Systematics, phylogeny and biogeography of the Meliponinae (, ): a mini-review Jmf de Camargo, Sr de Menezes Pedro

To cite this version:

Jmf de Camargo, Sr de Menezes Pedro. Systematics, phylogeny and biogeography of the Meliponinae (Hymenoptera, Apidae): a mini-review. Apidologie, Springer Verlag, 1992, 23 (6), pp.509-522. ￿hal- 00891046￿

HAL Id: hal-00891046 https://hal.archives-ouvertes.fr/hal-00891046 Submitted on 1 Jan 1992

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Review article

Systematics, phylogeny and biogeography of the Meliponinae (Hymenoptera, Apidae): a mini-review

JMF de Camargo, SR de Menezes Pedro

Departamento de Biologia da Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901, Ribeirão Preto, SP, Brazil

(Received 15 November 1991; accepted 10 July 1992)

Summary — The main proposals for systematics, phylogeny and biogeography of the Meliponi- nae, and the polarity and significance of some morphological characters are discussed. Although a set of probable synapomorphies is suggestive of the Meliponinae as a co-phyletic group with the Ap- inae, Bombinae and Euglossinae, the relationships with these subfamilies remain unclear. The dis- tributional pattern and fossil record are indicative of greater antiquity for the Meliponinae and sug- gestive of an independent origin or an early divergence from a proto-other Apidae branch. The sister-group relationship between Malayan and neotropical Meliponinae (Tetragona-Tetragonisca line and possibly Trigonisca-Pariotrigona, Lisotrigona), and the probable relationship between Aus- troplebeia and the neotropical line, are suggestive of a West-Gondwanan origin for the Meli- poninae, with 2 main dispersal routes via the holarctic and panaustral regions. systematics / biogeography / Apidae / Meliponinae / phylogeny

ON THE RELATIONSHIPS OF THE rather than excavated in the substrate - MELIPONINAE AND OTHER APIDAE as possible synapomorphies, in addition to the well known corbicula and rastellum Sakagami and Michener (1987) and Mi- (present in females, except in parasitic chener (1990) presented strong argu- and cleptobiotic forms and in queens of ments in favor of the hypothesis that the the highly eusocial groups). Michener Meliponinae (M), (A), Bombinae (1990) also included other possible synap- (B) and Euglossinae (E) constitute a ho- omorphies (hind basitarsus of female ar- lophyletic clade, the probable sister-group ticulated near anterior end of apex of tibia, of the Xylocopinae. They included certain reduced maxillary palpus, 1- or 2- seg- characters - absence of basitibial and py- mented), and other characters, such as gidial plates and nests usually constructed form and type of cephalic and thoracic sal- in large or irregular cavities, cells built up ivary glands and hypopharyngeal glands (see also Cruz-Landim, 1967), and com- Winston (1979), in a study of the mouth- mented that this association of character parts, suggested a relationship between M states is an indication "that the 4 subfami- and the Xylocopinae, or an early divergence lies of Apidae are related to one another, of M from the other Apidae. Plant and Pau- ie, that no one of them is an anthophorid lus (1987) considered E as the oldest group that has convergently evolved the branch, a sister-group of the other Apidae. external features of Apidae". Despite these Michener (1990) presented 5 of the 15 pos- deductions, Michener (1990) did not ex- sibilities of relationship among the 4 taxa; clude the possibility that the main charac- he considered the cladograms where M-A teristic of the Apidae, the complex pollen- appears as a sister-group of B-E, and E as manipulating behavior and associated a sister-group of B, A-M more probable: structures, could have arisen independent- however, from the biogeograhic point of ly in 2 or more of the groups included in view and possible greater antiquity of M, he the Apidae, considering the distinctive me- also considered reasonable the cladograms chanical and morphological solutions they where this taxa appears as a sister-group of present (rastellum and auricula in A and B, E, B and A. Prentice (1991) suggested E rastellum or posterior parapenicillum and and B as older branches and A-M as sister- penicillum in M, and an auricula-like struc- groups (as originally proposed by Michener, ture in E; cf Michener et al, 1978; Wille, 1944). 1979a). Even the corbicula (a bare or In recent papers, based on mitochondrial sparsely haired area on the outer surface and ribosomal DNA sequences, Cameron on the hind tibia, used for the transport of (1991) and Sheppard and McPheron (1991) both sticky material for nest construction proposed the Meliponinae and Bombinae and pollen), the principal synapomorphy, as sister-groups. Although this refined me- and one that, in the opinion of Michener et thodological approach may constitute a val- al (1978), precedes the origin of the highly uable tool for and systematics, derived pollen-manipulating behavior and the number of Apidae and non-Apidae associated structures, is not an exclusive presently analysed is too small to allow in- attribute of the Apidae. A corbicular struc- ference of phylogenetic relationships. ture also occurs in Canephorula apiformis, As previously pointed out by Camargo an Anthophorinae from Argentina (cf (1989), none of the propositions on phylo- Friese, 1920; Michener et al, 1955). Some genetic relationships of the Meliponinae of the other possible synapomorphies sug- with the other Apidae considered congruity gested by Sakagami and Michener (1987) with the biogeographic patterns, apart from and Michener (1990), ie absence of basiti- some considerations presented by Michen- bial and pygidial plates and reduced maxil- er (1990:82). M is widely distributed, rang- lary palpus indicate loss and may occur in- ing through the pantropical and southern dependently as in some other Apoidea. subtropical regions (cf