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.

Morphology of immatures of the thelytokous ant, Monomorium triviale Wheeler (Formicidae: Myrmicinae: Solenopsidini) with descriptions of the larval caste dimorphism

The ant genus Monomorium is one of the most species-rich but taxonomically problematic groups in the hyperdiverse subfamily Myrmicinae. An East Asian species, M. triviale Wheeler, W. M., produces both reproductive queens and sterile workers via obligate thelytokous parthenogenesis. Here, we describe the immature forms of M. triviale based on light and scanning electron microscopy observations, with a note on the striking caste dimorphism in the last larval instar. The last-instar queen larvae were easily recognized by their large size, "aphaenogastoroid" body shape, and rows of doorknob-like tubercles on the lateral and dorsal body surface. This type of queen-specific structure has not been found in ants in general, let alone congeneric species found in Japan. In stark contrast to the queen larvae, worker larvae showed a "pheidoroid" body shape and a body surface similar to other ants. The worker larvae were estimated to have three instars, consistent with previously described congeners. The pupae of both castes also had no cocoon, a characteristic commonly described in other Myrmicinae species. In total, the developmental period from egg to adult worker averaged 59 days under 25℃. We discuss possible functions of the tubercles of queen larvae based on previous studies.

Effects of Thelytokous Parthenogenesis-Inducing Wolbachia on the Fitness of Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) in Superparasitised and Single-Parasitised Hosts

Thelytokous Wolbachia-infected Trichogramma species have long been considered as biological control agents against lepidopteran pests in agriculture and forestry. Wolbachia has been suggested to increase the probability of the superparasitism of Trichogramma, but the fate of infected offspring in the superparasitised host is still unknown. The present study aimed to evaluate the fitness of thelytokous Wolbachia-infected (TDW) and bisexual Wolbachia-free (TD) Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) lines in superparasitised or single-parasitised hosts. The results showed that irrespective of whether Trichogramma wasps were developed from superparasitised or single-parasitised hosts, the TDW line was characterized by reduced fitness, including lower fecundity, shorter longevity, and smaller body size of F1 offspring, and lower emergence rate of F2 offspring than the TD line. This was not true for the survival rate and developmental time of F1 offspring. Additionally, the fitness parameters of T. dendrolimi that developed from superparasitised hosts were lower compared with that of T. dendrolimi that developed from single-parasitised hosts. Interestingly, Wolbachia-infected females had higher dispersal capacity than bisexual females when they developed from superparasitised hosts. The results indicated that Wolbachia negatively affects fitness of T. dendrolimi, but enhance dispersal capacity of T. dendrolimi females in superparasitism condition. Further studies need to be carried out to select the best line that will allow Wolbachia and their host Trichogramma to be better adapted to one another.

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 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.

Adaptive, caste-specific changes to recombination rates in a thelytokous honeybee population

The ability to clone oneself has clear benefits—no need for mate hunting or dilution of one's genome in offspring. It is therefore unsurprising that some populations of haplo-diploid social insects have evolved thelytokous parthenogenesis—the virgin birth of a female. But thelytokous parthenogenesis has a downside: the loss of heterozygosity (LoH) as a consequence of genetic recombination. LoH in haplo-diploid insects can be highly deleterious because female sex determination often relies on heterozygosity at sex-determining loci. The two female castes of the Cape honeybee, Apis mellifera capensis , differ in their mode of reproduction. While workers always reproduce thelytokously, queens always mate and reproduce sexually. For workers, it is important to reduce the frequency of recombination so as to not produce offspring that are homozygous. Here, we ask whether recombination rates differ between Cape workers and Cape queens that we experimentally manipulated to reproduce thelytokously. We tested our hypothesis that Cape workers have evolved mechanisms that restrain genetic recombination, whereas queens have no need for such mechanisms because they reproduce sexually. Using a combination of microsatellite genotyping and whole-genome sequencing we find that a reduction in recombination is confined to workers only.

Comprehensive analysis of male-free reproduction in Monomorium triviale (Formicidae: Myrmicinae)

We report comprehensive evidence for obligatory thelytokous parthenogenesis in an ant Monomorium triviale. This species is characterized by distinct queen–worker dimorphism with strict reproductive division of labor: queens produce both workers and new queens without mating, whereas workers are completely sterile. We collected 333 nests of this species from 14 localities and three laboratory-reared populations in Japan. All wild queens dissected had no sperm in their spermathecae. Laboratory observation confirmed that virgin queens produced workers without mating. Furthermore, microsatellite genotyping showed identical heterozygous genotypes between mothers and their respective daughters, suggesting an extremely low probability of sexual reproduction. Microbial analysis detected no bacterial genera that are known to induce thelytokous parthenogenesis in Hymenoptera. Finally, the lack of variation in partial sequences of mitochondrial DNA among individuals sampled from across Japan suggests recent rapid spread or selective sweep. M. triviale would be a promising model system of superorganism-like adaptation through comparative analysis with well-studied sexual congeners, including the pharaoh ant M. pharaonis.

Comprehensive analysis of male-free reproduction in Monomorium triviale (Formicidae: Myrmicinae)

We report comprehensive evidence for obligatory thelytokous parthenogenesis in an ant Monomorium triviale. This species is characterized by distinct queen–worker dimorphism with strict reproductive division of labor: queens produce both workers and new queens without mating, whereas workers are completely sterile. We collected 333 nests of this species from 14 localities and three laboratory-reared populations in Japan. All wild queens dissected had no sperm in their spermathecae. Laboratory observation confirmed that virgin queens produced workers without mating. Furthermore, microsatellite genotyping showed identical heterozygous genotypes between mothers and their respective daughters, suggesting an extremely low probability of sexual reproduction. Microbial analysis detected no bacterial genera that are known to induce thelytokous parthenogenesis in Hymenoptera. Finally, the lack of variation in partial sequences of mitochondrial DNA among individuals sampled from across Japan suggests recent rapid spread or selective sweep. M. triviale would be a promising model system of superorganism-like adaptation through comparative analysis with well-studied sexual congeners, including the pharaoh ant M. pharaonis.