Parasitoid Wasp Community Dynamics in Vineyards Following Insecticide Application

In order to integrate parasitoid wasps in agroecosystems as biological control agents, we need to understand how insecticides affect the parasitoids in the crops and their surroundings. We investigated the non-target effect of Indoxacarb, an insecticide commonly used against European grapevine moth, on parasitoid wasp communities in vineyards. We focused on characterizing: 1. The dynamics of common wasp species, and 2. Wasp abundance and species richness in the vineyard center, edge, and nearby natural area. Seven vineyards, with neighboring natural areas, were sampled before, and up to 2 weeks after, Indoxacarb applications over 2 years. We expected initial negative effects of spraying in the vineyard with some effect of Indoxacarb drift into the natural habitat, followed by wasp recovery, first in natural areas, then at the vineyard edge and finally in the center. Sticky traps were hung at the vineyard edge and center to evaluate migration into and out of the vineyard. Vacuum sampling was used to obtain parasitoid total abundance and species richness, and the abundances of four common species (43% of the wasps collected). From the vacuum samples we found that total wasp abundance and richness declined after spraying in the vineyards’ margins and center but rose over time in the natural area. Vineyard wasp abundance was restored to pre-spraying levels within 2 weeks. Among the abundant species, Trichogramma sp. and Telenomus sp., which parasitize lepidopteran hosts, declined after spraying, and Trichogramma sp. recovered more quickly than Telenomus sp. Two other abundant species, Lymaenon litoralis and Oligosita sp., did not decline after spraying. In the sticky traps, wasp abundance increased at the vineyard edge but not center after spraying, suggesting that there was migration of wasps at the vineyard edge, into or out of the crop. The results indicate an effect of Indoxacarb on the parasitoid wasp community, particularly on parasitoids of lepidopterans, the target group of Indoxacarb. The results also indicate a potential for recovery of the parasitoid community through migration from neighboring natural vegetation.

Genome of the parasitoid wasp Dinocampus coccinellae reveals extensive duplications, accelerated evolution, and independent origins of thelytokous parthenogeny and solitary behavior

Dinocampus coccinellae (Hymenoptera: Braconidae) is a generalist parasitoid wasp that parasitizes >50 species of predatory lady beetles (Coleoptera: Coccinellidae), with thelytokous parthenogeny as its primary mode of reproduction. Here we present the first high quality genome of D. coccinellae using a combination of short and long read sequencing technologies, followed by assembly and scaffolding of chromosomal segments using Chicago+HiC technologies. We also present a first-pass ab initio and a reference-based genome annotation, and resolve timings of divergence and evolution of (1) solitary behavior vs eusociality, (2) arrhenotokous vs thelytokous parthenogenesis, and (3) rates of gene loss and gain among Hymenopteran lineages. Our study finds (1) at least two independent origins of eusociality and solitary behavior among Hymenoptera, (2) two independent origins of thelytokous parthenogenesis from ancestral arrhenotoky, and (3) accelerated rates of gene duplications, loss, and gain along the lineages leading to D. coccinellae. Our work both affirms the ancient divergence of Braconid wasps from ancestral Hymenopterans and accelerated rates of evolution in response to adaptations to novel hosts, including polyDNA viral co-evolution.

The complete genome of Chelonus insularis reveals dynamic arrangement of genome components in parasitoid wasps that produce bracoviruses

