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Hymenoptera, Apidae): a Mini-Review 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 Plebeia 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), Apinae (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 taxonomy and systematics, derived pollen-manipulating behavior and the number of Apidae and non-Apidae bees 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 species 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 bee 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 Trigona 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.
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