Denis Michez

Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants

Concern about biodiversity loss has led to increased public investment in conservation. Whereas there is a widespread perception that such initiatives have been unsuccessful, there are few quantitative tests of this perception. Here, we evaluate whether rates of biodiversity change have altered in recent decades in three European countries (Great Britain, Netherlands and Belgium) for plants and flower visiting insects. We compared four 20-year periods, comparing periods of rapid land-use intensification and natural habitat loss (1930–1990) with a period of increased conservation investment (post-1990). We found that extensive species richness loss and biotic homogenisation occurred before 1990, whereas these negative trends became substantially less accentuated during recent decades, being partially reversed for certain taxa (e.g. bees in Great Britain and Netherlands). These results highlight the potential to maintain or even restore current species assemblages (which despite past extinctions are still of great conservation value), at least in regions where large-scale land-use intensification and natural habitat loss has ceased.

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.

How Does Pollen Chemistry Impact Development and Feeding Behaviour of Polylectic Bees

Larvae and imagos of bees rely exclusively on floral rewards as a food source but host-plant range can vary greatly among bee species. While oligolectic species forage on pollen from a single family of host plants, polylectic bees, such as bumblebees, collect pollen from many families of plants. These polylectic species contend with interspecific variability in essential nutrients of their host-plants but we have only a limited understanding of the way in which chemicals and chemical combinations influence bee development and feeding behaviour. In this paper, we investigated five different pollen diets (Calluna vulgaris, Cistus sp., Cytisus scoparius, Salix caprea and Sorbus aucuparia) to determine how their chemical content affected bumblebee colony development and pollen/syrup collection. Three compounds were used to characterise pollen content: polypeptides, amino acids and sterols. Several parameters were used to determine the impact of diet on micro-colonies: (i) Number and weight of larvae (total and mean weight of larvae), (ii) weight of pollen collected, (iii) pollen efficacy (total weight of larvae divided by weight of the pollen collected) and (iv) syrup collection. Our results show that pollen collection is similar regardless of chemical variation in pollen diet while syrup collection is variable. Micro-colonies fed on S. aucuparia and C. scoparius pollen produced larger larvae (i.e. better mates and winter survivors) and fed less on nectar compared to the other diets. Pollen from both of these species contains 24-methylenecholesterol and high concentrations of polypeptides/total amino acids. This pollen nutritional “theme” seems therefore to promote worker reproduction in B. terrestris micro-colonies and could be linked to high fitness for queenright colonies. As workers are able to selectively forage on pollen of high chemical quality, plants may be evolutionarily selected for their pollen content, which might attract and increase the degree of fidelity of generalist pollinators, such as bumblebees.

An overview of the Bombus terrestris (L. 1758) subspecies (Hymenoptera: Apidae)

Abstract Bombus terrestris is one of the most abundant bumblebee species in the West-Palaearctic. Its widespread domestication results in the movement of many colonies. The aim of this paper is to describe the 9 subspecies currently recognised and to list some of their most obvious characteristics. Bombus terrestris is not declining anywhere, on the contrary, its synanthropic spread through domestication may be expected. However, its autumn and winter populations rely on a restricted choice of flowers so they may be threatened locally by scrub clearance and the destruction of their favourite autumnal flowers.

Pollen and nectar quality drive the major and minor floral choices of bumble bees

To investigate whether floral resource quality impacts on bumble bee floral choices, we determined the pollen foraging constancy and floral choices of four bumble bee species commonly occurring in peaty, wet meadows in South Belgium. We subsequently analyzed the chemical contents of pollen and nectar, as well as the nectar production of the major host plant species. Individuals of B. lapidarius and B. pascuorum collected high-quality pollen (i.e., having high essential amino acid and phytosterol content) on Comarum palustre and Trifolium pratense, whereas individuals of B. terrestris s.l. and B. hypnorum enlarged their diet breadth to less valuable pollen resources (Cirsium palustre and Valeriana repens). Since Persicaria bistorta and Comarum palustre offer abundant and concentrated nectar, these plant species might represent major nectar sources for bumble bee species in peaty, wet meadows. The present study demonstrated the role of pollen composition on differences in foraging strategies among bumble bee species.