Moure, 1961); the Although the set of characters considered neotropical region, Africa, south of the Sa- here is more indicative of holophyly for the hara, Madagascar, the Malayan region, s Apidae, the situation becomes more com- lat including the islands on the east of the plex when one searches for the synapo- Wallace’s line (New Guinea, Sakagami et morphies indicative of relationships among al, 1990), the eastern Indian subcontinent, the 4 taxa, as verified by the different pro- New Guinea, and northeastern Australia, posals of phylogeny. Winston and Michen- with several hundred and many er (1977) and Kimsey (1984) suggested M supra-specific taxa (21 recent genera, ac- as the sister-group of the other Apidae; cording to Michener 1990; and 54 accord- ing to Camargo 1989, besides 3 extinct Michener, 1990), with a few species reach- genera). This distribution pattern and the ing South America (probably a not very an- antiquity (the oldest known fossil, Trig- cient migration; cf Simpson and Neff, 1985) ona prisca from late Cretaceous New Jer- and mountain areas in the south of the Him- sey - USA amber, 96-74 mya, is very sim- alayas. In Africa, it ranges up to the North- ilar to the recent species of s str ern Sahara - fossil forms attributed to the from the neotropics; cf Michener and Gri- genus Bombus have been recorded from maldi, 1988a,b; Grimaldi et al, 1989) sug- the Oligocene-Miocene in palearctic and gest that M is an ancient group, possibly nearctic regions (Zeuner and Manning, Gondwanan (see item Origin, phylogeny 1976). A relationship with a proto-Bombinae and biogeography), 100-130 mya old (Mi- branch is possible if the origin of the Meli- chener, 1979; Camargo and Wittmann, poninae in the Laurasian continent is con- 1989 respectively). The other taxa seem to sidered, as suggested by Michener (1990). be more recent (Michener, 1990), except It is clear that the Apidae complex still possibly B. E is limited to the neotropics remains an incognita. The geographic vi- (basically in tropical areas), and is presum- cariance patterns and fossil record, howev- ably post-Gondwanan. A is a typical Indo- er, support the hypothesis of greater antiq- Malayan group. Amongst the 9 recent spe- uity for M compared with A, B and E, and cies admitted (cf Michener, 1990; see also that M presents a considerably remote re- comments by Alexander, 1991), only 1 oc- lationship, or possibly no direct relationship curs in Eurasia and Africa and another in with the other Apidae. Indo-Malaya and east Asia, the other spe- cies, including the most conservative forms (the dorsata and florea complex; Camargo, The Meliponinae tribes 1972; Ruttner, 1988; Alexander, 1991) are found in the Indo-Malayan region up to Moure (1946, 1951) divided the Meliponi- Timor. Representatives of A are absent in nae into the tribes Meliponini Börner 1919 New Guinea and Australia (cf Ruttner, (genus Melipona), Lestrimelittini Moure 1988; Michener, 1990). Fossil records from 1946 (genus Lestrimelitta, maintaining Oligocene-Miocene Europe indicate forms Cleptotrigona apart, since he did not know that are apparently related to the A mellife- it de visu) and Trigonini Moure 1946 (the ra group according to Zeuner and Manning remaining genera). Moure (1961:183; (1976); on the basis of forewing morpho- Moure et al, 1958:491) suppressed the metric analysis of Synapis and Apis arm- Lestrimelittini, incorporating the genus into brusteri, Ruttner (1988) suggested approxi- the Trigonini. mation with the Apis dorsata group. Such The genus Melipona is exclusively neo- taxonomic and distributional patterns might tropical and, according to Moure (1951), a indicate that A is less ancient than M (cf post-Gondwanan derivative group and so Michener, 1990), and evolved well after more recent than the main lines of the Meli- the breakup of Gondwana (cf Roubik, poninae. Moure (1951, 1961) and Wille 1989), possibly after formation of the Him- (1979b) admitted a cleavage line between alayas (it could be hypothesized that Apis the Plebeia line and Melipona. In the clado- evolved in isolation in the Indian subconti- gram presented by Michener (1990; fig 6), nent while it was still an island!). Thus, a Melipona arises isolated at the base as a direct derivation of M from the A or E sister-group of the other Meliponinae; how- branch is quite unlikely. B is holarctic (ca ever, this author recognized (p 92) that this 250 morphologically homogeneous spp; cf genus is reasonably closely related to Ple- beia. Michener (1990:112) suggested the line, and Sakagamilla, a monotypic genus, suppression of tribal status for Melipona. here considered as synonymous with Scaptotrigona, since it shows all the autap- omorphies of the latter without enough rel- The Meliponinae genera evant discontinuity to be recognized as an independent clade. The outline of modern systematics of the Finally, Michener (1990) suggested for Meliponinae began with the monumental re- the entire world 21 genera and 17 subgen- vision made by Schwarz (mainly 1932, era (one of them new, Papuatrigona Mi- 1948) and the comprehensive synthesis by chener et Sakagami, included in Trigona), Moure (1951, 1961). A critical revision was and made synonymous 19 of the general presented by Wille (1979b), and some com- admitted by Moure (table I). ments were made by Camargo (1989). Re- For the fossil forms, the genera Kelneri- cently, a detailed and comprehensive paper apis Sakagami, 1978 (= Kelnermelia was published by Michener (1990), taking Moure in Moure and Camargo, 1978), type into account unknown characters or those species Trigona (Hypotrigona) eocenica not much explored by other authors. Keiner-Pillaut, from the later Eocene Baltic 1982 Schwarz (1948) recognized 3 genera for amber, Proplebeia Michener type the entire world (Melipona, Lestrimelitta and species, Trigona (Liotrigona) dominicana Trigona, including 18 subgenera). He main- Wille et