A second cuckoo wasp species from the mid-Miocene Zhangpu biota (Hymenoptera: Chrysididae)

BackgroundHost-parasite interactions are among the most important biotic relationships. Host species should evolve mechanisms to detect their enemies and employ appropriate counterstrategies. Parasites, in turn, should evolve mechanisms to evade detection and thus maximize their success. Females of the European beewolf (Philanthus triangulum, Hymenoptera, Crabronidae) hunt exclusively honeybee workers as food for their progeny. The brood cells containing the paralyzed bees are severely threatened by a highly specialized cuckoo wasp (Hedychrum rutilans, Hymenoptera, Chrysididae). Female cuckoo wasps enter beewolf nests to oviposit on paralyzed bees that are temporarily couched in the nest burrow. The cuckoo wasp larva kills the beewolf larva and feeds on it and the bees. Here, we investigated whether H. rutilans evades detection by its host. Since chemical senses are most important in the dark nest, we hypothesized that the cuckoo wasp might employ chemical camouflage.ResultsField observations suggest that cuckoo wasps are attacked by beewolves in front of their nest, most probably after being recognized visually. In contrast, beewolves seem not to detect signs of the presence of these parasitoids neither when these had visited the nest nor when directly encountered in the dark nest burrow.In a recognition bioassay in observation cages, beewolf females responded significantly less frequently to filter paper discs treated with a cuticular extract from H. rutilans females, than to filter paper discs treated with an extract from another cuckoo wasp species (Chrysis viridula). The behavior to paper discs treated with a cuticular extract from H. rutilans females did not differ significantly from the behavior towards filter paper discs treated with the solvent only.We hypothesized that cuckoo wasps either mimic the chemistry of their beewolf host or their host's prey. We tested this hypothesis using GC-MS analyses of the cuticles of male and female beewolves, cuckoo wasps, and honeybee workers. Cuticle extracts of Hedychrum nobile (Hymenoptera: Chrysididae) and Cerceris arenaria (Hymenoptera: Crabronidae) were used as outgroups. There was little congruence with regard to cuticular compounds between H. rutilans females and honeybees as well as females of C. arenaria and H. nobile. However, there was a considerable similarity between beewolf females and H. rutilans females. Beewolf females show a striking dimorphism regarding their cuticular hydrocarbons with one morph having (Z)-9-C25:1 and the other morph having (Z)-9-C27:1 as the major component. H. rutilans females were more similar to the morph having (Z)-9-C27:1 as the main component.ConclusionWe conclude that H. rutilans females closely mimic the composition of cuticular compounds of their host species P. triangulum. The occurrence of isomeric forms of certain compounds on the cuticles of the cuckoo wasps but their absence on beewolf females suggests that cuckoo wasps synthesize the cuticular compounds rather than sequester them from their host. Thus, the behavioral data and the chemical analysis provide evidence that a specialized cuckoo wasp exhibits chemical mimicry of the odor of its host. This probably allows the cuckoo wasp to enter the nest with a reduced risk of being detected by olfaction and without leaving traitorous chemical traces.

Kleptoparasitic and parasitoid insects are expected to be particularly sensitive to changes in habitat availability due to their high trophic position and small population sizes compared with their hosts, but there are only few quantitative studies on their population changes.Here, we studied the distribution and abundance of 48 kleptoparasitic and parasitoid species of cuckoo wasps (Chrysididae) and eight selected host species recorded in Finland from 1840 to 2015 based on an extensive survey of entomological collections. Population trends were assessed by studying changes in occupancy in 10 × 10 km grid squares between two study periods, 1840–1967 and 1968–2015.Statistically significant decreases in occurrence were found for 11 cuckoo wasp species and one host species, while significant increases were not observed for any species. Trends of cuckoo wasps and their hosts were positively correlated, and changes were generally stronger in cuckoo wasps than in their hosts.In a comparative analysis of species traits, abundance, body size and nesting type of host were related to occurrence changes of cuckoo wasps. Scarce and small species that use above ground‐nesting hosts declined more than abundant and large species that use ground‐nesting hosts.Cuckoo wasp species dependent on dead wood are more vulnerable to changes in the environment than species associated with open sandy habitats. While both groups of species have probably suffered from habitat loss, the emergence of secondary habitats may have benefitted species living in sandy areas and compensated for the negative impact of habitat destruction.

