Christophe J. Praz

SPECIALIZED BEES FAIL TO DEVELOP ON NON- HOST POLLEN: DO PLANTS CHEMICALLY PROTECT THEIR POLLEN?

Bees require large amounts of pollen for their own reproduction. While several morphological flower traits are known to have evolved to protect plants against excessive pollen harvesting by bees, little is known on how selection to minimize pollen loss acts on the chemical composition of pollen. In this study, we traced the larval development of four solitary bee species, each specialized on a different pollen source, when reared on non-host pollen by transferring unhatched eggs of one species onto the pollen provisions of another species. Pollen diets of Asteraceae and Ranunculus (Ranunculaceae) proved to be inadequate for all bee species tested except those specialized on these plants. Further, pollen of Sinapis (Brassicaceae) and Echium (Boraginaceae) failed to support larval development in one bee species specialized on Campanula (Campanulaceae). Our results strongly suggest that pollen of these four taxonomic groups possess protective properties that hamper digestion and thus challenge the general view of pollen as an easy-to-use protein source for flower visitors.

The Impact of Molecular Data on Our Understanding of Bee Phylogeny and Evolution

Our understanding of bee phylogeny has improved over the past fifteen years as a result of new data, primarily nucleotide sequence data, and new methods, primarily model-based methods of phylogeny reconstruction. Phylogenetic studies based on single or, more commonly, multilocus data sets have helped resolve the placement of bees within the superfamily Apoidea; the relationships among the seven families of bees; and the relationships among bee subfamilies, tribes, genera, and species. In addition, molecular phylogenies have played an important role in inferring evolutionary patterns and processes in bees. Phylogenies have provided the comparative framework for understanding the evolution of host-plant associations and pollen specialization, the evolution of social behavior, and the evolution of parasitism. In this paper, we present an overview of significant discoveries in bee phylogeny based primarily on the application of molecular data. We review the phylogenetic hypotheses family-by-family and then describe how the new phylogenetic insights have altered our understanding of bee biology.

Why do leafcutter bees cut leaves? New insights into the early evolution of bees

Stark contrasts in clade species diversity are reported across the tree of life and are especially conspicuous when observed in closely related lineages. The explanation for such disparity has often been attributed to the evolution of key innovations that facilitate colonization of new ecological niches. The factors underlying diversification in bees remain poorly explored. Bees are thought to have originated from apoid wasps during the Mid-Cretaceous, a period that coincides with the appearance of angiosperm eudicot pollen grains in the fossil record. The reliance of bees on angiosperm pollen and their fundamental role as angiosperm pollinators have contributed to the idea that both groups may have undergone simultaneous radiations. We demonstrate that one key innovation—the inclusion of foreign material in nest construction—underlies both a massive range expansion and a significant increase in the rate of diversification within the second largest bee family, Megachilidae. Basal clades within the family are restricted to deserts and exhibit plesiomorphic features rarely observed among modern bees, but prevalent among apoid wasps. Our results suggest that early bees inherited a suite of behavioural traits that acted as powerful evolutionary constraints. While the transition to pollen as a larval food source opened an enormous ecological niche for the early bees, the exploitation of this niche and the subsequent diversification of bees only became possible after bees had evolved adaptations to overcome these constraints.

Patterns of Host-Plant Choice in Bees of the Genus Chelostoma: The Constraint Hypothesis of Host-Range Evolution in Bees

Abstract To trace the evolution of host-plant choice in bees of the genus Chelostoma (Megachilidae), we assessed the host plants of 35 Palearctic, North American and Indomalayan species by microscopically analyzing the pollen loads of 634 females and reconstructed their phylogenetic history based on four genes and a morphological dataset, applying both parsimony and Bayesian methods. All species except two were found to be strict pollen specialists at the level of plant family or genus. These oligolectic species together exploit the flowers of eight different plant orders that are distributed among all major angiosperm lineages. Based on ancestral state reconstruction, we found that oligolecty is the ancestral state in Chelostoma and that the two pollen generalists evolved from oligolectic ancestors. The distinct pattern of host broadening in these two polylectic species, the highly conserved floral specializations within the different clades, the exploitation of unrelated hosts with a striking floral similarity as well as a recent report on larval performance on nonhost pollen in two Chelostoma species clearly suggest that floral host choice is physiologically or neurologically constrained in bees of the genus Chelostoma. Based on this finding, we propose a new hypothesis on the evolution of host range in bees.