Chandler, presumably from the Oli- ly studied the neotropical and Indo-Malayan gocene amber, Dominican Republic, and fauna. For the neotropical region, Moure Meliponorytes Tosi 1896, type species Me- Miocene (1951) proposed 12 genera and 19 subgen- liponorytes succini Tosi, from the era. In 1961, when he reviewed the old Sicilian amber, have been described. world Meliponinae, he recognized 13 gene- Trigona prisca Michener and Grimaldi, ra for the Indo-Malayan and Australian re- the oldest fossil described up to now, 96- gions, 10 for the Ethiopian region and 11 74 mya, from Cretaceous New Jersey genera and 24 subgenera for the neotrop- (USA) amber, was considered to be direct- ics. Finally, in a short note, Moure (1971) ly related to Trigona (s str) an extant neo- proposed an identical approach to that of tropical genus (Michener and Grimaldi, the old world Meliponinae, elevating all sub- 1988a,b). Such a taxonomic position, how- genera to generic status. This position was ever, is dubious (cf Camargo and Witt- reasserted more categorically by Camargo mann, 1989; Michener, 1990:106). Com- and Moure (1988) and Camargo (1989). ments on other fossils of recent genera, Wille (1979b) centered his criticisms and some others which had not been com- Zeuner mainly on Moure’s view, and pointed out a pletely studied, were provided by Wille Moure new systematic arrangement for the sub- and Manning (1976), (1977), Michener family (8 genera and 14 subgenera, mak- and Camargo (1978) and (1990). ing synonymous 30 of the subgenera ad- mitted by Moure). PHYLOGENY and Moure ORIGIN, Camargo (1983) proposed AND BIOGEOGRAPHY the for an aberrant genus Trichotrigona OF THE MELIPONINAE form of Meliponinae found in the Amazon. Moure (1989a,b) described Camargoia for pilicornis Ducke and camargoi Moure, 2 di- The greatest Meliponinae diversity is found vergent forms of the neotropical Tetragona in the neotropics (30 supra-specific taxa and > 300 described forms) and Indo- Malayan regions (14 supra-specific taxa and ca 60 forms). In Africa (10 supra- specific taxa and ca 50 forms), Madagas- car (1 supra-specific taxon and 4 forms), Australia (2, 8-10) and New Guinea (4, 5), the diversity is much lower. In this taxon the continental disjunctions are unique within the Apoidea (Michener, 1979), as a result of which a very complex history of vicariance events and great an- tiquity is presumed. However, there are some obscure points in the taxonomic structure that do not permit a complete re- construction of the phylogeny of the group. There have been few proposals on the phylogeny (cf Moure, 1951, 1961; Wille, 1979b). Michener (1990) presented a clad- istic approach suggesting that the Melipon- inae originated in North America (West Laurasia); nevertheless, there is a certain difficulty in accepting the model, in view of some taxonomic problems. To analyze the hypothesis on the geo- state. In the fossil forms, it is present in T grahic origin of the Meliponinae and the prisca (Michener and Grimaldi, 1988a) possible sequence of events determining from the nearctic region and in Tetragonu- the present disjunction pattern, it is neces- la devicta from Burma (cf Kerr and Maule, sary to first clarify some questions on the 1964; Wille, 1977; Moure and Camargo, relationships among the taxa: which 1978). This grouping as proposed by groups can be recognized as sister- moure (1961), was regarded by Michener groups? as a single genus, Trigona, from which and were Moure (1951, 1961) proposed at least 3 only Oxytrigona Cephalotrigona considered as main phyletic lines, Tetragonisca- excluded, being specialized associated to the clade. He also Tetragona, Plebeia and Hypotrigona, genera excluded which, in of present in several continents, based princi- Dactylurina, spite this character state and others pally on the character form of the micropi- presenting in common with the line lose structure (= keirotrichia; Michener, Trigona (eg plu- mose hairs the of 1990) of the inner surface of the hind tibia along posterior margin the hind and an area in the hind basi- of the workers. tibia, tarsus of D staudingeri, similar to the seri- ceous area of the Trigona), is considered The Tetragonisca-Tetragona line by Michener (1990), to be closely related to Plebeina, another phyletic line from Afri- ca, based on the male and worker gonos- character Michener (1990: 87, 4), ques- tylus form and male gonocoxyte. tioned the polarity of this character state. Other such as the sericeous However, he considered elevated and nar- characters, area on the base of the inner surface of row keirotrichia, restricted to the median the hind basitarsus of the worker (a well longitudinal band, leaving a broad bare (or defined area of dense place with sparse bristles) depressed posterior micropilosity), the groups of (sen- as an apomorphic state (Moure, Indo-Malayan Trigona margin, Homo- personal communication) consider it primi- su lato) line, except Lepidotrigona, and directly as a sis- tive or plesiomorphic), and suggested the trigona Papuatrigona, ter-group of and Trigona (s Malayan Trigona (sensu Michener) as a Tetragonisca from the sister-group of the neotropical Trigona. str) neotropical region. However, this character can be for This character state is present in Trigona plesiomorphic A sericeous area is also (s str), Tetragona, Frieseomelitta, Geotrig- Trigona (s lat). present in the fossil T prisca. In addition to ona, Duckeola, Tetragonisca, Ptilotrigona, this character, La- Trichotrigona, Camargoia, Oxytrigona and treille has a structure as the 8th from the neotropical region interpreted Cephalotrigona metasomal sternum in and in Homotrigona, Heterotrigona, Platy- (Camargo, litt), which also indicates a con- Tetra- plesiomorphic trigona, Lophotrigona, Tetragonula, dition. gonilla, Geniotrigona, Odontotrigona, Tetri- gona, Trigonella and Papuatrigona from the and the eastern Indian Malayan region The Plebeia