many.

3.2.4. Preservation

The bee is preserved with the venterexposed (figure 4). The head is thrust for-ward exposing the hypostomal fossa andpostgena. The legs are only partially pre-served with most of the apical portionslost. The basal portion of the right wingis visible, while the left forewing is exten-ded and the venation faint but visible. Onlythe basal portion of the left hind wing isfaintly preserved below the forewing.There is debris, perhaps plant matter, justin front of the head.

3.2.5. Etymology

The specific epithet is the Latin wordvetustus meaning ’aged’ in reference tothe geological age of this species.

3.2.6. Remarks

This specimen was referred to by Coc-kerell (1907: 228) as possibly being aseparate species from the species he laterdescribed in the same paper as A. hen-shawi. He based this decision on the

straight basal vein. Cockerell also com-mented that there are "... dark spots at thesides of the abdominal segments...". Thedark spots Cockerell refers to are the lat-eral margins of the darker terga wrappingaround the metasoma to cover the lateral

margins of the sterna.

3.3. Apis miocenica Hong

Apis miocenica Hong, 1983, Bull. Tian-jin Inst. Geol. Min. Res., 8, 10.

Apis fota Zhang, 1989, Fossil insectsfrom Shanwang, Shandong, China, 323.New synonymy.

Apis shandongica Zhang, 1989, Fossil insects from Shanwang, Shandong, China,325. New synonymy.

3.3.1. Remarks

I have not had the opportunity to seethe holotypes of these species which arelocated at a small provincial museum inChina. However, the original descriptions,figures and photographs of the specimenshave been at my disposal and it is clearthat the species are not distinct. BothA. fota and A. shandongica are definedsolely on the basis of color differencesfrom A. miocenica. For example, the dif-ferences given by Zhang [43] for definingA. fota from A. miocenica are the darkercoloration of the hind tibia and metasoma,along with a broader width to the colorbands on the metasomal terga. A. similardiagnosis is given for A. shandongica.Such characters are known to vary withinextant species, even within a single colony,and are not useful for distinguishing Apisspecies. Zhang’s line drawings depictsome minor differences of wing venation;however, the photographs of the speci-mens show no differences at all. I, there-fore, have no trouble in placing these spe-cies under A. miocenica until the typescan be examined by a bee systematist andauthentic structural differences discov-

ered, should they exist.

Zhang [43], after redescribing A. mio-cenica, comments that this species is closelyrelated to A. mellifera and that the wingvenation of the two species is essentiallyidentical. The photograph provided by himof the holotype and the figures presentedby Hong [15], as part of the original des-cription, shows the basal vein distad of cu-a by about 2-3 times the width of a veinand a strong distal abscissa of vein M inthe hind wing (similar to figure 10). A. mel-lifera L. lacks the distal abscissa of vein Mand, like the other living species, has thebasal vein strongly distad of cu-a (e.g.figure 9). A. miocenica appears more clo-

sely related to A. henshawi than to A. mel-lifera or any of the other extant species.

A. longtibia Zhang [44], although alsodefined primarily on the basis of minorcolor differences from A. miocenica, pos-sibly has at least one apomorphy of the

wing venation that for the time beingallows it to retain its specific status. Thisspecies has the basal half of vein M in thehind wing strongly angulate, forming adistinctive point just after it branches fromM+Cu. This vein is gently curved in allother Apis species.

3.4. Apis petrefacta (Ríha),new combination

Synapis petrefacta Ríha, 1973, Vestn.Ústred ústavu geol., 48, 217.

3.4.1. Remarks

This species is from Oligocene depo-sits in the Ceské Stredhorí Mountains,Czech Republic. Based on both the des-cription of the species and the figures pre-sented by Ríha [27] this is a honey beespecies. Synapis Cockerell is a junior syno-nym of Apis and therefore this species isofficially placed within the genus. The sta-tus of this species will have to await futurestudy.

3.5. Apis (?) melisuga Zeunerand Manning, nomen dubium

’Apidae’ melisuga Handlirsch, 1907,Die fossilen Insekten und die Phylogenieder rezenten Formen, 893. Unavailablefollowing International Code of Zoologi-cal Nomenclature, 1985, 3rd ed., Art. 11h(iii).