Phylogeny and biogeography of bees of the tribe Osmiini (Hymenoptera: Megachilidae)

The Osmiini (Megachilidae) constitute a taxonomically and biologically diverse tribe of bees. To resolve their generic and suprageneric relationships, we inferred a phylogeny based on three nuclear genes (Elongation factor 1-alpha, LW-rhodopsin and CAD) applying both parsimony and Bayesian methods. Our phylogeny, which includes 95 osmiine species representing 18 of the 19 currently recognized genera, is well resolved with high support for most basal nodes. The core osmiine genera were found to form a well-supported monophyletic group, but four small genera, Noteriades, Afroheriades,Pseudoheriades and possibly Ochreriades, formerly included in the Osmiini, do not appear to belong within this tribe. Our phylogeny results in the following taxonomic changes: Stenosmia and Hoplosmia are reduced to subgeneric rank in Hoplitis and Osmia, respectively, Micreriades is recognized as a subgenus in Hoplitis and the subgenus Nasutosmia is transferred from Hoplitis to Osmia. We inferred a biogeographic scenario for the Osmiini applying maximum likelihood inference and models of character evolution. We provide evidence that the Osmiini originated in the Palearctic, and that extensive exchanges occurred between the Palearctic and the Nearctic. The latter finding may relate to the fact that many osmiine species nest in wood or in stems, facilitating dispersal by overseas transport of the nests.

Phylogeny of the bee family Megachilidae (Hymenoptera: Apoidea) based on adult morphology

Phylogenetic relationships within the bee family Megachilidae are poorly understood. The monophyly of the subfamily Fideliinae is questionable, the relationships among the tribes and subtribes in the subfamily Megachilinae are unknown, and some extant genera cannot be placed with certainty at the tribal level. Using a cladistic analysis of adult external morphological characters, we explore the relationships of the eight tribes and two subtribes currently recognised in Megachilidae. Our dataset included 80% of the extant generic‐level diversity, representatives of all fossil taxa, and was analysed using parsimony. We employed 200 characters and selected 7 outgroups and 72 ingroup species of 60 genera, plus 7 species of 4 extinct genera from Baltic amber. Our analysis shows that Fideliinae and the tribes Anthidiini and Osmiini of Megachilinae are paraphyletic; it supports the monophyly of Megachilinae, including the extinct taxa, and the sister group relationship of Lithurgini to the remaining megachilines. The Sub‐Saharan genus Aspidosmia, a rare group with a mixture of osmiine and anthidiine features, is herein removed from Anthidiini and placed in its own tribe, Aspidosmiini, new tribe. Protolithurgini is the sister of Lithurgini, both placed herein in the subfamily Lithurginae; the other extinct taxa, Glyptapina and Ctenoplectrellina, are more basally related among Megachilinae than Osmiini, near Aspidosmia, and are herein treated at the tribal level. Noteriades, a genus presently in the Osmiini, is herein transferred to the Megachilini. Thus, we recognise four subfamilies (Fideliinae, Pararhophitinae, Lithurginae and Megachilinae) and nine tribes in Megachilidae. We briefly discuss the evolutionary history and biogeography of the family, present alternative classifications, and provide a revised key to the extant tribes of Megachilinae.