line subcontinent (Platytrigona ranges as far as New Guinea; Tetragonula ranges as far as the Solomon Islands, Caroline Islands, This line is poorly defined and the relations New Guinea and northeastern Australia; among included taxa are obscure and Papuatrigona is restricted to New Guinea). doubtful. According to Moure (1951), this In Africa, only Dactylurina presents such a line includes the groups that have enlarged keirotrichia, leaving only a narrow posterior acters linking the African forms (including margin, depressed or not. They are as fol- Dactylurina and Plebeina) with the excep- lows: from the neotropical region, Plebeia tion of Hypotrigona, are the gonostyli in (s str), Mourella, Friesella, Schwarziana, workers, enlarged and diverging apically and the associated genera Melipona, and covered with micropilosity. Michener Scaura, Schwarzula, Partamona, Parapar- (1990:88, characters 11, 12, 13) consid- tamona and Nogueirapis, and possibly ered the worker gonostyli to be well separ- more remotely derived Paratrigona- ated at the base, converging apically and Aparatrigona and Nannotrigona- covered with abundant long bristles and Scaptotrigona; from the Ethiopian region, with absence of micropilosity, as plesio- Plebeina, Plebeiella and Meliplebeia, and morphic states. We are of the opinion that from Australia and New Guinea, Austrople- the polarity of the latter character (0 = mi- beia. Michener (1990) nevertheless, did cropilosity absent; 1 = present), is improba- not consider these African and Australian ble. If it is considered that reduced sting taxa as sister-groups of the neotropical without biological function is not subjected groups; for the African forms he suggested to selective pressure at least theoretically, a relationship with neotropical Trigonisca it therefore should not acquired new attrib- (s lat) and Hypotrigona from Africa. Mi- utes only to suffer reduction or loss of chener had good reasons for excluding structures (unless it is supposed that re- some African groups from a direct relation- duction of the sting occurred at least twice ship with Plebeia. Loss of the rastellum independently in ancestors of the Meliponi- and presence of a well-developed posteri- nae). In this way, bristles and micropilosity or parapenicillum are clear synapomor- would appear in combination in the ances- phies linking Meliponula, Plebeiella, Meli- tor (loss of micropilosity and bristles might plebeia, Axestotrigona and Apotrigona occur independently). This combination as- without corresponding forms in other conti- sociation to cylindrical and convergent go- nents, so that he considered them to be- nostyli, in our view, occurs in Trigonisca, (s long to a single genus: Meliponula. The in- lat, cf Michener, 1990; figs 38, 39), from clusion of Hypotrigona-Liotrigona in this the neotropical region, and indicates an clade seems logical, since the modifica- approximation to Plebeina, if it is also con- tions in the rastellum (soft hairs) and pos- sidered that both have a well developed terior parapenicillum, are similar to that of and functional rastellum. Although the rela- Meliponula (sensu Michener). On the other tionships between the African and neotrop- hand, contrary to Michener’s interpreta- ical taxa are still unclear, Michener (1990) a be- tions, Plebeina presents a functional and also recognized closer relationship than with other tax- well developed rastellum and an undevel- tween them, rather any oped parapenicillum, exactly like those of on from other continents. Plebeia (s str). Unless this character (ras- Among the neotropical taxa associated tellum) arose by reversion or de novo with the Plebeia line certain problems also (which is perfectly possible, since it is only arise. According to the characters consid- a comb of modified setae), such a feature ered by Michener (1990), Melipona arises could indicate a relationship between Ple- at the base as an isolated branch, a sister- beina and neotropical forms (Michener group of the other Meliponinae. The acute codified rastellum as weak or absent in submarginal angle in the forewing consti- Plebeina, Austroplebeia, Dactylurina and tutes the main synapomorphy that separ- Trigonisca s lat; nevertheless, it is present ates Melipona from the Plebeia branch and and functional in all of them). Other char- associated taxa; this, however, is a difficult character to codify. An acute angle (= 75°) spatha, even Michener (1990) recognized occurs in some species of Paratrigona (an- an approximation to neotropical forms. Fur- other plesiomorphic character in this ge- thermore, other characters such as un- nus is the presence of the 2 submarginal modified pregenital sterna and the 6th met- cells, which are very well delimited in asomal sternum with a median apical some species; cf Camargo and Moure, process in males, general body form, trian- 1992), while in Melipona, in some forms of gular hind tibia, enlarged keirotrichia, and the marginata group, this angle is practi- rastellum present in workers are sugges- cally at a right angle (85-90°). Some tive of a relationship with the neotropical doubts about the form of the male genital Plebeia line, primarily Mourella. It is less capsule (rectigonal, schizogonal) also re- probable that such a combination of char- main, eg the schizogonal condition of Meli- acter states, even if they are considered as pona also appears, according to Michener plesiomorphic states, is present in unrelat- (1990) in some other taxa such as Nannot- ed taxa (see also Camargo and Wittmann, rigona. Reevaluation of these characters 1989) or arises convergently, as suggest- could bring Melipona much nearer the Ple- ed by Michener (1990:104); there is no beia branch, or even place it as a deriva- known determinant factor of convergence tive group of the Plebeia stock. On the oth- for such a set of characters. With refer- er hand, Plebeia (s str), even taking into