Nicolas Vereecken

The evolution of imperfect floral mimicry

The theory of mimicry predicts that selection favors signal refinement in mimics to optimally match the signals released by their specific model species. We provide here chemical and behavioral evidence that a sexually deceptive orchid benefits from its mimetic imperfection to its co-occurring and specific bee model by triggering a stronger response in male bees, which react more intensively to the similar, but novel, scent stimulus provided by the orchid.

Pollinator convergence and the nature of species' boundaries in sympatric Sardinian Ophrys (Orchidaceae).

BACKGROUND AND AIMS In the sexually deceptive Ophrys genus, species isolation is generally considered ethological and occurs via different, specific pollinators, but there are cases in which Ophrys species can share a common pollinator and differ in pollen placement on the body of the insect. In that condition, species are expected to be reproductively isolated through a pre-mating mechanical barrier. Here, the relative contribution of pre- vs. post-mating barriers to gene flow among two Ophrys species that share a common pollinator and can occur in sympatry is studied. METHODS A natural hybrid zone on Sardinia between O. iricolor and O. incubacea, sharing Andrena morio as pollinator, was investigated by analysing floral traits involved in pollinator attraction as odour extracts both for non-active and active compounds and for labellum morphology. The genetic architecture of the hybrid zone was also estimated with amplified fragment length polymorphism (AFLP) markers, and pollination fitness and seed set of both parental species and their hybrids in the sympatric zone were estimated by controlled crosses. KEY RESULTS Although hybrids were intermediate between parental species in labellum morphology and non-active odour compounds, both parental species and hybrids produced a similar odour bouquet for active compounds. However, hybrids produced significantly lower fruit and seed set than parental species, and the genetic architecture of the hybrid zone suggests that they were mostly first-generation hybrids. CONCLUSIONS The two parental species hybridize in sympatry as a consequence of pollinator overlap and weak mechanical isolation, but post-zygotic barriers reduce hybrid frequency and fitness, and prevent extensive introgression. These results highlight a significant contribution of late post-mating barriers, such as chromosomal divergence, for maintaining reproductive isolation, in an orchid group for which pre-mating barriers are often considered predominant.

Population differentiation in female sex pheromone and male preferences in a solitary bee

Population differentiation in female mating signals and associated male preferences can drive reproductive isolation among segregated populations. We tested this assumption by investigating intraspecific variation in female sex pheromone and associated male odour preferences among distant populations in the solitary bee Colletes cunicularius (L.) by using quantitative gas chromatography and by performing field bioassays with synthetic blends of key sex pheromone compounds. We found significant differences in sex pheromone blends among the bee populations, and the divergence in odour blends correlated positively with geographic distance, suggesting that genetic divergence among distant populations can affect sex pheromone chemistry. Our behavioural experiments, however, demonstrate that synthetic copies of allopatric female sex pheromones were cross-attractive to patrolling males from distant populations, making reproductive isolation by non-recognition of mating signals among populations unlikely. Our data also show that patrolling male bees from different populations preferred odour types from allopatric populations at the two sites of bioassays. These male preferences are not expected to select for changes in the female sex pheromone, but may influence the evolution of floral odour in sexually deceptive orchids of the genus Ophrys that are pollinated by C. cunicularius males.

On the roles of colour and scent in a specialized floral mimicry system.

BACKGROUND AND AIMS Sexually deceptive orchids achieve cross-pollination by mimicking the mating signals of female insects, generally hymenopterans. This pollination mechanism is often highly specific as it is based primarily on the mimicry of mating signals, especially the female sex pheromones of the targeted pollinator. Like many deceptive orchids, the Mediterranean species Ophrys arachnitiformis shows high levels of floral trait variation, especially in the colour of the perianth, which is either green or white/pinkinsh within populations. The adaptive significance of perianth colour polymorphism and its influence on pollinator visitation rates in sexually deceptive orchids remain obscure. METHODS The relative importance of floral scent versus perianth colour in pollinator attraction in this orchid pollinator mimicry system was evaluated by performing floral scent analyses by gas chromatography-mass spectrometry (GC-MS) and behavioural bioassays with the pollinators under natural conditions were performed. KEY RESULTS The relative and absolute amounts of behaviourally active compounds are identical in the two colour morphs of O. arachnitiformis. Neither presence/absence nor the colour of the perianth (green versus white) influence attractiveness of the flowers to Colletes cunicularius males, the main pollinator of O. arachnitiformis. CONCLUSION Chemical signals alone can mediate the interactions in highly specialized mimicry systems. Floral colour polymorphism in O. arachnitiformis is not subjected to selection imposed by C. cunicularius males, and an interplay between different non-adaptive processes may be responsible for the maintenance of floral colour polymorphism both within and among populations.