Bracoviruses (BVs) are endogenized nudiviruses in parasitoid wasps of the microgastroid complex (family Braconidae). Microgastroid wasps have coopted nudivirus genes to produce replication-defective virions that females use to transfer virulence genes to parasitized hosts. The microgastroid complex further consists of six subfamilies and ∼50,000 species but current understanding of BV gene inventories and organization primarily derives from analysis of two wasp species in the subfamily Microgastrinae ( Microplitis demolitor and Cotesia congregata ) that produce M. demolitor BV (MdBV) and C. congregata BV (CcBV). Notably, several genomic features of MdBV and CcBV remain conserved since divergence of M. demolitor and C. congregata ∼53 million years ago (MYA). However, it is unknown whether these conserved traits more broadly reflect BV evolution, because no complete genomes exist for any microgastroid wasps outside of the Microgastrinae. In this regard, the subfamily Cheloninae is of greatest interest because it diverged earliest from the Microgastrinae (∼85 MYA) after endogenization of the nudivirus ancestor. Here, we present the complete genome of Chelonus insularis , which is an egg-larval parasitoid in the Cheloninae that produces C. insularis BV (CinsBV). We report that the inventory of nudivirus genes in C. insularis is conserved but are dissimilarly organized when compared to M. demolitor and C. congregata . Reciprocally, CinsBV proviral segments share organizational features with MdBV and CcBV but virulence gene inventories exhibit almost no overlap. Altogether, our results point to the functional importance of a conserved inventory of nudivirus genes and a dynamic set of virulence genes for the successful parasitism of hosts. Our results also suggest organizational features previously identified in MdBV and CcBV are likely not essential for BV virion formation. Significance Bracoviruses are a remarkable example of virus endogenization, because large sets of genes from a nudivirus ancestor continue to produce virions that thousands of wasp species rely upon to parasitize hosts. Understanding how these genes interact and have been coopted by wasps for novel functions is of broad interest in the study of virus evolution. This manuscript characterizes bracovirus genome components in the parasitoid wasp Chelonus insularis , which together with existing wasp genomes captures a large portion of the diversity among wasp species that produce bracoviruses. Results provide new information about how bracovirus genome components are organized in different wasps while also providing additional insights on key features required for function.

First record in Africa of the parasitoid Dolichogenidea gelechiidivoris (Hymenoptera: Braconidae) on tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae) from tomato fields in Algeria

The Neotropical parasitoid wasp Dolichogenidea gelechiidivoris (Marsh, 1975) (Hymenoptera: Braconidae), one of the most important biocontrol agents of the South American tomato pinworm Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae), is reported for the first time from Africa, from tomato grown in open fields and greenhouses in several regions of Algeria. Color photos of specimens from Algeria, Spain and South America, as well as the holotype and one paratype are provided. Morphological and molecular details to better characterize and recognize the species are also provided. We speculate that D. gelechiidivoris arrived accidentally to Algeria from Spain, where it has recently been reported. The consequences for future biocontrol projects against T. absoluta in Africa are discussed.

Psix striaticeps (Dodd) (Hymenoptera, Scelionidae): an Old World parasitoid of stink bug eggs arrives in Florida, USA

Psix striaticeps (Dodd) is an egg-parasitoid wasp previously known only from the Old World. We report this species from twelve counties in Florida, which are the first records in the Western Hemisphere. It was collected in yellow cylinder traps and reared from the eggs of three stink bug species: Nezara viridula L., Chinavia marginata (Palisot de Beauvois), and Piezodorus guildinii (Westwood). A COI barcode analysis found a 100% match between the Floridian population and a specimen from South Africa. The prospects of using Ps. striaticeps as a biological control agent against exotic stink bugs are discussed.

 Gryon aetherium Talamas (Hymenoptera, Scelionidae): Parasitoid of Bagrada hilaris (Burmeister) (Hemiptera, Pentatomidae) Adventive in Chile

A parasitoid wasp, Gryon aetherium Talamas (Hymenoptera, Scelionidae), was reared from eggs of the invasive stink bug Bagrada hilaris (Burmeister) (Hemiptera, Pentatomidae) in Chile. The identification of G. aetherium, which is under study as a biological control agent, was made with morphological and molecular data in the context of a recent taxonomic treatment of this species. The presence of an adventive population of G. aetherium in South America has implications for biological control of B. hilaris in Chile, and other countries on the continent, where this stink bug may become a pest.

Prototeleia Talamas, Popovici, Shih & Ren: A new genus of Platygastridae from Burmese amber

A new genus and species of parasitoid wasp is described from Burmese amber: Prototeleia kleiogen. nov., sp. nov. (Platygastroidea, Platygastridae). Prototeleia kleio exhibits multiple characters that we consider to be plesiomorphic for Platygastridae. These characters are analyzed and discussed in the context of extant and fossil taxa.

Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process?