Cuckoo wasps, also known as jewel or gold wasps (Hymenoptera: Chrysididae), are kleptoparasites and parasitoids that impose their offspring on the breeding efforts of other wasp species. Chrysidids oviposit in the nests of predatory wasps, and the hatched larva kills the host's larva and consumes the resources collected by the host. When a cuckoo wasp is detected by the host wasp, the host may abandon the nest or take other measures to prevent the development of the kleptoparasite. Chemical camouflage, particularly involving cuticlar hydrocarbons (CHCs), is crucial for cuckoo wasp females. There is a conflict because females need chemical signals that are easily detectable by males but not by the host wasps. It was demonstrated that virgin females of Chrysis angustula, Chrysis fulgida, and Chrysis iris contain CHCs that stimulate behavioral reactions in conspecific males. Coupled gas chromatography-electroantennogram detection analysis revealed 16 hydrocarbons with carbon chain lengths of C23-27 in virgin females: 6 in C. angustula, 8 in C. fulgida, and 13 in C. iris. A specific ratio of CHC compounds, including putative sex pheromones, was established for these three chrysidid species. Observations of re-mating refusals led to the hypothesis that virgin females of cuckoo wasps cease production of some unsaturated CHCs, functioning as sex pheromones, following mating. This change could reduce the risk of detection of CHCs traces left while entering the host's nest.

Insect brood parasites have evolved a variety of strategies to avoid being detected by their hosts. Few previous studies on cuckoo wasps (Hymenoptera: Chrysididae), which are natural enemies of solitary wasps and bees, have shown that chemical mimicry, i.e., the biosynthesis of cuticular hydrocarbons (CHC) that match the host profile, evolved in several species. However, mimicry was not detected in all investigated host-parasite pairs. The effect of host range as a second factor that may play a role in evolution of mimicry has been neglected, since all previous studies were carried out on host specialists and at nesting sites where only one host species occurred. Here we studied the cuckoo wasp Parnopes grandior, which attacks many digger wasp species of the genus Bembix (Hymenoptera: Crabronidae). Given its weak host specialization, P. grandior may either locally adapt by increasing mimicry precision to only one of the sympatric hosts or it may evolve chemical insignificance by reducing the CHC profile complexity and/or CHCs amounts. At a study site harbouring three host species, we found evidence for a weak but appreciable chemical deception strategy in P. grandior. Indeed, the CHC profile of P. grandior was more similar to all sympatric Bembix species than to a non-host wasp species belonging to the same tribe as Bembix. Furthermore, P. grandior CHC profile was equally distant to all the hosts’ CHC profiles, thus not pointing towards local adaptation of the CHC profile to one of the hosts’ profile. We conducted behavioural assays suggesting that such weak mimicry is sufficient to reduce host aggression, even in absence of an insignificance strategy, which was not detected. Hence, we finally concluded that host range may indeed play a role in shaping the level of chemical mimicry in cuckoo wasps.