ence to the sting structure of Austrople- account some of the characters consid- beia, cylindrical gonostylus, covered with ered by Michener (1990), seems to be a micropilosity and setae (or bristles) are derivative form. For example, the median plesiomorphic states and are also present apical process of the 6th metasomal ster- in neotropical forms (Trigonisca). In fact, in num of the male (a plesiomorphic state, cf our opinion Austroplebeia does not share Michener, 1990:88), present in most of the apomorphies with any other taxa, but ex- other taxa, including Mourella (considered hibits a series of plesiomorphic states, re- forms rather than Af- synonymous with Plebeia s str by Michen- sembling neotropical rican forms. er, 1990), is absent in Plebeia (s str). Moreover, Mourella exhibits a set of other Fossils related to Plebeia (s str) have bionomic characters associated with sub- been described from the Oligocene Amber, terranean nesting habits (simple nest en- Chiapas, Mexico (Nogueirapis silacea trance, not delimited by resin or cerumen, Wille, 1959) and from the Oligocene Am- gallery between the surface and the nest ber of the Dominican Republic (Proplebeia not lined with cerumen, listed among oth- dominicana; cf Michener, 1982). ers by Camargo and Wittmann, 1989), considered by us as plesiomorphic states. The line For Austroplebeia, the problems are Hypotrigona just as numerous. In the cladograms of Mi- chener (1990), it appears related to deriva- This line includes Hypotrigona (s str) and tive African forms, mainly because of the Liotrigona from Africa, Trigonisca, Leurotri- way in which the characters were codified, gona, Celetrigona and Dolichotrigona from particularly the main synapomorphy, ras- the neotropical region, and Pariotrigona tellum absent. On the contrary, Austrople- and Lisotrigona from Indo-Malaya. These beia has a well developed and functional are the smallest Meliponinae known (ca rastellum, as in neotropical Plebeia (s str). 2.0 mm) and, according to Moure (1961), Taking into account male genital charac- most of the characters considered could in- ters, with the exception of the absence of dicate convergence associated with reduc- tion in body size rather than phylogenetic tionships between Trigonisca (s lat) and Li- relatonships. In Michener’s cladograms sotrigona and Pariotrigona. they appear as related taxa, with the ex- - Between the neotropical region and Aus- of to Michen- ception Liotrigona. According tralia and New Guinea, there is no defined er the malar (1990), long space, nearly sister-group, but indications of a close rela- right-angled submarginal angle and bris- tionship between the Plebeia line and Aus- tles arranged in successive transversal troplebeia exist. rows on the inner surface of the hind basi- - Between the African and Malayan re- tarsus of Pariotrigona suggest some spe- do not occur. There cies of the neotropical Trigonisca (s lat). gions, sister-groups are indications of a be- Males of Pariotrigona which might corrobo- only relationship tween Hypotrigona and Pariotrigona. In the rate or refute such a relationship, are not there are no forms related known. Malayan region to the Plebeia line. Between Africa and related to Fossils, possibly Hypotrigona Australia, there is no sister group. (s lat), have been described from the Eo- - From the Malayan taxa, 3 genera occur cene Baltic Amber eocenica; (Kelneriapis in New Guinea and 1 in Australia. cf Moure and Camargo, 1978; Sakagami, only occurs in New Guinea and from the East African Austroplebeia only 1978) Copal and Australia. (Hypotrigona gribodor, cf Wille, 1977). Liot- rigona vetula was described by Moure and The hypothesis suggested by Michener Camargo (1978) from a Copal piece of un- (1990) of an origin in North America (West known age and origin. Laurasia) seems well sustained in his cla- dograms (figs 6, 7, 8) and in the fossil An of all taxa, into ac- analysis taking record He that the count the biogeographic regions, allows (T prisca). suggested vicariance in the Meliponi- the following relationships to be suggest- present pattern nae results from a distribution ed: throughout the holarctic region which took place when

- Between neotropical and African regions this area was warmer. He considered the there are no defined sister-groups, but indi- discontinuity between the neotropical and cations of possible relationships among Ple- African fauna as indicative that the Meli- beina, Plebeia line and Trigonisca (s lat) poninae from North America reached and between Hypotrigona and Trigonisca (s South America after considerable separa- lat), as suggested by a still confused combi- tion between the latter and Africa, and that nation of plesiomorphies and apomorphies. the African fauna evolved when Africa was The conspicuous divergence of the remain- substantially isolated from American and ing African taxa and the absence of repre- Eurasian invasions. On the other hand, the sentatives from the Tetragonisca- indication of a relationship between Austro- Tetragona line (except possibly Dactylurina plebeia from Australia and the Plebeia line as a relict form) in Africa indicate, according from the neotropical region rather than with to Michener (1990:97), that the African fau- African forms, and the absence of forms na have evolved in substantial isola- must related to this group in the Indo-Malayan tion from African and Eurasian invasions. region, are suggestive of a panaustral mi- - Between the neotropical and Malayan re- gration route via Antarctica (Camargo, gions, the relationships are more clearly 1989; Camargo and Wittmann, 1989). This defined by the presence of sister groups pattern is indicative of the presence of the from the Tetragonisca-Tetragona line Meliponinae in Southern South America; at (Trigona s lat) and also by possible rela- least between the Upper Cretaceous and the Early Tertiary. Also, the presence of India, in