Apis melisuga Zeuner and Manning,1976 (non Handlirsch, 1907), Bull. Brit.Mus. Nat. Hist. (Geol.), 27, 248.

3.5.1. Remarks

This fossil was mentioned by Hand-lirsch [13] simply as "’Apidae’ melisuga"in his seminal work on fossil insects. Thecomments given by Handlirsch, whichwere to constitute his description of thespecies, was that the specimen resembledA. mellifera. Since the name was not pub-lished in combination with any genericassignment nor a differential diagnosis itcannot be considered valid. Zeuner and

Manning [42], however, assigned meli-suga to Apis based on Handlirsch’s remark. Their publication of the epithet isthe first valid usage in combination with a

generic name and it must therefore bereferred to as A. melisuga Zeuner andManning (non Handlirsch). However, Zeu-ner and Manning’s description of the spe-cies was a simple regurgitation of Hand-lirsch’s comments, with the addition thatthe legs are suggestive of Apis. The wingsof the specimen were apparently not pre-served. There is no reason to believe, inthe absence of the type (the whereaboutsof which is unknown, and was so even toZeuner and Manning), that Handlirsch’sspecimen was indeed a honey bee. Thename A. melisuga should therefore beconsidered a nomen dubium, and, giventhe nature of the ’description’, perhapseven a nomen nudum.

4. DISCUSSION

The first person to place the fossilhoney bees into an explicit phylogeneticframework with the living species wasvon Buttel-Reepen [4]; however the fossilspecies he used in his study have all beenremoved from Apis. His species A. meli-ponoides (= Electrapis meliponoides) wasplaced as the most primitive ancestor ofthe lineage producing A. mellifera, whilethe other honey bee species were believedto have diverged prior to this in the middleEocene. A. meliponoides eventually gaveway to A. adamitica Heer (= Lithurgusadamiticus, a megachilid genus not evenremotely related to the apines) and ulti-mately A. mellifera. Statz [34] updatedvon Buttel-Reepen’s phylogeny correctlyplacing A. meliponoides in the 45 millionyear old Baltic amber genus Electrapis(after Cockerell [7]) and removing L. ada-miticus altogether. Statz kept the rela-tionships among the Apis species as wasproposed by von Buttel-Reepen and retai-ned E. meliponoides as ancestral to thelineage producing A. mellifera. Statz’s scheme, however, replaced A. dormitansas the immediate ancestor of A. mellifera,with his own new species A. kaschkei. He

considered A. dormitans and A. henshawito have branched from this lineage be-tween E. meliponoides and A. kaschkei inthe late Oligocene. Just over a half a cen-tury later, Ruttner et al. [3 1 ] and Ruttner[29] examined morphometric values ofwing venation for living and fossil honeybees along with their close relatives. Thesestudies produced compound clusters of

Bombus spp., A. cerana + A. mellifera,A. florea, and A. henshawi + A. armbrus-teri + A. dorsata. A. florea had an isolatedposition near the A. henshawi + A. arm-brusteri + A. dorsata cluster, with the nextnearest group being that of A. cerana +A. mellifera. This pattern is generally inaccord with recent examinations of Apisphylogeny [1, 10] as well as the results

discussed below. Interestingly, the singlespecies of Electrapis examined (presu-mably E. minuta) took a position nearest toBombus. The overall conclusions of thesestudies were of an elongation of venationtowards the apex and the proximal migra-tion of 2r-m along Rs (see figure 9), butthat in general Apis wing venation had notchanged drastically since the Miocene.Most recently Hong and Miao [ 17] attemp-ted to explain honey bee evolution in thelight of the Jurassic fossil, Palaeapis bei-boziensis [16]. Palaeapis, however, is nota primitive honey bee nor even a bee atall, but instead an aculeate wasp (see alsoMichener [25]) and can shed no light ontoearly bee history.

