Phylogeny of the bees of the family Apidae based on larval characters with focus on the origin of cleptoparasitism (Hymenoptera: Apiformes)

Abstract.  Fifty-four genera of the bee family Apidae comprising almost all tribes were analysed based on 77 traditional and one new character of the mature larvae. Nine, especially cleptoparasitic species, were newly added. Analyses were performed by maximum parsimony and Bayesian inference. Trees inferred from the analysis of the complete dataset were rooted by taxa from the families Melittidae and Megachilidae. Unrooted trees inferred from the analysis of the partial dataset (excluding outgroup taxa) are also presented to preclude possible negative effects of the outgroup on the topology of the ingroup. Only the subfamily Nomadinae was statistically well supported. The monophyly of the subfamilies Xylocopinae and Apinae was not topologically recovered. The monophyly of the tribe Tetrapediini was supported, and this tribe was found to be related to xylocopine taxa. At the very least, larval morphology suggests that Tetrapedia is not a member of the subfamily Apinae. Our analyses support the monophyly of the Eucerine line (Emphorini, Eucerini, Exomalopsini, Tapinotaspidini) and of the Apine line (Anthophorini, Apini, Bombini, Centridini, Euglossini, Meliponini). All analyses support the monophyly of totally cleptoparasitic tribes of the subfamily Apinae. We named this group the Melectine line (Ericrocidini, Isepeolini, Melectini, Osirini, Protepeolini, Rhathymini). In previous studies all these cleptoparasitic tribes were considered independent evolutionary lineages. Our results suggest that their similarities with hosts in morphology and pattern are probably the result of convergence and host–parasite co-evolution than phylogenetic affinity. According to the present analysis, the cleptoparasitism has evolved independently only six times within the family Apidae.     

The major opsin in bees (Insecta: Hymenoptera): A promising nuclear gene for higher level phylogenetics.

We report the phylogenetic utility of the nuclear gene encoding the long-wavelength opsin (LW Rh) for tribes of bees. Aligned nucleotide sequences were examined in multiple taxa from the four tribes comprising the corbiculate bees within the subfamily Apinae. Phylogenetic analyses of sequence variation in a 502-bp fragment (approx 40% of the coding region) strongly supported the monophyly of each of the four tribes, which are well established from previous studies of morphology and DNA. Trees estimated from parsimony and maximum likelihood analyses of LW Rh sequences show a strongly supported relationship between the tribes Meliponini and Bombini, a relationship that has been found uniformly in studies of other genes (28S, 16S, and cytochrome b). All of the tribal clades as well as relationships among the tribes are supported by high bootstrap values, suggesting the utility of LW Rh in estimating tribal and subfamily rank for these bees. The sequences exhibit minimal base composition bias. Both 1st + 2nd and 3rd position sites provide information for estimating a reliable tree topology. These results suggest that LW Rh, which has not been reported previously in studies of organismal phylogenetics, could provide important new data from the nuclear genome for phylogeny reconstruction.     

Comparative morphology of the postmentum of bees (Hymenoptera: Apoidea) with special remarks on the evolution of the lorum

A comparative morphological study of the basal sclerites of the bee labium was undertaken. The term postmentum was applied to the basal sclerite of the bee labium. In contrast to recent interpretations, the undivided postmentum was found to be ancestral for bees and homologous with the single postmental sclerite of other Hymenoptera. This sclerite has previously been incorrectly indentified as two separate sclerites, usually termed mentum and lorum (= submentum), for many short-tongued bees (Colletidae, Halictidae, Andrenidae, Melittidae) and for the long-tongued families of bees (Anthophoridae, Fideliidae Megachilidae) excepting most members of the Apidae. The postmentum, divided into a true mentum and lorum, was found only in certain members of the Apidae. A phylogenetic implication resulting from this study shows that the Andrenidae may be the sister group to the MCL-T group (Melittidae, Ctenoplectridae and long-tongued families of bees). In addition, it is proposed that the Euglossinae should be the sister group to the Apinae (Meliponini, Apini and Bombini). This means that eusociality may be considered a synapomorphy for the Apinae.     