Phylogeny of the bee family Melittidae (Hymenoptera: Anthophila) based on combined molecular and morphological data

The bee family Melittidae comprises a small, but biologically fascinating, group of mostly oligolectic bees, some of which are oil collecting. Phylogenetic relationships within this family are poorly understood and some genera cannot be placed with confidence at the subfamily level. We analysed melittid phylogeny using a combined dataset of five nuclear genes [28S, elongation factor‐1α (EF‐1α, F2 copy), long‐wavelength rhodopsin, Na‐K ATPase and RNA polymerase II] spanning 4842 bp plus 68 adult morphological characters. Our study included 25% of the species‐level diversity and 81% of the generic‐level diversity and included all previously recognized tribes and subfamilies. We analysed the dataset using parsimony, maximum likelihood and Bayesian methods. All methods yielded congruent results. All topologies recovered the three previously recognized subfamilies (Dasypodainae, Melittinae, Meganomiinae), but two genera (Afrodasypoda and Promelitta) are transferred from Dasypodainae to Melittinae. On the basis of our tree topologies we identify four tribes (Dasypodaini comb.n., Hesperapini stat.n., Macropidini comb.n. and Melittini), only one of which (Melittini) matches a widely used classification. Lastly, we discuss the evolution of host‐plant association in the light of our new phylogenetic hypothesis. Our results strongly support multiple independent origins of oil‐collecting behaviour in the Melittinae.

Phylogeny and host-plant evolution in Melittidae s.l. (Hymenoptera: Apoidea)

Bees and the angiosperms they pollinate have developed intimate and often complex interactions over the past 100 million years. As in other insect-plant interactions, host-plant specificity is variable among taxa. While many solitary bee species display an obvious preference for a narrow spectrum of host-plants (oligolecty), others regularly visit a diversified array of pollen hosts (polylecty). Few studies have examined the patterns of host-plant associations in bees using well-resolved phylogenies at the species level combined with accurate and quantitative data on host-plant preferences. In this study, we examined the evolution of bee-plant relationships in several genera of specialist (oligolectic) bees. We used the Melittidae s.l. as a model taxon by mapping the preferred pollen hosts onto species-level phylogenies to investigate the frequency and pattern of host-plant switching. Our results suggest that host-plant associations are maintained over time in many lineages, but that host switches to unrelated plant families are also common. We find some evidence that host-switches occur more frequently to morphologically similar, rather than closely-related, host-plants suggesting that floral morphology plays a key role in host-plant evolution in bees.ZusammenfassungWie viele Gruppen pflanzenfressender Insekten zeigen auch Bienen Variation sowohl in der Wirtspflanzenwahl als auch in der Breite ihrer Wirtspflanzen. Einige Bienen zeigen eine hohe Spezifität in der Blütenwahl (Oligolektie; viele Solitärbienen), während andere ein weites Spektrum in der Blütenwahl aufweisen (Polylektie; die meisten eusozialen Bienen). Nur wenige frühere Studien haben die Muster der Wirtspflanzenwahl in Beziehung zu einer gut aufgelösten Phylogenie auf dem Artniveau untersucht.Wir untersuchten die Vererbung der Wirtspflanzenwahl über ihre evolutionäre Geschichte bei fünf Gattungen von spezialisierten Bienen innerhalb der Melittidae s.l. (Tab. II–V, Capicola, Dasypoda, Hesperapis, Macropis und Melitta). Wir kartierten die bevorzugten Pollenwirte über den Phylogenien auf dem Artniveau (Abb. 2–6). Wir versuchten insbesondere zu ermitteln, ob (i) Verschiebungen der Wirtspflanzen in diesen Kladen spezialisierter Bienen häufig sind, (ii) ob Wirtspflanzenverschiebungen zu entfernt verwandten Wirten vorkommen, (iii) ob Wirtspflanzenverschiebungen mit der Entstehung besonderer morphologischer Anpassungen einhergehen, und (iv) ob die Wirtspflanzenspezialisierung in diesen Gattungen als ursprünglich oder als abgeleitet angesehen werden kann.Wir zeigen, dass nahverwandte Arten in den meisten Fällen ähnliche Wirtspflanzen aufsuchen. Allerdings beobachteten wir in vier der fünf Gattungen Verschiebungen zu nichtverwandten Wirtspflanzen (mit Macropis als der einzigen Ausnahme). Die meisten Wechsel beinhalteten Umstellung von einer Wirtspflanzenfamilie zu einer anderen, nicht verwandten Wirtsfamilie, mit wenig Änderung der Auswahlbreite. Wechsel der Auswahlbreite, wenn sie beobachtet wurden, fanden hauptsächlich von Oligolektie zu Polylektie statt. Wirtspflanzenspezifität erscheint daher bei den melittiden Bienen ein ursprüngliches Verhalten zu sein. In mehreren anderen Bienenfamilien sind die basalen Gruppen ebenfalls oligolektisch (z. B. Lithurginae, Panurginae und Rophitinae). Dies legt den Schluss nahe, dass der ursprüngliche Zustand der Bienen oligolektisch war.

Patterns of genetic and reproductive traits differentiation in Mainland vs. Corsican populations of bumblebees.