isolation for a long period (cf lit- Plebeia line forms restricted to southern erature in Patterson and Owen, 1991) pos- Brazil, especially Mourella, as previously sibly did not participate in the dispersal of discussed, suggests the origin of this the Meliponinae, and was invaded later by group (Plebeia line) in the southern south- Malayan Trigona (s lat) (this would explain American cratons (Camargo, 1989, 1990; the presence of only about 5 species on Camargo and Wittmann, 1989). This pos- eastern India). The invasion of New Guin- sible antiquity of the Plebeia line (a basic ea and Australia by Trigona (s lat) taxa of branch in the cladogram of Michener, the Malayan region seems to be much 1990) in South America, and the indication more recent. of a more remote relatonship between the The hypotheses of Kerr and Maule neotropical and African taxa (cf Michener, (1964), who supposed that the Meliponi- 1990), as already discussed, are sugges- nae originated in South America and mi- tive that a West Gondwanan origin for Mel- grated to North America during the Eo- iponinae is also a plausible hypothesis cene, and via the Bering strait to other (Camargo, 1989, 1990; Michener, 1979; continents, and that of Wille (1979b, 1983) Roubik, 1989). Thus, the Malayan and who suggested an African origin in the Australian taxa would be derived from the Upper Cretaceous-Lower Tertiary, and mi- neotropical stock, possibly after the split gration to Europe during the Tertiary, and from Africa. from there to the other continents, are not The presence of sister-groups from the supported, in view of recent evidence on Tetragonisca-Tetragona line in Malayan the antiquity of this group and relationships and neotropical regions, and absence of among the taxa. related taxa in Africa suggest an ancient connection track, via the holarctic region, before the separation of West Eurasia and ACKNOWLEDGMENTS North America, and before the formation of the immense Himalayan mountain range We thank R Zucchi and CD Michener for sug- by the collision of India with Asia, a re- gestions and De Jong for correcting the lan- markable barrier to recent fauna. The guage and style, anonymous referees for correc- of fossils from the Creta- tions and suggestions. This project received presence Upper financial support from the FINEP, CNPq and FA- ceous in New USA relat- Jersey, (T prisca, PESP; JMFC is a CNPq associate researcher, ed to Tetragonisca-Tetragona line) and Ref 300014/84-8/ZO/FV. from the Eocene Amber Baltic (Kelneriapis eocenica, related to Hypotrigona line) are possible indications of this migratory route. Résumé — Systématique, phylogenèse An ancient communication between South et biogéographie des Meliponinae (Hy- and North America, via the proto-Caribbean menoptera, Apidae) : synthèse. Dans cet arc, in the Early Tertiary (Camargo et al, article de synthèse sont discutées les prin- 1988) or in the Upper Cretaceous, has cipales propositions concernant la systé- been proposed for bees and other fauna (cf matique, la phylogenèse et la biogéogra- Savage, 1983; Rage, 1986; Guyer and phie des Meliponinae, ainsi que la polarité Savage, 1987; Roubik, 1990; see also the et l’importance de quelques caractères literature in Savage, 1991). The neotropical morphologiques. Bien que tout un ensem- Tetragona-Tetragonisca group has its ble de synapomorphies (par ex les corbicu- greatest diversity and dispersal center at les, le rastellum, l’articulation du basitarse the Guyana and northern Brazil shields. postérieur près de l’extrêmité antérieure de l’apex du tibia) suggèrent que les Meliponi- entre Trigonisca (s lat) et Lisotrigona et nae constituent un groupe cophylétique Pariotrigona suggèrent une liaison ancien- des Apinae, des Bombinae et des Euglos- ne, peut-être du Crétacé supérieur, à tra- sinae, leurs relations avec ces sous- vers la région holarctique. Les formes fos- familles restent floues. Leur répartition gé- siles du New Jersey et d’Eurasie (ambre ographique (Meliponinae : zone pantropi- de la Baltique) sont une preuve éventuelle cale; Bombinae : zone holarctique; Euglos- de cette route de migration. L’Inde n’a vrai- sinae : zone strictement néotropicale; semblablement pas pris part à la disper- Apinae, principalement indo-malaisienne) sion des Meliponinae et n’a été colonisée et les données des fossiles indiquent un que plus tard à partir de la Malaisie. âge très ancien pour les Meliponinae (le L’absence de représentants de la lignée plus vieux fossile, Trigona prisca, prove- Tetragona-Tetragonisca en Afrique et la nant de l’ambre du New Jersey, USA, est grande divergence des taxons présents daté du Crétacé, soit 96-74.106 ans) et sur ce continent indiquent une longue pé- suggèrent une origine indépendante ou riode d’isolement. Néanmoins des relations une divergence très précoce d’une bran- plus étroites avec les taxons néotropicaux che des proto-Apidae. L’interprétation de (lignée Plebeina-Plebeia et Trigonisca s certains caractères (par ex rastellum, kei- lat, Hypotrigona et Trigonisca) qu’avec tout rotrichia, angle submarginal de l’aile anté- autre taxon des autres continents sont rieure), présentée dans une analyse cla- suggérées par une combinaison confuse distique récente (Michener, 1990), est de plésiomorphies et d’apomorphies. discutée. Une autre polarité pour les carac- tères de l’aiguillon est suggérée (0 = go- systématique / biogéographie / phyloge- nostyle avec micropilosité abondante, 1 = nèse / Meliponinae / Apidae micropilosité absente). L’absence de repré- sentants semblables à Plebeia en Indo- Malaisie et des indications selon lesquelles Zusammenfassung — Systematik, Phy- Austroplebeia (d’Australie) est étroitement logenie und Biogeographie der Melipo- apparentée à la lignée Plebeia des néotro- ninen (Hymenoptera, Apidae): Eine piques (dont les centres de diversité et de Mini-Review. In dieser Ubersicht werden dispersion sont situés dans les boucliers