Fungi associated with Bombinae (Apidae: Hymenoptera) in North America

Eleven genera of fungi were isolated from overwintered queens of six species of Bombinae, as well as Penicillium from their nests. Hirsutella and Metarrhizium are suggested for the first time to be pathogens of Bombus This survey of fungi was part of a more general study of the natural enemies and associates of these bees in Ontario (3).     

A new wild, pollinating bee species of the genus Tetraloniella from the Arabian Peninsula (Hymenoptera, Apidae)

A new species of the eucerine bee genus Tetraloniella Ashmead (Apinae: Eucerini) is described and figured from central Saudi Arabia and Qatar. Tetraloniella (Tetraloniella) persiciformissp. n. is distinguished on the basis of coloration, integumental sculpturing, male metafemoral structure, and male terminalia. A floral record of Pulicaria undulata (L.) C.A. Mey. (Compositae) is noted for some of the material. Females superficially resemble those of Tarsalia persica (Warncke) (Ancylaini) in overall coloration but can be distinguished by the typical generic and tribal characters.     

Palaeocene origin of the Neotropical lineage of cleptoparasitic bees Ericrocidini‐Rhathymini (Hymenoptera,Apidae)

Cleptoparasitic bees abandoned pollen‐collecting for their offspring and lay their eggs in other bees' provisioned nests. Also known as cuckoo bees, they belong to several lineages, but are especially diverse in Apinae. We focused on a lineage of apine cleptoparasitic bees, the clade Ericrocidini + Rhathymini, which attack nests of oil‐collecting bees. We sequenced five genes for 20 species in all genera of this clade plus a large outgroup to reconstruct the phylogeny and estimate divergence times. We confirmed the monophyly of the clade Ericrocidini + Rhathymini and its position inside the ericrocidine line together with the tribes Protepeolini, Isepeolini, Osirini and Coelioxoidini. Our results corroborated the current taxonomic classification. Ericrocis is sister to all Ericrocidini and the position of Acanthopus and the most diverse genus Mesoplia were inconclusive. Ericrocidini + Rhathymini diverged from other apine cleptoparasitic lineages 74 Ma in the Cretaceous and from each other in the Palaeocene at 61 Ma. Considering the robust molecular evidence of their sister relationships, the striking differences in the morphology of first‐instar larvae of the two groups may represent adaptations to the nesting biology of their hosts. As other cleptoparasites in the ericrocidine line, Ericrocidini and Rhathymini possess larvae which are adapted to kill the immature host and to feed on floral oil provided by the host female. The evolution of host specialization in the line Ericrocidini + Rhathymini retroceded to the Eocene when they differentiated synchronously with their hosts, Centris and Epicharis .     

The genetic structure of a tribal population, the Yanomama Indians XI. Gene frequencies for 10 blood groups and the ABH-Le secretor traits in the Yanomama and their neighbors; the uniqueness of the tribe.

In this paper we present the results of blood group typings for a total of 33 villages distributed among five South American Indian tribes--Yanomama (21 villages), Makiritare (eight villages), Macushi (two villages), Piaroa (one village), and Wapishana (one village). These new results for the Yanomama and Makiritare tribes have been combined with those previously reported to allow a better appreciation of the distribution of allelic frequencies in the tribes. The relationship of the Yanomama to other South American Indian tribes is investigated using data on six polymorphic loci (Rh, MNS, Fy, Jk, Di, Hp). By use of four genetic measures (two of genetic relationship and two of genetic diversity), we demonstrate that the Yanomama are genetically unique among a sample of 20 South American tribes. In addition, the Yanomama show somewhat less genetic diversity for the six loci analyzed than the average South American tribe. Taken together, these results indicate a rather long period of isolation for the population antecedent to the Yanomama--perhaps since the time of entry of man into the South American continent. The pattern of genetic relationships and genetic diversity for the 20 tribes is consistent with the hypothesis that evolution in South America proceeded by a process of fission-fusion leading to isolation of subpopulations with subsequent genetic differentiation as a consequence of population isolation. The uniqueness of the Yanomama appears to stem entirely from such a process, there being no evidence of any selective differential for the loci analyzed.     