Populations on islands often exhibit lower levels of genetic variation and ecomorphological divergence compared to their mainland relatives. While phenotypic differentiation in characters, such as size or shape among insular organisms, has been well studied, insular differentiation in quantitative reproductive traits involved in chemical communication has received very little attention to date. Here, we investigated the impact of insularity on two syntopic bumblebee species pairs: one including species that are phylogenetically related (Bombus terrestris and B. lucorum), and the other including species that interact ecologically (B. terrestris and its specific nest inquiline B. vestalis). For each bumblebee species, we characterized the patterns of variation and differentiation of insular (Corsican) vs. mainland (European) populations (i) with four genes (nuclear and mitochondrial, 3781 bp) and (ii) in the chemical composition of male marking secretions (MMS), a key trait for mate attraction in bumblebees, by gas chromatography-mass spectrometry (GC-MS). Our results provide evidence for genetic differentiation in Corsican bumblebees and show that, contrary to theoretical expectations, island populations of bumblebees exhibit levels of genetic variation similar to the mainland populations. Likewise, our comparative chemical analyses of MMS indicate that Corsican populations of bumblebees are significantly differentiated from the mainland yet they hold comparative levels of within-population MMS variability compared to the mainland. Therefore, insularity has led Corsican populations to diverge both genetically and chemically from their mainland relatives, presumably through genetic drift, but without a decrease of genetic diversity in island populations. We hypothesize that MMS divergence in Corsican bumblebees was driven by a persistent lack of gene flow with mainland populations and reinforced by the preference of Corsican females for sympatric (Corsican) MMS. The impoverished Corsican bumblebee fauna has not led to relaxation of stabilizing selection on MMS but to consistent differentiation chemical reproductive traits on the island.

Scent of a break-up: phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius)

BackgroundThe Pleistocene climatic oscillations are considered as a major driving force of intraspecific divergence and speciation. During Ice Ages, populations isolated in allopatric glacial refugia can experience differentiation in reproductive traits through divergence in selection regimes. This phenomenon may lead to reproductive isolation and dramatically accentuates the consequences of the climatic oscillations on species. Alternatively, when reproductive isolation is incomplete and populations are expanding again, further mating between the formerly isolated populations can result in the formation of a hybrid zone, genetic introgression or reinforcement speciation through reproductive trait displacements. Therefore changes in reproductive traits driven by population movements during climatic oscillations can act as an important force in promoting pre-zygotic isolation. Notwithstanding, divergence of reproductive traits has not been approached in the context of climatic oscillations. Here we investigate the impact of population movements driven by climatic oscillations on a reproductive trait of a bumblebee species (Bombus lapidarius). We characterise the pattern of variation and differentiation across the species distribution (i) with five genes (nuclear and mitochondrial), and (ii) in the chemical composition of male marking secretions (MMS), a key trait for mate attraction in bumblebees.ResultsOur results provide evidence that populations have experienced a genetic allopatric differentiation, in at least three main refugia (the Balkans, Centre-Eastern Europe, and Southern Italy) during Quaternary glaciations. The comparative chemical analyses show that populations from the Southern Italian refugium have experienced MMS differentiation and an incipient speciation process from another refugium. The meeting of Southern Italian populations with other populations as a result of range expansion at a secondary contact zone seems to have led to a reinforcement process on local MMS patterns.ConclusionsThis study suggests that population movement during Quaternary climatic oscillations can lead to divergence in reproductive traits by allopatric differentiation during Ice Ages and by reinforcement during post-glacial recolonization.

Molecular and chemical characters to evaluate species status of two cuckoo bumblebees: Bombus barbutellus and Bombus maxillosus (Hymenoptera, Apidae, Bombini)

Many methods, based on morphological, molecular or chemical characters, have been used to address the question of species taxonomic status. Integrative taxonomy aims to define stronger supported taxonomic hypotheses by considering complementary datasets from different characters. By following an integrative approach, the present study includes molecular, chemical and morphological criteria to establish the taxonomic status of two rare and doubtful cuckoo bumblebee taxa: Bombus (Psithyrus) barbutellus and Bombus (Psithyrus) maxillosus. These two sympatric taxa are discriminated by few morphological criteria (mainly wing darkness and hair length). We used these morphological character diagnoses to establish an a priori status of our samples (23 specimens). We developed a combined molecular dataset from one nuclear gene, elongation factor 1α (EF‐1α), and one mitochondrial gene, cytochrome c oxidase subunit I (COI), spanning 1623 bp, and a chemical dataset of sexual marking pheromones (73 compounds). The molecular data were subjected to maximum‐likelihood and Bayesian phylogenetic inference under partitioned model and maximum parsimony. The chemical data were analysed by clustering and the two‐group k‐means method to test divergences between the two species. The resulting phylogenetic trees show no consistent divergence between the two taxa. Moreover, we found no divergence in the sexual marking pheromones in the clustering and two‐group k‐means analyses. These converging results support the conspecificity of both taxa. Nonetheless, our determinations using the traditional morphological criteria separated our samples into two taxa. We conclude that the morphological criteria seem to relate to intraspecific variations: B. maxillosus is regarded as a syn.n. of B. barbutellus.