Pollen diet diversity across bee lineages varies with lifestyle rather than colony size.

The shift to a pollen diet and the evolution of more highly organized societies, i.e., eusocial, were key milestones in bee diversification over their evolutionary history, culminating in a high dependence on feeding broods with a large variety of floral resources. Here, we hypothesized that obligatory eusocial bees have a wider diet diversity than their relatives with solitary lifestyles, and this would be related to colony size. To test both hypotheses, we surveyed diet breadth data (palynological analysis) based on the Shannon-Wiener index (H') for 85 bee taxa. We also obtained colony size for 47 eusocial bee species. These data were examined using phylogenetic comparative methods. The results support the generalist strategy as a derived trait for the bee taxa evaluated here. The dietary diversity of eusocial bees (H': 2.1, on average) was 67.5% higher than that of noneusocial bees (H': 1.21, on average). There was, however, no relationship between diet breadth and colony size, indicating that smaller colonies can harvest a pollen variety as diverse as larger colonies. Taken together, these results provide new insights into the impact of lifestyle on the diversity of collected pollen. Furthermore, this work sheds light on an advantage of living in more highly structured societies irrespective of the size of the colony.

A tribute to Fernando A. Silveira and his contributions to bee research.

Fernando A. Silveira had the unique combination of being a sagacious scientist and a remarkable human being. Throughout his career, he made significant contributions to understanding bee diversity and keenly spread this scientific information to the academic community at large and beyond the university walls. His rich character, warm heart, strong voice and laughter are missed by those privileged to be Fernandos students, friends, mentors, and family. In this volume, we honor Fernando A. Silveira, who prematurely passed away at the age of 62, leaving three sons, his wife, and numerous friends.

A new neopasiphaeine bee associated with flowers of Loasaceae (Hymenoptera: Colletidae: Actenosigynes).

The genus Actenosigynes includes two species, A. fulvoniger (Michener, 1989) and A. mantiqueirensis Silveira, 2009, both oligolectic on flowers of Blumenbachia (Loasaceae) in southern Brazil. We describe a third species, Actenosigynes silveirai Siriani-Oliveira, sp. n., and provide additional evidence to the suspected narrow host-plant specificity between bees of this genus and Loasaceae. This new species was only recorded to collect resources on flowers of Aosa, a genus closely related to Blumenbachia in the subfamily Loasoideae. We illustrate female and male specimens of the three species to offer a complete summary of the morphological variation within this modestly sized genus of Neopasiphaeinae, including photographs of male genitalia and associated metasomal sterna. Moreover, we provide an identification key for the three species of Actenosigynes and the first phylogenetic and dating estimate for these taxa. The genus diversified in southern South America during the Miocene-Pliocene, following a more ancient divergence associated with the orogenic events that separated its sister-genus, Torocolletes, west of the Andes. We dedicate this newly described species to Fernando A. Silveira for his contributions to research on Brazilian bee taxonomy and biology.

Flowering Time Variation in Two Sympatric Tree Species Contributes to Avoid Competition for Pollinator Services.

Competition is an important biological filter that can define crucial features of species' natural history, like survival and reproduction success. We evaluated in the Brazilian tropical savanna whether two sympatric and congenereric species, Qualea multiflora Mart. and Q. parviflora Mart. (Vochysiaceae), compete for pollinator services, testing whether there is a better competitor or whether plants present any anti-competitive mechanism. Additionally, we investigated the breeding system, pollinators, and flowering phenology of both species. The results showed that Q. multiflora and Q. parviflora are dependent on pollinators for fruit formation, as they exhibited a self-incompatible and non-agamospermic breeding system. These plants shared the same guild of pollinators, which was formed by bees and hummingbirds, and an overlap in the flower visitation time was observed. Each plant species had different pollinator attraction strategies: Q. multiflora invested in floral resource quality, while Q. parviflora invested in resource quantity. The blooming time showed a temporal flowering partition, with highly sequential flowering and no overlap. Qualea parviflora bloomed intensely from September to October, while Q. multiflora bloomed from November to January, with the flowering peak occurring in December. The two Qualea species have morphologically similar flowers, are sympatric, and share the same pollinator community, with overlapping foraging activity during the day. However, they do not compete for pollinator services as they exhibit an anti-competitive mechanism mediated by temporal flowering partition.