die wichtigsten überlegungen zur Systema- du Brésil méridional) suggèrent l’existence tik, Phylogenie und Biogeographie der Sta- d’une voie de liaison panaustrale et la pré- chellosen Bienen, sowie die Polarität und sence de Meliponinae en Amérique du Bedeutung einiger morphologischer Merk- Sud au moins entre le Crétacé supérieur et male diskutiert. Obwohl eine ganze Reihe le début du Tertiaire. Les relations phylo- von Synapomorphien (zB Corbicula, Ra- génétiques probables et la répartition géo- stellum, Artikulation des hinteren Basitar- graphique laissent à penser que l’origine sus nahe dem vorderen Ende der Tibia- gondwanienne occidentale des Meliponi- spitze) die Einordnung der Meliponen als nae est une hypothèse plausible. Les rela- co-phyletische Gruppe mit den Apinen, tions de groupes sœurs entre les taxons Bombinen und Euglossinen nahelegt, blei- de Malaisie et la lignée Tetragona- ben doch die Beziehungen zu diesen Un- Tetragonisca (dont les centres de disper- terfamilien unklar. Geographische Vertei- sion et de diversité se situent dans les lung (Meliponinen - pantropisch, Bombi- boucliers des Guyanes et du Brésil septen- nen - holarktisch, Euglossinen - streng trional), telles que les indiquent certaines neotropisch, Apinen - vorwiegend indo- synapomorphies, et une relation possible malayisch) und fossile Funde deuten auf ein größeres Alter der Meliponinen hin (das und Trigonisca, sensu lato: Hypotrigona älteste Fossil, Trigona prisca, aus einem und Trigonisca), nahegelegt durch eine Bernstein aus New Jersey, USA, 96-75 106 verwirrende Kombination von Plesiomor- Jahre) und lassen einen unabhängigen Ur- phien und Apomorphien, als zu Gruppen sprung oder eine frühe Abzweigung von von anderen Kontinenten. einem Ur-Apidenzweig vermuten. Die Inter- pretation einiger Merkmale in einer kürzlich Systematik / Biogeographie / Apidae / publizierten kladistischen Analyse der Meli- Meliponinae / Phylogenie poninen (Rastellum, Keirotrichia, submargi- naler Winkel des Vorderflügels) wird disku- tiert. Außerdem wird eine andere Polarität REFERENCES von Stachelmerkmalen vorgeschlagen (0 = Gonostylus mit reichlicher Mikropilosität, 1 Alexander BA (1991) Phylogenetic analysis of = Mikropilosität fehlend). the genus Apis (Hymenoptera: Apidae). Ann Die Abwesenheit von Plebeia-ähnlichen Entomol Soc Am 84(2), 137-149 Vertretern in Indo-Malaya und die Ver- Camargo JMF (1972) Notas prévias sobre o tra- to de rainhas de dorsata e wandtschaft als Schwestergruppen von genital Apis Apis In: und florea (Hymenoptera, Apidae). Homenag- malayischen neotropischen Meliponi- em à WE Kerr. Rio Claro, 47-56 nen (die Linie Tetragona-Tetragonisca JMF Comentários sobre a sis- und Camargo (1989) möglicherweise Trigonisca- temática de Meliponinae (Hymenoptera, Api- Pariotrigona, Lisotrigona) so wie die mögli- dae). In: An XIV Simp Anual da ACIESP. 68 che Verwandtschaft zwischen Austrople- (suppl), 41-61 beia und der neotropischen Plebeia-Linie Camargo JMF (1990) Stingless bees of the Am- legen einen panaustralischen Verbin- azon. In: Proc 11th IUSSI Int Congr: Social dungsweg und einen weiteren über die ho- and the Environment (Veeresh GK, larktische Region (möglicherweise in der Mallik B, Viraktamath CA, eds) Bangalore, In- oberen Kreide) nahe. Die Anwesenheit dia, 736-738 von meliponinen im südlichen Südamerika Camargo JMF, Moure JS (1983) Trichotrigona, (mindestens zwischen der oberen Kreide um novo genero de Meliponinae (Hymenop- do rio Brasil. und dem frühen ist wahrscheinlich. tera, Apidae) Negro, Amazonas, Tertiär) Acta Amazonica 13 (2), 421-429 Diese phylogenetischen Beziehungen und Moure JS Notas sobre os machen die Camargo JMF, (1988) Ausbreitungsmuster Hypothe- Meliponinae (Hymenoptera, Apidae) colecio- se eines der aus Ursprungs Meliponen nados por Felippo Silvestri na Bacia do rio West-Gondwana plausibel. Fossile Funde Prata. Rev Bras Entomol 32 (2), 293-314 in New Jersey, USA, und Eurasien (Balti- Camargo JMF, Wittmann D (1989) Nest archi- scher Bernstein) sind mögliche Beweise tecture and distribution of the primitive sting- für diese Wanderungsrouten. Indien war less bee, Mourella caerulea (Hymenoptera, wahrscheinlich an diesen Ausbreitungswe- Apidae, Meliponinae): evidence for the origin gen nicht beteiligt, sondern wurde erst of Plebeia (sensu lato) on the Gondwana continent. Stud Neotrop Fauna Environ 24 später von Malaya aus besiedelt. Das (4), 213-229 Fehlen der Tetragona-Tetragonisca- Gruppe in Afrika und die große Divergenz Camargo JMF, Moure JS (1992) Os generos Schwarz, 1938 e der auf diesem Kontinent vorhandenen Paratrigona Paratrigona Moure, 1951 (Hymenoptera, Apidae, Meli- Taxa weisen auf eine lange Isolationspe- poninae). Arq Zool (São Paulo) (in press) riode hin. Es bestehen jedoch Hinweise Camargo JMF, Moure JS, Roubik DW (1988) einer näheren Verwandtschaft zu den neo- Melipona yucatanica new species (Hymenop- tropischen Taxa (Plebeina-Plebeia-Gruppe tera: Apidae: Meliponinae); dis- persal across the Caribbean Arc and post- Michener CD, Laberge W, Moure JS (1955) Eocene vicariance. Pan-Pac Entomol 64 (2), Canephorulini, a tribe of South American 147-157 bees (Hymenoptera-Apoidea). Dusenia 6 Cameron SA (1991) A new tribal phylogeny of (5), 207-212 the Apidae interred from mitochondrial DNA Michener CD, Winston ML, Jander R (1978) Pol- sequences. In: Diversity in the Genus Apis len manipulation and related activities and (Smith DR, ed) Westview Press / Oxford and structures in bees of the family Apidae. Univ IBH Publishing Co Pvt Ltd Boulder, CO, 71- Kansas Sci Bull 51 (19), 575-601 87 Moure JS (1946) Meliponas do Brasil. Chácaras Cruz-Landin C (1967) Estudo comparativo de al- Quintaes, SP, 74, 609-612 gumas glandulas das abelhas (Hymenoptera, Moure JS (1951) Notas sobre Meliponinae (Hy- Apoidea) e respectivas implicações evoluti- menoptera-Apoidea). Dusenia 2 (1), 25-70 vas. Arq Zool S Paulo 15, 177-290 Moure JS (1961) A preliminary supra-specific Friese H (1920) Canephorula apiformis Friese classification of the Old World Meliponine (Hymenoptera), eine Bienen-Art mit dem Be- bees (Hymenoptera, Apoidea). Stud Entomol ginne der Koerbchenbildung aus Argentinien. 