Hymenopterans are haplodiploids and unlike most other Arthropods they do not possess sexual chromosomes. Sex determination typically happens via the ploidy of individuals: haploids become males and diploids become females. Arrhenotoky is believed to be the ancestral reproduction mode in Hymenopterans, with haploid males produced parthenogenetically, and diploid females produced sexually. However, a number of transitions towards thelytoky (diploid females produced parthenogenetically) have appeared in Hymenopterans, and in most cases populations or species are either totally arrhenotokous or totally thelytokous. Here we present the case of Cotesia typhae (Fernandez-Triana), a Braconidae that produces parthenogenetic females at a low frequency. The phenotyping of two laboratory strains and one natural population showed that this frequency is variable, and that this rare thelytokous phenomenon also happens in the wild. Moreover, mated females from one of the laboratory strains produce a few parthenogenetic daughters among a majority of sexual daughters. The analysis of daughters of heterozygous virgin females allowed us to show that a mechanism of automixis with central fusion is very likely at play in C. typhae. This mechanism allows some parts of the genome to remain heterozygous, especially at the chromosomes' centromeres, which can be advantageous depending on the sex determination system involved. Lastly, in most species, the origin of thelytoky is either bacterial or genetic, and an antibiotic treatment as well as PCR experiments did not demonstrate a bacterial cause in C. typhae. The unusual case of low parthenogenetic frequency described in this species constitutes another example of the fascinating diversity of sex determination systems in Arthropods.

Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids

Multinucleated giant hemocytes (MGHs) represent a novel type of blood cell in insects that participate in a highly efficient immune response against parasitoid wasps involving isolation and killing of the parasite. Previously, we showed that circulating MGHs have high motility and the interaction with the parasitoid rapidly triggers encapsulation. However, structural and molecular mechanisms behind these processes remained elusive. Here, we used detailed ultrastructural analysis and live cell imaging of MGHs to study encapsulation in <i>Drosophila ananassae</i> after parasitoid wasp infection. We found dynamic structural changes, mainly driven by the formation of diverse vesicular systems and newly developed complex intracytoplasmic membrane structures, and abundant generation of giant cell exosomes in MGHs. In addition, we used RNA sequencing to study the transcriptomic profile of MGHs and activated plasmatocytes 72 h after infection, as well as the uninduced blood cells. This revealed that differentiation of MGHs was accompanied by broad changes in gene expression. Consistent with the observed structural changes, transcripts related to vesicular function, cytoskeletal organization, and adhesion were enriched in MGHs. In addition, several orphan genes encoding for hemolysin-like proteins, pore-forming toxins of prokaryotic origin, were expressed at high level, which may be important for parasitoid elimination. Our results reveal coordinated molecular and structural changes in the course of MGH differentiation and parasitoid encapsulation, providing a mechanistic model for a powerful innate immune response.

The emergence of ecotypes in a parasitoid wasp: a case of incipient sympatric speciation in Hymenoptera?

Background To understand which reproductive barriers initiate speciation is a major question in evolutionary research. Despite their high species numbers and specific biology, there are only few studies on speciation in Hymenoptera. This study aims to identify very early reproductive barriers in a local, sympatric population of Nasonia vitripennis (Walker 1836), a hymenopterous parasitoid of fly pupae. We studied ecological barriers, sexual barriers, and the reduction in F1-female offspring as a postmating barrier, as well as the population structure using microsatellites. Results We found considerable inbreeding within female strains and a population structure with either three or five subpopulation clusters defined by microsatellites. In addition, there are two ecotypes, one parasitizing fly pupae in bird nests and the other on carrion. The nest ecotype is mainly formed from one of the microsatellite clusters, the two or four remaining microsatellite clusters form the carrion ecotype. There was slight sexual isolation and a reduction in F1-female offspring between inbreeding strains from the same microsatellite clusters and the same ecotypes. Strains from different microsatellite clusters are separated by a reduction in F1-female offspring. Ecotypes are separated only by ecological barriers. Conclusions This is the first demonstration of very early reproductive barriers within a sympatric population of Hymenoptera. It demonstrates that sexual and premating barriers can precede ecological separation. This indicates the complexity of ecotype formation and highlights the general need for more studies within homogenous populations for the identification of the earliest barriers in the speciation process.