The evolutionary history of bees in time and space.

Bees are the most significant pollinators of flowering plants. This partnership began ca. 120 million years ago, but the uncertainty of how and when bees spread across the planet has greatly obscured investigations of this key mutualism. We present a novel analysis of bee biogeography using extensive new genomic and fossil data to demonstrate that bees originated in Western Gondwana (Africa and South America). Bees likely originated in the Early Cretaceous, shortly before the breakup of Western Gondwana, and the early evolution of any major bee lineage is associated with either the South American or African land masses. Subsequently, bees colonized northern continents via a complex history of vicariance and dispersal. The notable early absences from large landmasses, particularly in Australia and India, have important implications for understanding the assembly of local floras and diverse modes of pollination. How bees spread around the world from their hypothesized Southern Hemisphere origin parallels the histories of numerous flowering plant clades, providing an essential step to studying the evolution of angiosperm pollination syndromes in space and time.

Behavioural evolution of Neotropical social wasps (Vespidae: Polistinae): the queen selection process.

All Epiponini wasps are polygynic, with multiple queens alternating over the colony cycle. There are several potential queens in the early stages of this cycle, but as it progresses, the number of queens is reduced. Because most individuals remain reproductively totipotent, there is great potential for conflicts over reproduction. Workers could have an advantage in controlling queen production because they are much more numerous than queens. Nevertheless, the queen selection process is little known for Epiponini. For this reason, we aimed to study the behaviour of queens and workers during queen selection in multiple species of Epiponini, integrate information from previous behavioural studies, and perform a comparative analysis to interpret changes evolutionarily. We conducted observations on nine species belonging to five genera: Brachygastra, Chartergellus, Metapolybia, Polybia and Protopolybia. Females were individually marked to make direct and video observations. Queen production was artificially induced. A total of 28 behaviours related to queen selection were identified. The most aggressive interactions between castes, such as bite and dart, were lost in the major lineages of Epiponini. Bending display I is an ancient behaviour used as the main dominance display. Behaviours exhibited by workers to test queen status arose in the common ancestor of the Epiponini and are not shared by other polistine wasps. Consequently, the act of workers testing queen status probably was present in the Epiponini ancestor. Ritualized test display and dominance behaviours are used in Epiponini as honest signals of the queen's reproductive potential instead of aggressive behaviours. Caste flexibility had already been suggested as the ground plan for Epiponini and is herein discussed as decisive for colony survival of swarm wasps, because it allows colonies to respond efficiently to different situations that may eventually arise.

Taxonomic review of the elampine cuckoo wasps from northeastern Brazil (Hymenoptera: Chrysididae), with the description of three new species.

The diversity of the Elampini cuckoo wasps in northeastern Brazil is reviewed. Three new species are described: Hedychrum oxente Lucena & Zanella sp. nov., Holopyga lunae Lucena sp. nov., and Muesebeckidium clemensi Lucena & Zanella sp. nov. A lectotype is designated for Holopyga piliventris Ducke, 1907 and herein illustrated. Elampus aequinoctialis Ducke, 1901 is restored as a valid species (previously synonymized with Elampus gayi Spinola, 1851) and diagnosed. Holophris huberi (Ducke, 1901) and Muesebeckidium clemensi sp. nov. represent the first records of both genera to northeastern Brazil. New records along with up-to-date distributional maps are discussed, and an identification key to the species of Holopyga from northeastern Brazil is provided. The total diversity of Elampini recorded for northeastern Brazil is now represented by the following eight species: Elampus aequinoctialis Ducke, 1901, Exallopyga guatemalensis (Cameron, 1888), Hedychrum oxente Lucena & Zanella sp. nov., Holophris huberi (Ducke, 1901), Holopyga iheringi du Buysson, 1901, H. lunae Lucena sp. nov., H. piliventris Ducke, 1907, and Muesebeckidium clemensi Lucena & Zanella sp. nov.

speciesLink: rich data and novel tools for digital assessments of biodiversity / speciesLink: dados valiosos e ferramentas inovadoras para avaliações digitais da biodiversidade