Cleptoparasitic wasps and bees smuggle their eggs into the nest of a host organism. Here the larvae of the cleptoparasite feed upon the food provision intended for the offspring of the host. As cleptoparasitism incurs a loss of fitness for the host organism (offspring of the host fail to develop), hosts of cleptoparasites are expected to exploit cues that alert them to potential cleptoparasite infestation. Cuticular hydrocarbons (CHCs) could serve as such cues, as insects inevitably leave traces of them behind when entering a nest. By mimicking the host's CHC profile, cleptoparasites can conceal their presence and evade detection by their host. Previous studies have provided evidence of cleptoparasites mimicking their host's CHC profile. However, the impact of this strategy on the evolution of the host's CHC profile has remained unexplored. Here, we present results from our investigation of a host-cleptoparasite system consisting of a single mason wasp species that serves syntopically as the host to three cuckoo wasp species. We found that the spiny mason wasp (Odynerus spinipes) is able to express two substantially different CHC profiles, each of which is seemingly mimicked by a cleptoparasitic cuckoo wasp (i.e. Chrysis mediata and Pseudospinolia neglecta). The CHC profile of the third cuckoo wasp (Chrysis viridula), a species not expected to benefit from mimicking its host's CHC profile because of its particular oviposition strategy, differs from the two CHC profiles of its host. Our results corroborate the idea that the similarity of the CHC profiles between cleptoparasitic cuckoo wasps and their hosts are the result of chemical mimicry. They further suggest that cleptoparasites may represent a hitherto unappreciated force that drives the evolution of their hosts' CHCs.

Cuckoo wasps (Chrysididae) are a medium-sized and widespread family of Hymenoptera whose species are generally parasitoids or cleptoparasites of solitary wasps and bees. The identities of the hosts are known from various studies and occasional records; however the utility of such data is often low due to unstable taxonomy of the species and the inappropriate methods used to determine the host species. Therefore, despite numerous publications on the subject, the host-parasite relationships of cuckoo wasps are poorly understood. Moreover, a revision of existing literature reveals that cuckoo wasps are often unreasonably considered to be unspecialized (i.e., sharing host species). In this study we use an accurate method (trap-nests) to determine the host relationships of Estonian cuckoo wasps of the genera Chrysis and Trichrysis and determine their level of specialization. 568 trap nest bundles (each containing 15-20 single reed stems) were established at 361 locations across Estonia during the vegetation periods of 2009-2011. Nests built in traps were opened and the order of cells documented in order to determine the host-parasite relationships of mason wasps and cuckoo wasps. Altogether, 5386 insects were recorded, including 12 species of Chrysidini. Hosts of all 12 cuckoo wasp species were determined and included some not previously recorded. Analysis of host-parasite relationships revealed that Estonian species of Chrysidini exhibit a greater degree of host specialization than previously thought, with only a minimal overlap in hosts between species. Such a high degree of specialization accounts for the high species diversity of cuckoo wasps, as the diversity of parasitic insects is often associated with narrow host specialization.

Simple SummaryThe biology of many species of cuckoo wasps (Chrysididae) is largely unknown, except for, if at all, the host species of these brood parasites. Cuticular hydrocarbons (CHCs), which form a waxy layer on the body surface of insects, have been shown to be mimicked by host-specific cuckoo wasp species. We studied the CHC profiles of a rather generalist brood parasitic cuckoo wasp species, Trichrysis cyanea, in detail. We found sex-related differences in CHCs and three different chemotypes among females. Genetic data reject the possibility that these different chemotypes represent different (cryptic) species. The CHC polymorphism could be an adaptation for females to sneak into nesting holes of hosts with the different female chemotypes representing adaptations to a broader host range. However, since information on the CHC profiles of the hosts is missing, it remains unclear whether these different CHC profiles are used for chemical mimicry or are simply age-related, reflecting the females’ reproductive state. Cuckoo wasps (Chrysididae, Hymenoptera) are known for their parasitoid or cleptoparasitic life histories. Indeed, the biology of only a few species has been studied in detail and often only little more is known than the host species. By mimicking their hosts’ cuticular hydrocarbon (CHC) profiles, species that parasitize single (or a few closely related) host species manage to deceive their hosts. However, the variability of the CHC profile in generalist cuckoo-wasp species is still unknown. Here, we used gas chromatography—mass spectrometry (GC-MS) and DNA barcoding to study intraspecific variation in cuticular hydrocarbons of one less host-specific species of cuckoo wasps, Trichrysis cyanea. Cuticular hydrocarbon (CHC) patterns were found to differ between males and females. Additionally, we found chemical polymorphism among females, which formed three distinct chemical subgroups characterized by different alkene patterns. A lack of divergence in the DNA barcoding region suggests that these different chemotypes do not represent cryptic species. Whether this intrasexual CHC-profile variation is an adaptation (mimicry) to different host species, or simply signaling the reproductive status, remains unclear.