MHC Class II haplotypes of Colombian Amerindian tribes

We analyzed 1041 individuals belonging to 17 Amerindian tribes of Colombia, Chimila, Bari and Tunebo (Chibcha linguistic family), Embera, Waunana (Choco linguistic family), Puinave and Nukak (Maku-Puinave linguistic families), Cubeo, Guanano, Tucano, Desano and Piratapuyo (Tukano linguistic family), Guahibo and Guayabero (Guayabero Linguistic Family), Curripaco and Piapoco (Arawak linguistic family) and Yucpa (Karib linguistic family). for MHC class II haplotypes (HLA-DRB1, DQA1, DQB1). Approximately 90% of the MHC class II haplotypes found among these tribes are haplotypes frequently encountered in other Amerindian tribes. Nonetheless, striking differences were observed among Chibcha and non-Chibcha speaking tribes. The DRB1*04:04, DRB1*04:11, DRB1*09:01 carrying haplotypes were frequently found among non-Chibcha speaking tribes, while the DRB1*04:07 haplotype showed significant frequencies among Chibcha speaking tribes, and only marginal frequencies among non-Chibcha speaking tribes. Our results suggest that the differences in MHC class II haplotype frequency found among Chibcha and non-Chibcha speaking tribes could be due to genetic differentiation in Mesoamerica of the ancestral Amerindian population into Chibcha and non-Chibcha speaking populations before they entered into South America.     

On the subdivision of the family Lophopidae (Homoptera,Auchenorrhyncha: Fulgoroidea) on the subfamilies and tribes with description of two new tribes

A new classification of the family Lophopidae is proposed where it is subdivided intoe two subfamilies Menoscinae Melichar with four tribes (Carrioniini trib. n., Virgiliini trib. n., Menoscini Melichar, and Acarnini Baker) and Lophopinae Stål with two tribes (Elasmoscelini Melichar and Lophopini Stål).     

Phylogenetic relationships and the primitive X chromosome inferred from chromosomal and satellite DNA analysis in Bovidae

The early phylogeny of the 137 species in the Bovidae family is difficult to resolve; knowledge of the evolution and relationships of the tribes would facilitate comparative mapping, understanding chromosomal evolution patterns and perhaps assist breeding and domestication strategies. We found that the study of the presence and organization of two repetitive DNA satellite sequences (the clone pOaKB9 from sheep, a member of the 1.714 satellite I family and the pBtKB5, a 1.715 satellite I clone from cattle) on the X and autosomal chromosomes by in situ hybridization to chromosomes from 15 species of seven tribes, was informative. The results support a consistent phylogeny, suggesting that the primitive form of the X chromosome is acrocentric, and has satellite I sequences at its centromere. Because of the distribution of the ancient satellite I sequence, the X chromosome from the extant Tragelaphini (e.g. oryx), rather than Caprini (sheep), line is most primitive. The Bovini (cow) and Tragelaphini tribes lack the 1.714 satellite present in the other tribes, and this satellite is evolutionarily younger than the 1.715 sequence, with absence of the 1.714 sequence being a marker for the Bovini and Tragelaphini tribes (the Bovinae subfamily). In the other tribes, three (Reduncini, Hippotragini and Aepycerotini) have both 1.714 and 1.715 satellite sequences present on both autosomes and the X chromosome. We suggest a parallel event in two lineages, leading to X chromosomes with the loss of 1.715 satellite from the Bovini, and the loss of both 1.714 and 1.715 satellites in a monophyletic Caprini and Alcelaphini lineage. The presence and X chromosome distribution of these satellite sequences allow the seven tribes to be distributed to four groups, which are consistent with current diversity estimates, and support one model to resolve points of separation of the tribes.     

The apid cuckoo bees of the Cape Verde Islands (Hymenoptera, Apidae)

The apid cuckoo bees of the Cape Verde Islands (Republic of Cape Verde) are reviewed and five species recognized, representing two genera. The ammobatine genus Chiasmognathus Engel (Nomadinae: Ammobatini), a specialized lineage of cleptoparasites of nomioidine bees is recorded for the first time. Chiasmognathus batelkaisp. n. is distinguished from mainland African and Asian species. The genus Thyreus Panzer (Apinae: Melectini) is represented by four species - Thyreus denoliisp. n., Thyreus batelkaisp. n., Thyreus schwarzisp. n., and Thyreus aistleitnerisp. n. Previous records of Thyreus scutellaris (Fabricius) from the islands were based on misidentifications.     