Abstract speciesLink is a large-scale biodiversity information portal that exists thanks to a broad collaborative network of people and institutions. CRIA's involvement with the scientific community of Brazil and other countries is responsible for the significant results achieved, currently reaching more than 15 million primary biodiversity data records, 95% of which are associated with preserved specimens and about 25% with high-quality digital images. The network provides data on over 200,000 species, of which over 110,000 occur in Brazil. This article describes thematic networks within speciesLink, as well as some of the most useful tools developed. The importance and contributions of speciesLink are outlined, as are concerns about securing stable budgetary support for such biodiversity data e-infrastructures. Here we review the value of speciesLink as a major source of biodiversity information for research, education, informed decision-making, policy development, and bioeconomy.

Resumo speciesLink é um portal de informações em larga escala sobre biodiversidade, que existe graças a uma ampla rede colaborativa de pessoas e instituições. O envolvimento do CRIA com a comunidade científica do Brasil e de outros países é responsável pelos resultados expressivos alcançados, atingindo atualmente mais de 15 milhões de registros de dados primários de biodiversidade, sendo 95% associados a espécimes preservados e cerca de 25% a imagens digitais de alta qualidade. A rede fornece dados sobre mais de 200.000 espécies, das quais mais de 110.000 ocorrem no Brasil. Este artigo descreve as redes temáticas do speciesLink, bem como algumas das ferramentas mais úteis desenvolvidas. A importância e as contribuições do speciesLink são destacadas, assim como as preocupações em garantir um apoio financeiro estável para e-infraestruturas de dados sobre biodiversidade. Aqui revisamos o valor do speciesLink como uma das principais fontes de informação sobre biodiversidade para pesquisa, educação, tomada de decisão, desenvolvimento de políticas e bioeconomia.

Marimbondos: systematics, biogeography, and evolution of social behaviour of neotropical swarm-founding wasps (Hymenoptera: Vespidae: Epiponini).

Neotropical swarm-founding wasps are divided into 19 genera in the tribe Epiponini (Vespidae, Polistinae). They display extensive variation in several colony-level traits that make them an attractive model system for reconstructing the evolution of social phenotypes, including caste dimorphism and nest architecture. Epiponini has been upheld as a solid monophyletic group in most phylogenetic analyses carried out so far, supported by molecular, morphological and behavioural data. Recent molecular studies, however, propose different relationships among the genera of swarm-founding wasps. This study is based on the most comprehensive epiponine sampling so far and was analyzed by combining morphological, nesting and molecular data. The resulting phylogenetic hypothesis shows many of the traditional clades but still impacts the way certain behavioural characters, such as nest structure and castes, evolved, and thus requires some re-interpretations. Angiopolybia as sister to the remaining Epiponini implies that nest envelopes and a casteless system are plesiomorphic in the tribe. Molecular dating points to an early tribal diversification during the Eocene (c. 55-38 Ma), with the major differentiation of current genera concentrated in the Oligocene/Miocene boundary.

The relevance of chromosome fissions for major ribosomal DNA dispersion in hymenopteran insects.

Ribosomal DNA (rDNA) loci are essential for cellular metabolism due to their participation in ribosome biogenesis. Although these genes have been widely cytogenetically mapped, the evolutionary mechanisms behind their variability in number and chromosomal location remain elusive, even in well-known biological groups, such as ants, bees and wasps (Insecta: Hymenoptera). To address this question in Hymenoptera and therefore advance the understanding of rDNA evolution in insects in general, we integrated molecular cytogenetic data, a phylogenomic framework, model-based predictions and genome sequencing. Hence, we assessed the main evolutionary trends shaping the chromosomal distribution of rDNA loci in Hymenoptera. We noticed the conservation of one site of rDNA per haploid genome, suggesting that a single 45S rDNA locus is the putative ancestral pattern for aculeate Hymenoptera. Moreover, our results highlighted a nonrandom distribution of rDNA in Hymenoptera karyotypes, as well as a lineage-specific preferential location. The proximal location of rDNA is favoured in species with multiple loci and in the two families of Hymenoptera that show the highest range of chromosome numbers: Formicidae and Vespidae. We propose that chromosome fissions have played a crucial role in the distribution pattern of rDNA loci through the evolutionary diversification of Hymenoptera. Moreover, our genomic analysis of two species, one with a single locus of rDNA and one with multiple loci, supported that loci multiplication is followed by sequence divergence. Our results provide detailed information about the number and chromosomal position of rDNA in Hymenoptera and, therefore, broaden our knowledge regarding rDNA evolutionary dynamics in insects.