Cuckoo wasps (Hymenoptera: Chrysididae) are a species‐rich family of obligate brood parasites (i.e. parasitoids and kleptoparasites) whose hosts range from sawflies, wasps and bees, to walking sticks and moths. Their brood parasitic lifestyle has led to the evolution of fascinating adaptations, including chemical mimicry of host odours by some species. Long‐term nomenclatural stability of the higher taxonomic units (e.g. genera, tribes, and subfamilies) in this family and a thorough understanding of the family's evolutionary history critically depend on a robust phylogeny of cuckoo wasps. Here we present the results from phylogenetically analysing ten nuclear‐encoded genes and one mitochondrial gene, all protein‐coding, in a total of 186 different species of cuckoo wasps representing most major cuckoo wasp lineages. The compiled data matrix comprised 4946 coding nucleotide sites and was phylogenetically analysed using classical maximum‐likelihood and Bayesian inference methods. The results of our phylogenetic analyses are mostly consistent with earlier ideas on the phylogenetic relationships of the cuckoo wasps' subfamilies and tribes, but cast doubts on the hitherto hypothesized phylogenetic position of the subfamily Amiseginae. However, the molecular data are not fully conclusive in this respect due to low branch support values at deep nodes. In contrast, our phylogenetic estimates clearly indicate that the current systematics of cuckoo wasps at the genus level is artificial. Several of the currently recognized genera are para‐ or polyphyletic (e.g. Cephaloparnops , Chrysis , Chrysura , Euchroeus , Hedychridium , Praestochrysis , Pseudochrysis , Spintharina , and Spinolia ). At the same time, our data support the validity of the genus Colpopyga , previously synonymized with Hedychridium . We discuss possible solutions for how to resolve the current shortcomings in the systematics of cuckoo wasp genera and decided to grant Prospinolia the status of a valid genus ( Prospinolia stat.n. ) and transferring Spinolia theresae [du Buysson 1900] from Spinolia to Prospinolia ( Prospinolia theresae stat.restit. ). We discuss the implications of our phylogenetic inferences for understanding the evolution of host associations in this group. The results of our study not only shed new light on the evolutionary history of cuckoo wasps, but also set the basis for future phylogenomic investigations on this captivating group of wasps by guiding taxonomic sampling efforts and the design of probes for target DNA enrichment approaches.

DNA barcoding technologies have provided a powerful tool for the fields of ecology and systematics. Here, we present a part of the InBIO Barcoding Initiative Database: contribution to the knowledge on DNA barcodes of cuckoo wasps (Hymenoptera, Chrysididae) dataset representing 144 specimens and 103 species, covering approximately 44% of the Iberian and 21% of the European fauna. The InBIO Barcoding Initiative (IBI - DNA Barcoding Portuguese terrestrial invertebrate biodiversity) aims to fill the barcoding gap for the terrestrial invertebrate taxa. All DNA extractions are deposited in the IBI collection at CIBIO, Research Center in Biodiversity and Genetic Resources and specimens are deposited in the University of Mons collection (Belgium) and in the Natur-Museum in Lucerne (Switzerland). This dataset increases the knowledge on the DNA barcodes and distribution of 102 species of cuckoo wasps. A total of 52 species, from 11 different genera, were new additions to the Barcode of Life Data System (BOLD), with DNA barcodes for another 44 species added from under-represented taxa in BOLD. All specimens have their DNA barcodes publicly accessible through the BOLD online database. Nine cuckoo wasp species are newly recorded for Portugal. Additionally, two new species for science are described: Chrysiscrossi Rosa, sp. nov. from southern Portugal and Hedychridiumcalcarium Rosa, sp. nov. from eastern Spain. Several taxonomic changes are proposed and Hedychrumrutilans Dahlbom, 1845 is found to consist of two different taxa that can be found in sympatry, Hedychrumrutilans s. str. and Hedychrumviridaureum Tournier, 1877 stat. nov. Stilbumwestermanni Dahlbom, 1845 stat. nov. is confirmed as distinct from Stilbumcalens (Fabricius, 1781), with the latter species not confirmed as present in Iberia; barcoded Stilbum material from Australia is distinct and represents Stilbumamethystium (Fabricius, 1775) sp. resurr.; Portuguese material identified as Hedychridiumchloropygum Buysson, 1888 actually belongs to Hedychridiumcaputaureum Trautmann & Trautmann, 1919, the first confirmed record of this species from Iberia. Philoctetesparvulus (Dahlbom, 1845) is confirmed to be a synonym of Philoctetespunctulatus (Dahlbom, 1845). Chrysislusitanica Bischoff, 1910 is confirmed as a valid species. Chrysishebraeica Linsenmaier, 1959 stat. nov. is raised to species status.