It is difficult to place any of the fossilspecies into Apis phylogeny due to thelack of information for most charactersneeded to perform a comprehensive cla-distic analysis. Honey bees are fairlyhomogeneous and in the absence of infor-mation on the males, nesting biology, etc.,it is not possible to include the fossils in ameaningful cladistic study with the extantspecies. Despite this trouble, some infor-mation can be gleaned from the little dataavailable. A hypothesis of relationships

among the honey bees is presented infigure 13. The polarity of characters forthe following outline of relationships wasdetermined by comparing those states pre-sent in the living and fossil honey bees tothe only other representative of the tribeApini, namely the genus Electrapis, and tothe Meliponini, sister tribe to the Apini[5, 32]. The extant species of honey bees(see table I) are here considered to consti-tute a monophyletic group, with relation-ships among them derived from a recent’total evidence’ analysis of Apis phylo-geny [10] corroborating those relation-ships presented by Alexander [1]. Thismonophyly is based upon the sharing ofa less than 45° angle between veins 2r-mand M in the forewing (figure 9) as des-cribed by Alexander (1991: his angleBDE). The closest apparent relative of themodern species is A. armbrusteri Zeunerwhich shares the strongly distad basal veinrelative to cu-a (similar to that seen infigure 9). It is set outside of the clade ofliving species by the greater than 45° anglebetween 2r-m and M. A. vetustus is appa-rently the most plesiomorphic of theknown fossils owing to the confluence ofcu-a with the basal vein and the linear

basal vein (figure 12: similar to that statefound in Electrapis). The remaining spe-cies fall intermediate between A. vetustusand A. armbrusteri. The basal vein in all ofthese species is gently curved and offsetfrom cu-a by 1.5-2 times the vein’s width(similar to figure 11). Based on the cur-rent information, it is not possible toresolve relationships among these five spe-cies. All of the fossil species, for whichdata exist, have the distal abscissa of veinM in the hind wing, a feature correctlydetermined by Alexander [1] to be primi-tive within Apis. I have not been able toplace A. catanensis Roussy [28] in thescheme described above or to determinethe validity of this fossil as a species ofApis. This specimen will have to awaitfuture study.

All of the fossil species of the genuswere likely to have been highly eusocial.A cladistic reconstruction of this behavioron apine phylogeny supports a single ori-gin of advanced eusociality in the ancestorof Apini and Meliponini [5, 32]. Thuseusociality is a primitive character of thehoney bees and their ancestor would havealready been living in such societies. Addi-tionally, the known fossil specimens are allmorphologically suggestive of workers,supporting the notion that these specieswere eusocial (a characteristic also seenin fossils of the sister genus Electrapis:[9]). It is not possible to determine whetherany of the fossil species would have hadthe familiar ’waggle dance’ language thatis present among the species of today. Thischaracter may have arisen in the commonancestor of the living species only, or havebeen present in a few or all of the fossilspecies as well. The primitive nesting bio-logy of the living species was to constructa comb in the open. It is therefore logicalto conclude that the fossil species knowntoday were open-nesting as well; however,this may never be known with certainty.

It is likely that Apis arose sometime inthe early Oligocene. Extending one of the

conclusions of Ruttner et al. [31] and Rutt-ner [29] back an epoch, it appears as

though Apis wing venation has changedrelatively little since the middle Oligo-cene. The general vein patterns are remark-ably similar from species occurring in Oli-gocene strata to those of today (e.g.compare figures 9, 1 1 and 12). Apis diver-sity appears not to have changed muchthrough time as was suggested by Culliney[8] who regarded the genus as having lostdiversity since the Oligocene. If anything,the crude evidence available suggests thatApis diversity has slightly increased asonly three species are currently knownfrom the Oligocene, followed by anotherfive species from the Miocene (not inclu-ding A. melisuga), eventually leading up tothe six species recognized today.

ACKNOWLEDGMENTS

Special thanks are due to G. Chavarría (for-merly of the MCZ), S Cover, and P. Perkins(both of the MCZ) for help during my visits totheir collection. My advisor, J.K. Liebherr,kindly provided access to a camera-micro-scope mount for production of the figures pre-sented in this work. The late W.L. Brown Jr

(1922-1997) aided in the difficult interpretationof A. melisuga’s taxonomic status, he is gra-tefully acknowledged and dearly missed. I amindebted to M. Wang, Boston University andthe MCZ, for graciously translating Chinesepapers on fossil insects for me. I am grateful toP. Ríha for sending me original copies of hiswork on tertiary insects, and to D. Ren andY.C. Hong for original copies of work on thefossil insect fauna of China. I am also thankfulto G.W. Otis for allowing me to examine spe-cimens of A. nuluensis, at which time I failed tofind characters to support it under a phyloge-netic species concept and thus have not inclu-ded it in my table of Apis species. I am furtherindebted to G. Chavarría and two anonymousreviewers for reading an earlier version of thepaper. Their valuable insights helped toimprove this study. Support for this researchwas provided by a National Science Founda-tion Predoctoral Fellowship. This work is dedi-cated in loving memory of B.A. Alexander(1952-1996), a dear friend and mentor. Byron’s

work on honey bee phylogeny was one of myfirst introductions to systematics, and his inter-est in me, even though I was a student of che-mistry and cell biology, forever changed mylife. He is sorely missed.