Cheaters and liars: Chemical mimicry at its finest

Chemical mimicry is an essential part of certain interspecific interactions, where the outcome for both species may depend on the degree to which the original signals are mimicked. In this review, we discuss a number of specific cases relating to pollination and obtaining nutrient resources that we believe exemplify recent advances in our understanding of chemical mimicry. Subsequently, we suggest avenues for future ecological and chemical research that should allow us to gain further insight into the evolution of chemical mimicry.

Pollination Syndromes in Mediterranean Orchids—Implications for Speciation, Taxonomy and Conservation

The Mediterranean flora is spectacularly rich in orchid species that have evolved remarkable adaptations to their environment. Orchids have complex and delicate interactions with their pollinators, which makes them particularly prone to local extinction. Conservation actions should be encouraged for a range of endangered Mediterranean orchid species, but the current taxonomic confusion in several genera and the apparent disagreement among orchid taxonomists make the situation particularly confusing from a conservation perspective. In this review, we document how the different pollination syndromes of Mediterranean orchids (nectar reward, shelter offering, food deception and sexual deception) can have a profound impact on the type of reproductive barriers among species, on floral phenotypic variation as we perceive it, on potentially related processes of species sorting and extinction and, consequently, should have a strong influence on the related conservation management programs. We also highlight that the majority of Mediterranean orchids are pollinated by specialised bees often occupying otherwise narrow ecological niches (e.g. pollen specialisation, brood cell parasites, specific nesting site). This condition makes the orchid-pollinator interactions very fragile and several orchid species prone to local extinction. We illustrate this phenomenon by a selection of case studies that show how the adequate integration of the ecological requirements/traits of the orchids and their associated pollinators into conservation actions could help protect endangered species and ensure the sustainability of the often complex local pollination web.

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.

A synthesis of gynandromorphy among wild bees (Hymenoptera: Apoidea), with an annotated description of several new cases

Abstract We here describe six new specimens of gynanders (i.e. specimens where male and female phenotypic characters occur on the same individual) from distinct families of wild bees (Hymenoptera, Apoidea). The newly described cases include Melitta haemorrhoidalis (Fabricius 1775) (Melittidae), Dasypoda hirtipes (Fabricius 1775) (Melittidae), Anthophora plumipes (Pallas 1772) (Apidae), Bombus monticola rondoui Vogt 1909 (Apidae), Bombus vestalis vestalis (Fourcroy 1785) (Apidae) and Bombus vestalis sorgonis (Strand 1917) (Apidae). Descriptions are accompanied by behavioural observations of gynanders under natural conditions before their capture for two cases. We also list 109 gynanders already described in bees and we interpret the newly described cases along these previous records. The putative origins of gynandromorphy are then discussed in the light of recent advances in the field of sex determination in Hymenoptera.

Deceptive Behavior in Plants. I. Pollination by Sexual Deception in Orchids: A Host–Parasite Perspective

Sexually deceptive orchids attract male insects as pollinators by mimicking the reproductive signals emitted by the targeted females. Since this mimicry system involves the imitation of female mating signals of certain insects, and since mating signals, especially sex pheromones, generally act on a species-specific basis, theory holds that each sexually deceptive orchid is usually pollinated by only one or a few male insect species. While these orchids rely exclusively on their specialized pollinators for their own reproduction, the male insects derive no benefit from this interaction. In this chapter, I will argue that incorporating questions relevant to the field of animal-centered host–parasite interactions into investigations on the evolutionary ecology of orchid pollination by deception will provide important insights at both the proximate (or mechanistic) and at the ultimate (or evolutionary) levels.