Hemipterochilus bembeciformis and Tropidodynerus interruptus nest in ground with rather similar soil characteristics (light to medium clay loam). Two nests of the former species and four of the latter were excavated. Both species used water to moisten the ground. Females of H. bembeciformis surmounted the nest entrance with a 1–4 mm high mud collar; the nest entrance of T. interruptus was simple but temporary closed with mud pellets by the wasps. One nest of H. bembeciformis was abandoned, while another contained two brood cells as ends of a branched burrow; all nests of T. interruptus were one-celled. A caterpillar of Acontia trabealis (Lepidoptera: Noctuidae) was recorded as a prey of H. bembeciformis, while females of T. interruptus hunted on larvae of Rhinocyllus conicus (Coleoptera: Curculionidae) extracting them from fading capitula of Carduus nutans subsp. leiophyllus. Cuckoo wasps Chrysis cylindrica and Ch. valesiana were observed at nests of both species, while only cocoons of the former species were recorded in the brood cells of both H. bembeciformis and T. interruptus. Chrysis cylindrica is recorded as a parasitoid, since its larva consumes the host larva and its cocoons were found inside cocoons of the host-wasp species. The cocoon of T. interruptus is described. Hemipterochilus bembeciformis and T. interruptus form a Müllerian mimicry ring with at least two other eumenine-wasp species co-occurring in the Tarkhankut Nature Park: Paragymnomerus signaticollis and Pseudepipona herrichii. The biology of all four species is discussed; all of them are confined to threatened steppe habitats and require our attention and conservation efforts.

In a study on the host association of the cuckoo wasp, Chrysis fulgida L., at two nesting sites in Northern Italy, it was observed emerging from nests of the mason wasp, Symmorphus crassicornis (Panzer). Although other species of eumenine wasps nested in the same area, none of them was attacked by this parasitoid. Parasitism rate per nest ranged from 0% to 66.3%, 45.8% on average. The number of parasitized cells did not decrease either with the thickness of the nest closing plug or with the length of vestibular cell. No differences in the number of cells per nest or in the length of vestibular cell were found when comparing parasitized and unparasitized nests, suggesting that the wasps probably did not abandon their parasitized nest and that the cuckoo wasp larva was not detected. A review of the host associations of the species of Chrysis of the ignita group suggests that mason wasps are the preferred hosts and that cavity-nesters are more frequently attacked than soil- or mud-nesters. The prepupa of C. fulgida is described, illustrated, and compared with the described mature larvae of Chrysididae. The postdefecating larva of this species exhibits the autapomorphy that defines the genus Chrysis: “normally developed galeae.” The most salient character shown by the mature larva of this species lies in the maxillary palpus, which has 6 sensilla at apex. This character state allows this prepupa to be differentiated from the previously described mature larvae of the genus.

