Müllerian mimicry among bees and wasps: a review of current knowledge and future avenues of research.

Many bees and stinging wasps, or aculeates, exhibit striking colour patterns or conspicuous coloration, such as black and yellow stripes. Such coloration is often interpreted as an aposematic signal advertising aculeate defences: the venomous sting. Aposematism can lead to Müllerian mimicry, the convergence of signals among different species unpalatable to predators. Müllerian mimicry has been extensively studied, notably on Neotropical butterflies and poison frogs. However, although a very high number of aculeate species harbour putative aposematic signals, aculeates are under-represented in mimicry studies. Here, we review the literature on mimicry rings that include bee and stinging wasp species. We report over a hundred described mimicry rings, involving a thousand species that belong to 19 aculeate families. These mimicry rings are found all throughout the world. Most importantly, we identify remaining knowledge gaps and unanswered questions related to the study of Müllerian mimicry in aculeates. Some of these questions are specific to aculeate models, such as the impact of sociality and of sexual dimorphism in defence levels on mimicry dynamics. Our review shows that aculeates may be one of the most diverse groups of organisms engaging in Müllerian mimicry and that the diversity of aculeate Müllerian mimetic interactions is currently under-explored. Thus, aculeates represent a new and major model system to study the evolution of Müllerian mimicry. Finally, aculeates are important pollinators and the global decline of pollinating insects raises considerable concern. In this context, a better understanding of the impact of Müllerian mimicry on aculeate communities may help design strategies for pollinator conservation, thereby providing future directions for evolutionary research.

Biology of the southern giant hornet, Vespa soror: nest architecture, morphological differences among castes, and the genetic structure of colonies.

Giant hornets in the genus Vespa are apex predators that are known throughout Asia for their exceptional size and devastating group attacks on social insect colonies. The giant hornets include Vespa mandarinia, a well-studied and widespread temperate species, and Vespa soror, a poorly known sister species that is limited to subtropical and tropical regions of Southeast Asia. Both species have been recently documented on the west coast of North America, raising urgent questions about their potential impact in novel ecosystems. To better understand the biology of V. soror, we describe the nest architecture, caste morphology, and genetic structure of colonies collected in Vietnam. Comparisons of colony metrics between the two giant hornet species suggest important differences that are likely a consequence of the relatively warmer climate in which V. soror occurs. Like V. mandarinia, V. soror constructs large, underground nests of partially enveloped horizontal combs. However, compared to temperate V. mandarinia colonies, the longer nesting period of subtropical V. soror colonies likely resulted in relatively larger colony sizes and nests by the end of their annual cycle. Vespa soror workers and gynes were larger than males, distinguishable based on wing shape and body size (total length and measures of six body parts), and equivalent in size to female castes of V. mandarinia. We genotyped colony members from three mature nests, which revealed that males and females were offspring of singly mated queens. Two colonies were monogynous, but one colony was comprised of two unrelated matrilines. Polygyny has not been observed for V. mandarinia, but is more common in tropical hornet species. Our study sheds light on essential details about the biology of an understudied species of giant hornet, whose populous colonies and long nesting period suggest the potential for substantial ecological impact wherever they occur.

Seasonal Variations of Pollinator Assemblages among Urban and Rural Habitats: A Comparative Approach Using a Standardized Plant Community.

Even though urban green spaces may host a relatively high diversity of wild bees, urban environments impact the pollinator taxonomic and functional diversity in a way that is still misunderstood. Here, we provide an assessment of the taxonomic and functional composition of pollinator assemblages and their response to urbanization in the Paris region (France). We performed a spring-to-fall survey of insect pollinators in green spaces embedded in a dense urban matrix and in rural grasslands, using a plant setup standardized across sites and throughout the seasons. We compared pollinator species composition and the occurrence of bee functional traits over the two habitats. There was no difference in species richness between habitats, though urban assemblages were dominated by very abundant generalist species and displayed a lower evenness. They also included fewer brood parasitic, solitary or ground-nesting bees. Overall, bees tended to be larger in the city than in the semi-natural grasslands, and this trait exhibited seasonal variations. The urban environment filters out some life history traits of insect pollinators and alters their seasonal patterns, likely as a result of the fragmentation and scarcity of feeding and nesting resources. This could have repercussions on pollination networks and the efficiency of the pollination function.

Wasp Waist and Flight: Convergent Evolution in Wasps Reveals a Link between Wings and Body Shapes.

Insect flight is made possible by different morphological structures: wings produce the lift, the thorax drives the wings' movements, and the abdomen serves as a secondary control device. As such, the covariation of these structures could reflect functional constraints related to flight performances. This study examines evolutionary convergences in wasp body shapes to provide the first evidence for morphological integration among insect wings, thorax, and abdomen. The shapes of the forewings and hind wings, thorax, and petiole (connecting abdomen and thorax) of 22 Vespidae species were analyzed using computerized tomography and geometric morphometrics. Results show a clear relationship between petiole and wings or thorax shapes but not between wings and thorax. Wasps with elongated bodies have pointed wings, both features thought to improve flight maneuverability. In contrast, stouter species have rounded wings, which may allow for higher flight speeds. These integration patterns suggest that multiple selective regimes on flight performance, some of them biased toward maneuverability or maximal speed, drove the morphological diversity in Vespidae. The results also suggest that wing shapes evolved under constraints related to the body type they have to lift. The abdomen morphology is thus another factor to take into account to understand the flight performance of insects.