Host recognition in a pollen-specialist bee: evidence for a genetic basis

To investigate the effect of larval pollen diet on floral choice in a specialized bee species, we compared the floral preferences of individuals of Heriades truncorum (Megachilidae) reared on host pollen with those of individuals reared on two different types of non-host pollen. Females were allowed to nest in cages where both host and non-host flowers were available. All females, regardless of larval diet, restricted pollen collection to their host, although they visited the flowers of both host and non-host plants for nectar. When offered only the non-host pollen source, females ceased nesting activities. Males reared on non-host pollen exclusively restricted their patrolling flights to flowers of their normal host. This study provides the first empirical investigation of the imprinting theory in oligolectic bees, and unambiguously suggests that host recognition has a genetic basis in H. truncorum. We discuss the implication of this finding for the understanding of bee-flower relationships.ZusammenfassungAuf bestimmte Pollenarten spezialisierte Bienen zeigen bereits als naive Imagines Präferenzen für den Pollen ihrer Wirtsarten oder für spezifische Pollenduftstoffe. Eine wichtige Frage ist hierbei, ob bei diesen solitären Bienen die Präferenzen für Pollenduftstoffe angeboren sind und damit eine genetische Grundlage haben, oder ob sie das Ergebnis einer präimaginalen oder frühimaginalen Konditionierung sind (Prägungstheorie). In ihren Brutzellen, in denen die Entwicklung vom Ei bis zur Imago erfolgt, sind diese Bienen in der Tat sowohl als Larven als auch als frischgeschlüpfte Adulte ständig in Kontakt mit Pollenduftstoffen. Obwohl die Prägungstheorie in der Literatur verschiedentlich angesprochen wurde, wurde sie noch nie an einer pollenspezialisierten Biene überprüft. Wir untersuchten die Rolle der larvalen Pollennahrung auf die Wirtpflanzenwahl bei Heriades truncorum, einer auf Asteraceen spezialisierten Biene. Dabei verglichen wir die Blütenpräferenzen von Bienen, die auf Wirtspollen aufgezogen wurden, mit denen, die auf Nicht-wirtspollen aufgezogen wurden, insbesondere auf Pollen von Echium (Boraginaceae) und auf Pollen von Campanula (Campanulaceae). Zur Aufzucht von Larven auf diesen Nichtwirtspollen übertrugen wir noch ungeschlüpfte Eier von H. truncorum auf Pollenvorräte, die von zwei anderen oligolektischen Bienenarten angelegt worden waren. In den künstlichen Zellen wuchsen die aus den transferierten Eiern geschlüpften Larven heran, überwinterten und entwickelten sich zu Puppen. Nachdem die Imagines geschlüpft waren, konnten sie sich verpaaren und dann in Käfigen nisten, in denen ihnen sowohl Wirtsals auch Nichtwirtspflanzen angeboten wurden. Unabhängig vom Pollen, auf dem sie als Larven aufgezogen worden waren, sammelten alle Weibchen auschliesslich auf ihrer Wirtsart Pollen, während sie Nektar sowohl auf der Wirtsais auch den Nichtwirtsarten sammelten. Wenn ihnen nur Nichtwirtspflanzen als Pollenquelle angeboten wurden, stellten die Weibchen sofort die Nistaktivitäten ein. In ähnlicher Weise führten auch die Männchen ihre Patrouillienflüge ausschliesslich auf Wirtspflanzen durch, selbst wenn sie auf Nichtwirtspollen aufgezogen worden waren. Unsere Ergebnisse sind demzufolge ein eindeutiger Hinweis auf eine genetische Grundlage der Wirtserkennung bei H. truncorum und haben damit wichtige Implikationen für unser Verständnis der Evolution von Bienen/Pflanzen-Beziehungen. Unter der Annahme, dass die Wirtserkennung auf Prägung beruht, sollten Adulte, die sich z.B. infolge aus Mangel ihrer Wirts art auf Nichtwirtspollen entwickelt haben, die Wirtsart schnell wechseln und dieser neuen Art dann treu bleiben. Dieser Prozess könnte zur Bildung isolierter Wirtsrassen führen, da die Männchen solch spezialisierter Bienen dann auf der neuen Wirtsart nach Weibchen suchen würden. Im entgegengesetzten Fall einer genetischen Basis der Wirtserkennung, wie wir sie für H. truncorum in der dieser Studie nachweisen konnten, würden einem Wirtswechsel andere Mechanismen zugrundeliegen, wie z.B. geographische Isolation oder neurale Fixierung. In der Tat weigerten sich die Weibchen von H. truncorum, auf Nichtwirtspflanzen Pollen zu sammeln, obwohl sich dieser als für die Brutaufzucht geeignet erwiesen hatte. Dies ist ein Hinweis darauf, dass für diese Art neurale Beschränkungen für die Ausprägung des Wirtsspektrums wichtiger sind als Einschränkungen in der Ernährung.