Investigating Morphological Complexes Using Informational Dissonance and Bayes Factors: A Case Study in Corbiculate Bees.

It is widely recognized that different regions of a genome often have different evolutionary histories and that ignoring this variation when estimating phylogenies can be misleading. However, the extent to which this is also true for morphological data is still largely unknown. Discordance among morphological traits might plausibly arise due to either variable convergent selection pressures or else phenomena such as hemiplasy. Here, we investigate patterns of discordance among 282 morphological characters, which we scored for 50 bee species particularly targeting corbiculate bees, a group that includes the well-known eusocial honeybees and bumblebees. As a starting point for selecting the most meaningful partitions in the data, we grouped characters as morphological modules, highly integrated trait complexes that as a result of developmental constraints or coordinated selection we expect to share an evolutionary history and trajectory. In order to assess conflict and coherence across and within these morphological modules, we used recently developed approaches for computing Bayesian phylogenetic information allied with model comparisons using Bayes factors. We found that despite considerable conflict among morphological complexes, accounting for among-character and among-partition rate variation with individual gamma distributions, rate multipliers, and linked branch lengths can lead to coherent phylogenetic inference using morphological data. We suggest that evaluating information content and dissonance among partitions is a useful step in estimating phylogenies from morphological data, just as it is with molecular data. Furthermore, we argue that adopting emerging approaches for investigating dissonance in genomic datasets may provide new insights into the integration and evolution of anatomical complexes. [Apidae; entropy; morphological modules; phenotypic integration; phylogenetic information.].

Partitioned Gene-Tree Analyses and Gene-Based Topology Testing Help Resolve Incongruence in a Phylogenomic Study of Host-Specialist Bees (Apidae: Eucerinae).

Incongruence among phylogenetic results has become a common occurrence in analyses of genome-scale data sets. Incongruence originates from uncertainty in underlying evolutionary processes (e.g., incomplete lineage sorting) and from difficulties in determining the best analytical approaches for each situation. To overcome these difficulties, more studies are needed that identify incongruences and demonstrate practical ways to confidently resolve them. Here, we present results of a phylogenomic study based on the analysis 197 taxa and 2,526 ultraconserved element (UCE) loci. We investigate evolutionary relationships of Eucerinae, a diverse subfamily of apid bees (relatives of honey bees and bumble bees) with >1,200 species. We sampled representatives of all tribes within the group and >80% of genera, including two mysterious South American genera, Chilimalopsis and Teratognatha. Initial analysis of the UCE data revealed two conflicting hypotheses for relationships among tribes. To resolve the incongruence, we tested concatenation and species tree approaches and used a variety of additional strategies including locus filtering, partitioned gene-trees searches, and gene-based topological tests. We show that within-locus partitioning improves gene tree and subsequent species-tree estimation, and that this approach, confidently resolves the incongruence observed in our data set. After exploring our proposed analytical strategy on eucerine bees, we validated its efficacy to resolve hard phylogenetic problems by implementing it on a published UCE data set of Adephaga (Insecta: Coleoptera). Our results provide a robust phylogenetic hypothesis for Eucerinae and demonstrate a practical strategy for resolving incongruence in other phylogenomic data sets.

Illustrated catalogue of type specimens of insects (Hexapoda) at Coleção Entomológica "Prof. J.M.F.Camargo" (RPSP), Universidade de São Paulo, Brazil.