Antibacterial activity of honey from stingless honeybees (Hymenoptera; Apidae; Meliponinae).

The aim of the study was to examine antibacterial activity of the honey of stingless honeybees (Meliponinae). An agar well diffusion assay demonstrated that many honey samples of stingless honeybees inhibited the growth of test strains of Staphylococcus aureus, Enterococcus faecalis, Escherichia coli and Pseudomonas aeruginosa; moreover, they exhibited non-peroxide antibacterial activity against those strains. This is the first time that non-peroxide antimicrobial activity of honey from a number of species of stingless honeybees has been demonstrated. These antibacterial activities appear to be powerful, even when compared to those of"manuka honey" from Apinae honeybees.     

A worldwide phylogenetic classification of the Poaceae (Gramineae) III: An update

We present an updated worldwide phylogenetic classification of Poaceae with 11 783 species in 12 subfamilies, 7 supertribes, 54 tribes, 5 super subtribes, 109 subtribes, and 789 accepted genera. The subfamilies (in descending order based on the number of species) are Pooideae with 4126 species in 219 genera, 15 tribes, and 34 subtribes; Panicoideae with 3325 species in 242 genera, 14 tribes, and 24 subtribes; Bambusoideae with 1698 species in 136 genera, 3 tribes, and 19 subtribes; Chloridoideae with 1603 species in 121 genera, 5 tribes, and 30 subtribes; Aristidoideae with 367 species in three generaand one tribe; Danthonioideae with 292 species in 19 generaand 1 tribe; Micrairoideae with 192 species in nine generaand three tribes; Oryzoideae with 117 species in 19 genera, 4 tribes, and 2 subtribes; Arundinoideae with 36 species in 14 genera and 3 tribes; Pharoideae with 12 species in three generaand one tribe; Puelioideae with 11 species in two generaand two tribes; and the Anomochlooideae with four species in two generaand two tribes. Two new tribes and 22 new or resurrected subtribes are recognized. Forty-five new (28) and resurrected (17) genera are accepted, and 24 previously accepted genera are placed in synonymy. We also provide an updated list of all accepted genera including common synonyms, genus authors, number of species in each accepted genus, and subfamily affiliation. We propose Locajonoa, a new name and rank with a new combination, L. coerulescens. The following seven new combinations are made in Lorenzochloa: L. bomanii, L. henrardiana, L. mucronata, L. obtusa, L. orurensis, L. rigidiseta, and L. venusta.     

Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region

Sequence data from the nuclear encoded ribosomal internal transcribed spacer (ITS) region were used to determine monophyly of tribes, tribal limits, and tribal relationships of 96 so far unassigned or tentatively assigned genera (represented by 101 taxa/accessions) within the Brassicaceae. Maximum-parsimony and maximum-likelihood analyses of 185 ITS Brassicaceae sequences, which also included representatives of each of the 34 currently recognized tribes, supported the separate phylogenetic distinctness of these tribes and permitted the tribal assignment of all but 12 of the unassigned genera into tribal clades. The data support the recognition of eight new, well-resolved, uni- or oligogeneric tribes recognized herein as the Alyssopsideae [96% bootstrap support (BS); including the central and southwestern Asian Alyssopsis and Calymmatium], Asteae (100% BS; including the Mexican Asta), Eudemeae (97% BS; South American Brayopsis, Eudema, and Xerodraba), Kernereae (96% BS; European Kernera and Rhizobotrya), Notothlaspideae (100% BS; New Zealandic Notothlaspi), Oreophytoneae (100% BS; eastern African Oreophyton and southern European Murbeckiella), and Yinshanieae (100% BS; Chinese Yinshania), as well as the moderately supported Microlepidieae (75% BS; Australian Microlepidium and Carinavalva). Furthermore, the results fully support the recent findings that the tribes Schizopetaleae and Thelypodieae ought to be recognized as two distinct tribes instead of a single tribe, as well as provide some support for the re-establishment of the tribe Cremolobeae, bringing the total number to 44 tribes in the family. Nearly 92% (308) of the 336 genera in the family have been assigned to a tribe. The earlier-published Anastaticeae is taken here to replace the Malcolmieae.     