4 (1-4), 181-242 Zool Jahrb Abt Syst Oekol Geogr Tiere 43, Moure JS de uma nova 461-470 (1971) Descrição espé- cie de Tetragona do Brasil Central (Hyme- Grimaldi D, Beck CW, Boon JJ (1989) Occur- noptera, Apidae). Bol Univ Paraná Zool 4 rence, chemical characteristics, and paleon- (10), 47-50 tology of the fossil resins from New Jersey. Moure JS um novo Am Mus Novit 2948, 1-27 (1989a) Camargoia, genero Neotropical de Meliponinae (Hymenoptera, Guyer C, Savage JM (1987) A cladistic classifi- Apidae). Bol Mus Paraense Emilio Goeldi cation of anoles (Scauria: Iguanidae). Syst Ser Zool 5 (1), 71-78 Zool 35, 509-531 Moure JS (1989b) Sakagamilla affabra, gen n e Kerr Maule V distribution WE, (1964) Geographic sp n de Meliponinae (Hymenoptera, Apidae) of stingless bees and its implications (Hyme- de Rondonia. Rev Bras Zool 6 (4), 681-684 noptera: Apidae). J NY Entomol Soc 72, 2-17 Moure JS, Camargo JMF (1978) A fossil sting- Kimsey LS (1984) A re-evaluation of the phylo- less bee from Copal. J Kans Entomol Soc 51, genetic relationships in the Apidae (Hyme- 560-566 noptera). Syst Entomol 9, 435-441 Moure JS, Nogueira-Neto P, Kerr WE (1958) Ev- Michener CD external mor- (1944) Comparative olutionary problems among Meliponinae (Hy- phology, phylogeny and a classification of the menoptera, Apidae). Proc Int Congr Entomol bees (Hymenoptera). Bull Am Mus Nat Hist 2, 481-493 82, 151-326 Patterson C, Owen HG (1991) Indian isolation Michener CD of the bees. (1979) Biogeography or contact? A response to Briggs. Syst Zool Ann Missouri Bot Gard 66, 277-347 40, 96-100 A new of fos- Michener CD (1982) interpretation Plant JD, Paulus HF (1987) Comparative mor- sil social bees from the Dominican Republic. phology of the postmentum of bees (Hyme- Sociobiology 7, 37-45 noptera: Apoidea) with special remarks on Michener CD (1990) Classification of the Apidae the evolution of the lorum. Z Zool Syst Evol - (Hymenoptera). Univ Kansas Sci Bull 54 (4), Forsch 25, 81-103 75-164 Prentice M (1991) Morphological analysis of the Michener CD, Grimaldi DA (1988a) A Trigona tribes of Apidae. In: Diversity in the genus from late Cretaceous Amber of New Jersey Apis (Smith DR, ed) Westview Press Oxford (Hymenoptera: Apidae: Meliponinae). Am and IBH Publ Co Pvt Ltd, Boulder, CO, 51-69 Mus Novit 2917, 1-10 Rage JC (1986) South American/North Ameri- Michener CD, Grimaldi DA (1988b) The oldest can terrestrial interchanges in the latest Cre- fossil bee: apoid history, evolutionary stasis, taceous: short comments on Brett-Surman and antiquity of social behavior. Proc Natl and Paul (1985), with additional data. J Ver- Acad Sci USA 85, 6424-6426 tebr Paleontol 6, 382-383 Roubik DW (1989) Ecology and Natural History Schwarz HF (1948) The stingless bees (Meli- of Tropical Bees. Cambridge Univ Press, poninae) of the western hemisphere. Bull Am Cambridge, UK, 514 pp Mus Nat Hist 90, 1-546 Roubik DW (1990) Biogeographical ecology of Sheppard WS, McPheron BA (1991) Ribosomal Melipona (Apidae: Meliponinae). In: Proc DNA diversity in Apidae. In: Diversity in the 11th Int Congr IUSSI: Social Insects and the Genus Apis (Smith DR, ed) Westview Press Environment (Veeresh GK, Mallik B, Virakta- of Oxford, IBH Publ Co Pvt Ltd, Boulder, CO, math CA, eds) Bangalore, India, 579-580 89-102 Ruttner F (1988) Biogeography and Taxonomy Simpson BB, Neff JL (1985) Plants, their polli- of Honeybees. Springer-Verlag, Berlin, 284 nating bees, and the great American inter- pp change. In: The Great American Biotic Inter- Sakagami SF (1975) Stingless bees (excl Tetra- change (Stehli FG, Webb SD, eds) Plenum, gonula) from the Continental Southeast Asia New York, 427-452 in the collection of Bernice P Bishop Mu- Tosi A (1896) Di nuovo genere di Apiaria fossile seum, Honolulu (Hymenoptera, Apidae). nell’ambra di Sicilia (Meliponorytes succini, M J Fac Sci Hokkaido Univ, Ser VI Zool 20 (1), sicula). Rev Ital Paleontol 2, 352-356 49-76 Wille A (1959) A new fossil stingless bee (Melip- Sakagami SF (1978) Tetragonula stingless onini) from the amber of Chiapas, Mexico. bees of the continental Asia and Sri Lanka. J J Paleontol 33, 849-852, pl 119 Fac Sci Hokkaido Univ Ser VI Zool 165- 21, Wille A A review of the fossil 247 (1977) general stingless bees. Rev Biol Trop 25, 43-46 SF, Michener CD Tribes of Sakagami (1987) Wille A (1979a) A comparative study of the pollen Xylocopinae and origin of the Apidae (Hyme- press and nearby structures in the bees of the noptera: Apoidea). Ann Entomol Soc Am 80 family Apidae. Rev Biol Trop 27, 217-221 (3), 439-450 Wille A and SF, Inoue T, Salmah S (1979b) Phylogeny relationship Sakagami (1990) Sting- the and of the less bees of Central Sumatra. In: Natural among genera subgenera bees of the world. of Social and Bees in stingless (Meliponinae) History Wasps Equato- Rev Biol 241-277 rial Sumatra (Sakagami SF, Ohgushi R, Rou- Trop 27 (2), bik DW, eds) Hokkaido Univ Press, Sapporo, Wille A (1983) Biology of the stingless bees. 125-137 Ann Rev Entomol 28, 41-64 Savage JM (1983) The enigma of the Central Winston ML (1979) The proboscis of the long- American herpetofauna: dispersals or vicari- tongued bees: A comparative study. Univ ance? Ann MO Bot gard 69, 464-547 Kansas Sci Bull 51 (22), 631-667 Savage JM (1991) Reviews: biogeography of Winston ML, Michener Cd (1977) Dual origin of the West Indies. Past, present and future highly social behavior among bees. Proc Natl (Woods CA, ed) Syst Zool 40 (1), 110-111 Acad Sci USA 74 (3), 1135-1137 Schwarz HF (1932) The genus Melipona: the Zeuner FE, Manning FJ (1976) A monograph on type genus of the Meliponidae or stingless fossil bees. Bull Br Mus Nat Hist (Geol) 27, bees. Bull Am Mus Nat Hist 63, 231-460 149-268, 4 pl