Phylogenomics Controlling for Base Compositional Bias Reveals a Single Origin of Eusociality in Corbiculate Bees

As increasingly large molecular data sets are collected for phylogenomics, the conflicting phylogenetic signal among gene trees poses challenges to resolve some difficult nodes of the Tree of Life. Among these nodes, the phylogenetic position of the honey bees (Apini) within the corbiculate bee group remains controversial, despite its considerable importance for understanding the emergence and maintenance of eusociality. Here, we show that this controversy stems in part from pervasive phylogenetic conflicts among GC-rich gene trees. GC-rich genes typically have a high nucleotidic heterogeneity among species, which can induce topological conflicts among gene trees. When retaining only the most GC-homogeneous genes or using a nonhomogeneous model of sequence evolution, our analyses reveal a monophyletic group of the three lineages with a eusocial lifestyle (honey bees, bumble bees, and stingless bees). These phylogenetic relationships strongly suggest a single origin of eusociality in the corbiculate bees, with no reversal to solitary living in this group. To accurately reconstruct other important evolutionary steps across the Tree of Life, we suggest removing GC-rich and GC-heterogeneous genes from large phylogenomic data sets. Interpreted as a consequence of genome-wide variations in recombination rates, this GC effect can affect all taxa featuring GC-biased gene conversion, which is common in eukaryotes.

ORIGINS, EVOLUTION, AND DIVERSIFICATION OF CLEPTOPARASITIC LINEAGES IN LONG‐TONGUED BEES

The evolution of parasitic behavior may catalyze the exploitation of new ecological niches yet also binds the fate of a parasite to that of its host. It is thus not clear whether evolutionary transitions from free‐living organism to parasite lead to increased or decreased rates of diversification. We explore the evolution of brood parasitism in long‐tongued bees and find decreased rates of diversification in eight of 10 brood parasitic clades. We propose a pathway for the evolution of brood parasitic strategy and find that a strategy in which a closed host nest cell is parasitized and the host offspring is killed by the adult parasite represents an obligate first step in the appearance of a brood parasitic lineage; this ultimately evolves into a strategy in which an open host cell is parasitized and the host offspring is killed by a specialized larval instar. The transition to parasitizing open nest cells expanded the range of potential hosts for brood parasitic bees and played a fundamental role in the patterns of diversification seen in brood parasitic clades. We address the prevalence of brood parasitic lineages in certain families of bees and examine the evolution of brood parasitism in other groups of organisms.

Seedling survival and growth of three ectomycorrhizal caesalpiniaceous tree species in a Central African rain forest

Tree recruitment is determined in part by the survivorship and growth of seedlings. Two seedling cohorts of the three most abundant caesalpiniaceous species forming groves at Korup, Cameroon, were followed from 1995/1997 to 2002, to investigate why Microberlinia bisulcata, the most abundant species, currently has very few recruits compared with Tetraberlinia korupensis and T. bifoliolata. Numbers of seedlings dying, and the heights and leaf numbers of survivors, were recorded on 30 occasions. Survivorship after 2.5 y was 30% for M. bisulcata and 59% for the similar Tetraberlinia spp. together. After 7 y the corresponding values were 4 and 21%. Growth of all species was slow for the first 4 y; but survivors of T. korupensis became 63% taller, as the other species stagnated, by 7 y. The poor recruitment of M. bisulcata was the result of its very low seedling survival. Within species, the tallest seedlings of M. bisulcata and T. bifoliolata, but medium-height ones of T. korupensis, survived longest. This was likely due to higher root allocation in T. korupensis. Seedling dynamics of M. bisulcata and T. korupensis over 7 y accorded well with relative abundances of adult trees; T. bifoliolata is predicted to recruit later.