小腹茧蜂亚科的雄外生殖器及族级单元系统发育的研究

对分布在东洋区和古北区的小腹茧蜂亚科 (膜翅目: 茧蜂科)21个属的67个种及外群折脉茧蜂属 (膜翅目: 茧蜂科) 2个种的雄外生殖器的5个性状进行了比较研究。在形态学研究的基础上,通过选用头部、胸部和腹部(包括雌雄外生殖器的性状) 等34个性状,运用支序分析的方法探讨了分布在东洋区和古北区的小腹茧蜂亚科21个属以及它们所属的族间的系统发育关系,并对Mason (1981) 的分类系统进行了重新评价。雄外生殖器和支序分析基本上证实并恢复了由Mason (1981) 确定的2个主要分支,即绒茧蜂族Apantelini+小腹茧蜂族Microgastrini和拱茧蜂族Fornicini+盘绒茧蜂族Cotesiini+侧沟茧蜂族MicroplitinI。绒茧蜂族Apantelini、拱茧蜂族Fornicini和侧沟茧蜂族Microplitini为单系群也被支持,但小腹茧蜂族Microgastrini和盘绒茧蜂族Cotesiini是否为单系群尚难于在树形图中体现,而且族内各属间的分支关系有变动。因此,尽管Mason的族级分类单元有一些欠缺,但仍是可信、实用的,不同意Walker等 (1990) 认为不应再使用Mason分族系统的观点。     

A new record of Thaumastobombus andreniformis Engel 2001 in Eocene amber (Hymenoptera: Apidae)

A new specimen of the rare fossil bee Thaumastobombus andreniformis Engel 2001 (Apidae: Apinae: Electrapini) is reported and figured from middle Eocene (Lutetian) Baltic amber. The new specimen, a female of the worker caste, agrees in every respect with the holotype except some morphometric differences. These minor size differences are likely related to the degree of sociality of T andreniformis.     

The relationship between the ventral nerve cord, body size and phylogeny in ground beetles (Goleoptera: Garabidae)

The ventral nerve cord in the family Carabidae (considered in the widest sense! exhibits variations in the degree of fusion of thoracic and abdominal ganglia. There are usually three discrete thoracic ganglia and between one and seven discrete abdominal ganglia, the number differing between tribes. Of the 44 tribes and 177 species examined, 38 tribes contained species showing no differences in the degree of ventral nerve cord consolidation. However, the remaining six tribes showed variations in the degree of ventral nerve cord consolidation between genera (Lebiini, Cychrini, Nebriini, Scaritini, Licinini and Brachinini), whilst one genus showed variations between species (Leistus , Nebriini). No variation in ventral nerve cord consolidation was observed in conspecifics. The degree of ventral nerve cord consolidation is inversely proportional to overall body length. With respect to phylogeny, the degree of consolidation of the nerve cord docs not consistently support the traditional Carabinae-Harpalinae subfamily division. However, the Harpalinae always have four or less discrete abdominal ganglia (with the sole exception of the Broscinij, whilst the Carabinae exhibit almost the whole range of variations. Thus the Harpalinae (or the major pari of it) may be a monophyletic group, but this is not true of the Carabinae. Trends in the degree of ventral nerve cord consolidation for the various tribes were noted, and phylogenetic implications were evaluated wherever possible.     