The present catalogue lists the insect types (Hexapoda) deposited at Coleção Entomológica "Prof. J.M.F.Camargo" (RPSP), Universidade de São Paulo, Ribeirão Preto, Brazil. This collection is known as one of the most significant depositories of stingless bees (Hymenoptera: Apidae: Meliponini) for the Brazilian and Neotropical faunas, largely because of the legacy of Professor João Franco Maria de Camargo (in memoriam) and co-workers. The Meliponini constitute the most emblematic portion of the collection, comprising 3,335 type-specimens (66 holotypes, 3,254 paratypes, and 15 paralectotypes), which represent 132 species-names. In addition to stingless bees, 495 type specimens of other Hymenoptera (23 holotypes and 472 paratypes) are deposited at RPSP representing 71 hymenopteran species-names: Agaonidae (16 names), Andrenidae (3 names), non-Meliponini Apidae (21 names), Chrysididae (2 names), Halictidae (16 names), Colletidae (5 names), Megachilidae (5 names), Melittidae (1 name), Pteromalidae (1 name), and Vespidae (1 name); the only other insect order currently represented by types at RPSP is Diptera (Drosophilidae: 2 names). Altogether, there currently are 3,832 type-specimens deposited at RPSP. Label data and additional information from the RPSP registers, literature sources, and taxonomic remarks are given, including photographs of name bearing types and representatives of other type specimens of the species herein considered.

A comparative study of the pharyngeal plate of Apoidea (Hymenoptera: Aculeata), with implications for the understanding of phylogenetic relationships of bees.

The pharyngeal plate is a morphological complex with extensive anatomical variation among bees and, therefore, potential as a source of phylogenetic information. The pharyngeal plate of bees is divided into four morphologically distinct regions: sitophore, hypopharyngeal lobe, pharyngeal rods, and median oral plate. In this work we illustrate and document in detail for the first time the pharyngeal plate of 43 bee species, providing descriptions of the morphological variation and contrasting these findings with representatives of apoid wasps (Crabronidae and Sphecidae). We evaluate and discuss the potential of this structure as a rich source of morphological information in the context of bee phylogeny and any research potentially impacted by comparative morphological data. The shape of the hypopharyngeal lobe is highly variable among suprageneric taxa of bees and can be readily employed to characterise taxa at various levels. We argue that the global patterns in the variation of the pharyngeal plate can provide information for phylogenetic inference within bees and constructed and coded 10 characters that encompass the most noticeable morphological differences discussed herein.

Looking beyond the flowers: associations of stingless bees with sap-sucking insects.

The main sources of food for stingless bees are the nectar and pollen harvested from flowers, whereas one important kind of nesting material (i.e. wax) is produced by their own abdominal glands. Stingless bees can, nonetheless, obtain alternative resources of food and wax from exudates released by sap-sucking insects as honeydew and waxy cover, respectively. To date, there are no comprehensive studies investigating how diversified and structured the network interactions between stingless bees and sap-sucking insects are. Here, we conducted a survey of the data on relationship between stingless bees and sap-sucking insects to evaluate: (1) which resources are collected by which stingless bee species; (2) how diverse the interaction network is, using species degree and specialisation index as a proxy; and if (3) there would be any phylogenetic signal in the species degree and specialisation indices. Our findings demonstrate that approximately 21 stingless bee species like Trigona spp. and Oxytrigona spp. have been observed interacting with 11 sap-sucking species, among which Aethalion reticulatum is the main partner. From ca. 50 records, Brazil is the country with most observations (n = 38) of this type of ecological interaction. We found also that stingless bees harvest fivefold more honeydew than waxy covers on sap-sucking insects. However, we did not find any phylogenetic signal for the occurrence of this interaction, considering species degree and specialisation indices, suggesting that both traits apparently evolved independently among stingless bee species. We suggest that specific ecological demands may drive this opportunistic behaviour exhibited by stingless bees, because major sources of food are obtained from flowers and these bees produce their own wax.

Combining transcriptomes and ultraconserved elements to illuminate the phylogeny of Apidae.