Running in circles in phylomorphospace: host environment constrains morphological diversification in parasitic wasps.

Understanding phenotypic diversification and the conditions that spur morphological novelty or constraint is a major theme in evolutionary biology. Unequal morphological diversity between sister clades can result from either differences in the rate of morphological change or in the ability of clades to explore novel phenotype ranges. We combine an existing phylogenetic framework with new phylogenomic data and geometric morphometrics to explore the relative roles of rate versus mode of morphological evolution for a hyperdiverse group: cryptine ichneumonid wasps. Data from genomic ultraconserved elements confirm that cryptines are divided into two large clades: one specialized in the use of hosts that are deeply concealed under hard substrates, and another with a much more diversified host range. Using a phylomorphospace approach, we show that both clades have experienced similar rates of morphological evolution. Nonetheless, the more specialized group is much more restricted in morphospace occupation, indicating that it repeatedly evolved morphological change through the same morphospace regions. This is in agreement with our prediction that host use imposes constraints in the morphospace available to lineages, and reinforces an important distinction between evolutionary stasis as opposed to a scenario of continual morphological change restricted to a certain range of morphotypes.

Testing the Dutilleul syndrome: host use drives the convergent evolution of multiple traits in parasitic wasps.

Common life-history aspects among independent lineages often result in the repeated evolution of suites of adaptive traits, or 'syndromes'. Such syndromes can be key avenues to understand relationships between morphological and ecological traits, but are rarely tested due to insufficient trait shift repetitions. We use a hyperdiverse lineage to investigate the evolution of a syndrome. Cryptine ichneumonid wasps that parasitize insects concealed in hard substrates display several traits that are putative adaptations to that end. Using a phylogenetic framework from a combined multigene molecular and morphological data set with 308 cryptine species, we tested whether these traits were part of a morphofunctional syndrome related to host use. Ancestral state estimations show multiple origins for six investigated traits, which are correlated to each other and to the use of deeply concealed hosts, suggesting adaptation. Putatively adaptive traits showed a much stronger link among themselves than with an assemblage of 49 other morphological traits. However, estimation of the order of evolution in adaptive traits showed no structured pattern. The results indicate that the challenge of attacking deeply concealed hosts induced the repeated evolution of a 'Dutilleul syndrome', named after the 'walker-through-walls' character from French literature. They also point towards a dynamic scenario in the evolution of complex functional systems. These findings highlight the power of morphology to illuminate poorly known aspects of natural history, and how hyperdiverse lineages can be used to understand the evolution of complex traits.

Comprehensive evolutionary analysis of the Anthroherpon radiation (Coleoptera, Leiodidae, Leptodirini).

The genus Anthroherpon Reitter, 1889 exhibits the most pronounced troglomorphic characters among Coleoptera, and represents one of the most spectacular radiations of subterranean beetles. However, radiation, diversification, and biogeography of this genus have never been studied in a phylogenetic context. This study provides a comprehensive evolutionary analysis of the Anthroherpon radiation, using a dated molecular phylogeny as a framework for understanding Anthroherpon diversification, reconstructing the ancestral range, and exploring troglomorphic diversity. Based on 16 species and 22 subspecies, i.e. the majority of Anthroherpon diversity, we reconstructed the phylogeny using Bayesian analysis of six loci, both mitochondrial and nuclear, comprising a total of 4143 nucleotides. In parallel, a morphometric analysis was carried out with 79 landmarks on the body that were subjected to geometric morphometrics. We optimized morphometric features to phylogeny, in order to recognize the way troglomorphy was expressed in different clades of the tree, and did character evolution analyses. Finally, we reconstructed the ancestral range of the genus using BioGeoBEARS. Besides further elucidating the suprageneric classification of the East-Mediterranean Leptodirini, our main findings also show that Anthroherpon dates back to the Early Miocene (ca. 22 MYA) and that the genus diversified entirely underground. Biogeographic reconstruction of the ancestral range shows the origin of the genus in the area comprising three high mountains in western Montenegro, which is in the accordance with the available data on the paleogeography of the Balkan Peninsula. Character evolution analysis indicates that troglomorphic morphometric traits in Anthroherpon mostly evolve neutrally but may diverge adaptively under syntopic competition.

Phylogeny, landmark analysis and the use of wing venation to study the evolution of social wasps (Hymenoptera: Vespidae: Vespinae).