Chrysididae is a diverse group of parasitoid/cleptoparasitic wasps; however, host–parasite relationships and life cycles of few species have been studied. Nests of different wasp and bee species were obtained during a trap-nesting programme, in the Pampean region. Some of these nests were parasitised by cuckoo wasps females of Caenochrysis taschenbergi (Mocsáry), Chrysis boutheryi (Brèthes), C. saltana Bohart, C. sp. 1 (ignita-group), C. sp. 2 (ignita-group), Neochrysis lecointei (Ducke), Pleurochrysis ancilla (Buysson) and P. lynchi (Bréthes). This paper reports new data about host–parasite relationships and life cycles for these species. Multiple parasites (from one species or from different families of insects) emerged from single cells of some parasitised nests: from each host cell parasitised by species of Pleurochrysis, two adults emerged successfully, information previously unknown for the genus; and in three cases of cells parasitised by C. boutheryi, two adults successfully emerged from a single cell; in two cases both individuals were chrysidine, and in third one was chrysidine and one Leucospis pulchripes (Leucospidae).

Comparison of the sternal spots and carinae of twelve species of North American cuckoo wasps (Hymenoptera: Chrysididae) using scanning electron microscopy

Solitary nest-provisioning wasps and bees in North America include species that naturally construct nests within existing cavities, such as hollow plant stems or tunnels left by wood-boring insects. The materials used to construct brood cells within nest cavities and the types of food provisions provided to offspring vary considerably among species. Over five summers (2001-2002, 2005-2007), we used trap nests to survey the cavity-nesting wasp and bee assemblage within the Montezuma Wetlands Complex in central New York State. Over 350 trap nests were occupied by 6 species of apoid wasps (Sphecidae, Crabronidae; 34% of nests), 7 vespid wasps (Vespidae: Eumeninae; 39%), 2 spider wasps (Pompilidae; 3%), and 12 bees (Megachilidae, Colletidae; 26%), as well as brood parasites and parasitoids of the nest provisioners. The most common nest-provisioning wasp was Trypoxylon lactitarse, followed by Ancistrocerus antilope, Isodontia mexicana, Symmorphus canadensis, Symmorphus cristatus, and Euodynerus foraminatus. The only two bee species with comparable incidences were Hylaeus annulatus and Heriades cari- natus. Natural enemies emerging from nests included at least 17 species from 10 families, the most common of which were brood-parasitic cuckoo wasps (7 species of Chrysididae; 39 nests) and flies (Sarcophagidae; 11 nests). We also report brood sex ratios of the seven most abundant species, finding them to be either male-biased (A. antilope, T. lactitarse), female-biased (E. foraminatus), or not significantly dif- ferent from unity. We compare our survey results to others done in north-central and eastern North America.

The work provides data on the dynamics of the abundance of 205 taxa from 19 genera: Cleptes, Colpopyga, Elampus, Omalus, Philoctetes, Pseudomalus, Hedychridium, Hedychrum, Holopyga, Chrysidea, Chrysis, Euchroeus, Chrysura, Pseudochrysis, Spinolia, Spinolia, including species rare and new for the fauna of the North Caucasus and Russia. By the nature of the population dynamics, five groups of cuckoo wasps were identified: spring – represented by 7 species from 4 genera; spring-summer – 76 species from 10 genera; summer – 113 species from 16 genera; summer-autumn – 4 species from 2 genera and spring-summer-autumn – 5 species from 3 genus. According to the duration of flight, eurychronous species of cuckoo wasps were identified, which are found throughout the season from spring to autumn; mesochronous – the years of which affect the end of May and summer months and stenochronous – confined to a short period of time. Eurychronic accounted for 2.4%, mesochronous 24.9%, stenochronic 72.7%. The number of generations of cuckoo wasps is related to the dynamics of the number of the host. In the mountains, the peaks of activity shift towards the middle of summer, most species have one peak of activity; due to the frequent changes in weather conditions in the mountains, the phenological characteristics of the cuckoo wasps and their hosts do not coincide in terms with the lowland populations and the periods of activity can be extended in time. Phenological characteristics of rare and new species for the fauna of the North Caucasus and Russia are presented for the first time. The data obtained expand the understanding of the biodiversity and dynamics of the abundance of cuckoo wasps in the North Caucasus and can be used for environmental protection measures and rational nature management in the south of Russia.