Two increasingly popular approaches to reconstruct the Tree of Life involve whole transcriptome sequencing and the target capture of ultraconserved elements (UCEs). Both methods can be used to generate large, multigene datasets for analysis of phylogenetic relationships in non-model organisms. While targeted exon sequencing across divergent lineages is now a standard method, it is still not clear if UCE data can be readily combined with published transcriptomes. In this study, we evaluate the combination of UCEs and transcriptomes in a single analysis using genome-, transcriptome-, and UCE data for 79 bees in the largest and most biologically diverse bee family, Apidae. Using existing tools, we first developed a workflow to assemble phylogenomic data from different sources and produced two large nucleotide matrices of combined data. We then reconstructed the phylogeny of the Apidae using concatenation- and coalescent-based methods, and critically evaluated the resulting phylogenies in the context of previously published genetic, genomic, and morphological data sets. Our estimated phylogenetic trees are robustly supported and largely congruent with previous molecular hypotheses, from deep nodes to shallow species-level phylogenies. Moreover, the combined approach allows us to resolve controversial nodes of the apid Tree of Life, by clarifying the relationships among the genera of orchid bees (Euglossini) and the monophyly of the Centridini. Additionally, we present novel phylogenetic evidence supporting the monophyly of the diverse clade of cleptoparasitic Apidae and the placement of two enigmatic, oil-collecting genera (Ctenoplectra and Tetrapedia). Lastly, we propose a revised classification of the family Apidae that reflects our improved understanding of apid higher-level relationships.

Are the TTAGG and TTAGGG telomeric repeats phylogenetically conserved in aculeate Hymenoptera?

Despite the (TTAGG)n telomeric repeat supposed being the ancestral DNA motif of telomeres in insects, it was repeatedly lost within some insect orders. Notably, parasitoid hymenopterans and the social wasp Metapolybia decorata (Gribodo) lack the (TTAGG)n sequence, but in other representatives of Hymenoptera, this motif was noticed, such as different ant species and the honeybee. These findings raise the question of whether the insect telomeric repeat is or not phylogenetically predominant in Hymenoptera. Thus, we evaluated the occurrence of both the (TTAGG)n sequence and the vertebrate telomere sequence (TTAGGG)n using dot-blotting hybridization in 25 aculeate species of Hymenoptera. Our results revealed the absence of (TTAGG)n sequence in all tested species, elevating the number of hymenopteran families lacking this telomeric sequence to 13 out of the 15 tested families so far. The (TTAGGG)n was not observed in any tested species. Based on our data and compiled information, we suggest that the (TTAGG)n sequence was putatively lost in the ancestor of Apocrita with at least two subsequent independent regains (in Formicidae and Apidae).

Repeated evolution of soldier sub-castes suggests parasitism drives social complexity in stingless bees.

The differentiation of workers into morphological castes represents an important evolutionary innovation that is thought to improve division of labor in insect societies. Given the potential benefits of task-related worker differentiation, it is puzzling that physical worker castes, such as soldiers, are extremely rare in social bees and absent in wasps. Following the recent discovery of soldiers in a stingless bee, we studied the occurrence of worker differentiation in 28 stingless bee species from Brazil and found that several species have specialized soldiers for colony defence. Our results reveal that worker differentiation evolved repeatedly during the last ~ 25 million years and coincided with the emergence of parasitic robber bees, a major threat to many stingless bee species. Furthermore, our data suggest that these robbers are a driving force behind the evolution of worker differentiation as targets of robber bees are four times more likely to have nest guards of increased size than non-targets. These findings reveal unexpected diversity in the social organization of stingless bees.Although common in ants and termites, worker differentiation into physical castes is rare in social bees and unknown in wasps. Here, Grüter and colleagues find a guard caste in ten species of stingless bees and show that the evolution of the guard caste is associated with parasitization by robber bees.

The Neotropical cuckoo wasp genus Ipsiura Linsenmaier, 1959 (Hymenoptera: Chrysididae): revision of the species occurring in Brazil.

The species of the chrysidid genus Ipsiura are reviewed with emphasis on the taxa occurring in Brazil. In the present study 34 Ipsiura species are recognized, diagnosed, and illustrated. Two new species are described here: Ipsiura bohartiana Lucena sp. nov. and I. duckeana Lucena sp. nov., and two others are transferred from Neochrysis to Ipsiura: I. assecia (Linsenmaier, 1997), comb. nov. and I. guayanensis (Linsenmaier, 1997), comb. nov., increasing to 41 the total of valid species in the genus. New diagnoses and redescriptions are provided for 34 species based on study of their types. For the first time, a comparative and illustrated study of male genitalia is presented for the majority of Ipsiura species. Notes on types and depository collections, a revised key for identification of species along with illustrations of diagnostic features, as well as geographical distribution maps are also given.