Résumé - Les abeilles mellifères fossileset l’évolution dans le genre Apis (Hyme-noptera, Apidae). La première abeillemellifère, Apis henshawi, est décrite entiè-rement pour la première fois et les spéci-mens de l’empreinte et de la contre-empreinte de l’holotype et du paratypesont illustrés. En outre une nouvelle espèced’abeille mellifère, A. vetustus n. sp., pro-venant de l’Oligocène d’Allemagne estdécrite et illustrée. A. henshawi dormienset A. aquisextana sont considérés commede nouveaux synonymes de A. henshawi,tandis que A. fota et A. shandongica sontconsidérés comme synonymes de A. mio-cenica. Synapis petrefacta est officielle-ment transferré dans le genre Apis. Zeuneret Manning (et non Handlirsch) sontreconnus comme les auteurs de A. meli-

suga, le nom étant considéré comme unnomen dubium. L’analyse comparative dela vénation alaire est utilisée pour inclureles abeilles mellifères fossiles dans uncadre phylogénétique qui comprend lesespèces vivantes. On considère ici que lesespèces vivantes forment un groupe mono-phylétique. D’après ces résultats les taxonséteints forment un groupe paraphylétiquequi conduit à un clade des espèces exis-tantes avec A. armbrusteri, qui représentele fossile le plus apparenté à la faunemoderne. Le genre semble avoir acquisune diversité depuis son origine dansl’Oligocène inférieur. On résume briève-ment la diversité du genre Apis qui com-prend 14 espèces vivantes et éteintes,considérées sous toutes réserves commevalides. © Inra/DIB/AGIB/Elsevier, Paris

Apis / Apoidea / Cénozoïque / paléon-tologie / fossile / systématique / phylo-genèse

Zusammenfassung - Fossile Honig-bienen und Evolution in der GattungApis (Hymenoptera: Apidae). Die erstefossile Honigbiene, Apis henshawi, wirderstmalig genau beschrieben und Exem-plare des Holotypus und Paratypus wer-den vorder - und rückseitig abgebildet.Weiterhin wird eine neue fossile Honig-biene aus dem Oligozän in Deutschlandals A. vetustus (neue Art) beschriebenund abgebildet. A. henshawi dormiensund A. aquisextana werden neuerdingsals jüngstgenannte Synonyme von A. hen-shawi angesehen, während A. fota undA. shandongica als jüngstgenannte Syno-nyme von A. miocenia eingestuft wer-den. Synapis petrefacta wird offiziell indie Gattung Apis übernommen. Die Auto-renschaft von A. melisuga wird richtigals Zeuner und Manning festgesetzt (nichtHandlirsch), der Name wird als einnomen dubium angesehen. Unter Ver-wendung von Vergleichsdaten der Flü-geladerung werden die fossilen Honig-bienen in einen phylogenetischenRahmen eingeordnet, der auch die leben-den Arten enthält. Hierbei wird ange-nommen, dass die rezenten Arten eine

monophyletische Gruppe bilden. Die aus-gestorbenen Taxa sind nach diesenBefunden ein paraphyletischer Zusam-menschluss , die zu den cladus der be-stehenden Arten hinführt. Hierbei stellt

A. armbrusteri das zu der modernen Bie-nenfauna nächstverwandte Fossil dar. Die

Vielfalt der Gattung scheint seit ihremUrsprung im frühen Oligozän zugenom-men zu haben. Es wird eine kurze

Zusammenfassung der Vielfalt von Apismit den 14 vorläufig als gültig angese-henen lebenden und ausgestorbenenArten gegeben. © Inra/DIB/AGIB/Else-

vier, Paris

Apis / Apoidea / Zenozoisch / Paläonto-logie / Taxonomie / Phylogenese

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