Wing venation provides useful characters with which to classify extant and fossil insects. Recently, quantification of its shape using landmarks has increased the potential of wing venation to distinguish taxa. However, the use of wing landmarks in phylogenetic analyses remains largely unexplored. Here, we tested landmark analysis under parsimony (LAUP) to include wing shape data in a phylogenetic analysis of hornets and yellow jackets. Using 68 morphological characters, nine genes and wing landmarks, we produced the first total-evidence phylogeny of Vespinae. We also tested the influence of LAUP parameters using simulated landmarks. Our data confirmed that optimization parameters, alignment method, landmark number and, under low optimization parameters, the initial orientation of aligned shapes can influence LAUP results. Furthermore, single landmark configurations never accurately reflected the topology used for data simulation, but results were significantly close when compared to random topologies. Thus, wing landmark configurations were unreliable phylogenetic characters when treated independently, but provided some useful insights when combined with other data. Our phylogeny corroborated the monophyly of most groups proposed on the basis of morphology and showed the fossil Palaeovespa is distantly related to extant genera. Unstable relationships among genera suggest that rapid radiations occurred in the early history of the Vespinae.

Phylogenetic tests reject Emery's rule in the evolution of social parasitism in yellowjackets and hornets (Hymenoptera: Vespidae, Vespinae).

Social parasites exploit the brood-care behaviour and social structure of one or more host species. Within the social Hymenoptera there are different types of social parasitism. In its extreme form, species of obligate social parasites, or inquilines, do not have the worker caste and depend entirely on the workers of a host species to raise their reproductive offspring. The strict form of Emery's rule states that social parasites share immediate common ancestry with their hosts. Moreover, this rule has been linked with a sympatric origin of inquilines from their hosts. Here, we conduct phylogenetic analyses of yellowjackets and hornets based on 12 gene fragments and evaluate competing evolutionary scenarios to test Emery's rule. We find that inquilines, as well as facultative social parasites, are not the closest relatives of their hosts. Therefore, Emery's rule in its strict sense is rejected, suggesting that social parasites have not evolved sympatrically from their hosts in yellowjackets and hornets. However, the relaxed version of the rule is supported, as inquilines and their hosts belong to the same Dolichovespula clade. Furthermore, inquilinism has evolved only once in Dolichovespula.

Patriline Differences Reveal Genetic Influence on Forewing Size and Shape in a Yellowjacket Wasp (Hymenoptera: Vespidae: Vespula flavopilosa Jacobson, 1978).

The wing venation is frequently used as a morphological marker to distinguish biological groups among insects. With geometric morphometrics, minute shape differences can be detected between closely related species or populations, making this technique useful for taxonomy. However, the direct influence of genetic differences on wing morphology has not been explored within colonies of social insects. Here, we show that the father's genotype has a direct effect on wing morphology in colonies of social wasps. Using geometric morphometrics on the venation pattern, we found significant differences in wing size and shape between patrilines of yellowjackets, taking allometry and measurement error into account. The genetic influence on wing size accounted for a small part of the overall size variation, but venation shape was highly structured by the differences between patrilines. Overall, our results showed a strong genetic influence on wing morphology likely acting at multiple levels of venation pattern development. This confirmed the pertinence of this marker for taxonomic purposes and suggests this phenotype as a potentially useful marker for phylogenies. This also raises doubts about the strength of selective pressures on this phenotype, which highlights the need to understand better the role of wing venation shape in insect flight.

A new paper wasp from Late Eocene of France (Hymenoptera: Vespidae: Polistinae).

The new vespid genus and species Palaeopolistes jattioti gen. et. sp. nov. is described from the Late Eocene of Monteils (Gard, France). The new taxon has clear features of the Polistinae but its tribal assignment is uncertain.

Geographic variation of melanisation patterns in a hornet species: genetic differences, climatic pressures or aposematic constraints?

Coloration of stinging insects is often based on contrasted patterns of light and black pigmentations as a warning signal to predators. However, in many social wasp species, geographic variation drastically modifies this signal through melanic polymorphism potentially driven by different selective pressures. To date, surprisingly little is known about the geographic variation of coloration of social wasps in relation to aposematism and melanism and to genetic and developmental constraints. The main objectives of this study are to improve the description of the colour variation within a social wasp species and to determine which factors are driving this variation. Therefore, we explored the evolutionary history of a polymorphic hornet, Vespa velutina Lepeletier, 1836, using mitochondrial and microsatellite markers, and we analysed its melanic variation using a colour space based on a description of body parts coloration. We found two main lineages within the species and confirmed the previous synonymy of V. auraria Smith, 1852, under V. velutina, differing only by the coloration. We also found that the melanic variation of most body parts was positively correlated, with some segments forming potential colour modules. Finally, we showed that the variation of coloration between populations was not related to their molecular, geographic or climatic differences. Our observations suggest that the coloration patterns of hornets and their geographic variations are determined by genes with an influence of developmental constraints. Our results also highlight that Vespa velutina populations have experienced several convergent evolutions of the coloration, more likely influenced by constraints on aposematism and Müllerian mimicry than by abiotic pressures on melanism.