Phylogenetic relationships of the Aurantioideae (Rutaceae) based on the nuclear ribosomal DNA ITS region and three noncoding chloroplast DNA regions, atpB-rbcL spacer, rps16, and trnL-trnF

The tribes and subtribes of Aurantioideae, an economically important subfamily of the Rutaceae, have a controversial taxonomic history because a phylogenetic framework has been lacking. In order to construct an evolutionary history and evaluate the most recent classification system [Swingle and Reece 1967. The botany of Citrus and its wild relatives, in: The Citrus Industry, vol. 1, History, World Distribution, Botany, and Varieties. University of California, Berkeley, pp. 190-430], one nuclear and three noncoding chloroplast genes were sequenced and analyzed phylogenetically along with selected non-molecular characters. Taxa representing tribes Citreae and Clauseneae and their six subtribes were sampled. In all analyses Aurantioideae is monophyletic. The majority-rule consensus tree from the combined analysis indicates that the two tribes are not monophyletic. The combined topology is not congruent with the widely used classification of Aurantioideae by Swingle and Reece (1967). The tribes and subtribes are in need of revision.     

The relationship between the ventral nerve cord,body size and phylogeny in ground beetles (Coleoptera: Carabidae)

The ventral nerve cord in the family Carabidae (considered in the widest sense! exhibits variations in the degree of fusion of thoracic and abdominal ganglia. There are usually three discrete thoracic ganglia and between one and seven discrete abdominal ganglia, the number differing between tribes. Of the 44 tribes and 177 species examined, 38 tribes contained species showing no differences in the degree of ventral nerve cord consolidation. However, the remaining six tribes showed variations in the degree of ventral nerve cord consolidation between genera (Lebiini, Cychrini, Nebriini, Scaritini, Licinini and Brachinini), whilst one genus showed variations between species (Leistus, Nebriini). No variation in ventral nerve cord consolidation was observed in conspecifics. The degree of ventral nerve cord consolidation is inversely proportional to overall body length. With respect to phylogeny, the degree of consolidation of the nerve cord docs not consistently support the traditional Carabinae-Harpalinae subfamily division. However, the Harpalinae always have four or less discrete abdominal ganglia (with the sole exception of the Broscinij, whilst the Carabinae exhibit almost the whole range of variations. Thus the Harpalinae (or the major pari of it) may be a monophyletic group, but this is not true of the Carabinae. Trends in the degree of ventral nerve cord consolidation for the various tribes were noted, and phylogenetic implications were evaluated wherever possible.     

ALLOZYME DIVERGENCE WITHIN THE BOVIDAE

We describe a phylogeny of the Bovidae based on 40 allozyme loci in 27 species, representing 10 of the 14 bovid tribes described by Vrba (1985). Giraffe represented a related family (Giraffidae). A phenogram was derived using the unweighted pair-group method with arithmetic means (UPGMA), based on Nei's genetic distances (ND) between species. A tree was also derived using the neighbor-joining technique, also based on ND. To provide a cladistic interpretation, the data were analyzed by a maximum parsimony method (phylogenetic analysis using parsimony, PAUP). We found marked divergence within the Bovidae, consistent with the appearance of the family in the early Miocene. Unexpectedly, the most divergent species was the impala, which occupied a basal position in all trees. Species in the tribe Alcelaphini were the most derived taxa in all trees. These patterns conflict strongly with the previous taxonomic alliance, based on immuno-distance and anatomical evidence, of the impala as a sister group of the Alcelaphini. All trees agreed that tribes described by Vrba (1985) are monophyletic, except the Neotragini, which was polyphyletic, with suni occupying a long branch by itself. The dikdik and klipspringer were consistently placed as sister taxa to species in the Antilopini. Three tribes (Aepycerotini, Tragelaphini and Cephalophini), whose fossils have not been found outside Africa, were basal in all trees, suggesting that bovids originated in Africa. Nodes connecting the remaining tribes were closely clustered, a pattern that agrees with fossil evidence of rapid divergence within the Bovidae in the mid-Miocene (about 15 mybp). The allozyme data suggested a second phase of rapid divergence within tribes during the Plio-Pleistocene, a pattern that also agrees with fossil evidence. Rates of bovid divergence have therefore been far from constant. However, the clustering of nodes imparts considerable uncertainty to the branching order leading to the derived tribes, and to a lesser extent, species within tribes. The classical division of the Bovidae into the Boodontia and Aegeodontia does not agree with the phylogenetic grouping of tribes presented in this analysis. However, the maximum parsimony tree derived using ‘local’ branch swapping clustered all grazing species into a derived, monophyletic group, suggesting that grazing may have evolved only once in bovid evolution.