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Comparative Genomics Sheds Light on the Convergent Evolution of Miniaturized Wasps.

ABSTRACT: Miniaturization has occurred in many animal lineages, including insects and vertebrates, as a widespread trend during animal evolution. Among Hymenoptera, miniaturization has taken place in some parasitoid wasp lineages independently, and may have contributed to the diversity of species. However, the genomic basis of miniaturization is little understood. Diverged approximately 200 Ma, Telenomus wasps (Platygastroidea) and Trichogramma wasps (Chalcidoidea) have both evolved to a highly reduced body size independently, representing a paradigmatic example of convergent evolution. Here, we report a high-quality chromosomal genome of Telenomus remus, a promising candidate for controlling Spodoptera frugiperda, a notorious pest that has recently caused severe crop damage. The T. remus genome (129 Mb) is characterized by a low density of repetitive sequence and a reduction of intron length, resulting in the shrinkage of genome size. We show that hundreds of genes evolved faster in two miniaturized parasitoids Trichogramma pretiosum and T. remus. Among them, 38 genes exhibit extremely accelerated evolutionary rates in these miniaturized wasps, possessing diverse functions in eye and wing development as well as cell size control. These genes also highlight potential roles in body size regulation. In sum, our analyses uncover a set of genes with accelerated evolutionary rates in Tri. pretiosum and T. remus, which might be responsible for their convergent adaptations to miniaturization, and thus expand our understanding on the evolutionary basis of miniaturization. Additionally, the genome of T. remus represents the first genome resource of superfamily Platygastroidea, and will facilitate future studies of Hymenoptera evolution and pest control.

SUBMITTER: Xu H

PROVIDER: S-EPMC8662594 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:For insects known as parasitoid wasps, successful development as a parasite results in the death of the host insect. As a result of this lethal interaction, wasps and their hosts have coevolved strategies to gain an advantage in this evolutionary arms race. Although normally considered to be strict pathogens, some viruses have established persistent infections within parasitoid wasp lineages and are beneficial to wasps during parasitism. Heritable associations between viruses and parasitoid wasps have evolved independently multiple times, but most of these systems remain largely understudied with respect to viral origin, transmission and replication strategies of the virus, and interactions between the virus and host insects. Here, we report a detailed characterization of Diachasmimorpha longicaudata entomopoxvirus (DlEPV), a poxvirus found within the venom gland of Diachasmimorpha longicaudata wasps. Our results show that DlEPV exhibits similar but distinct transmission and replication dynamics compared to those of other parasitoid viral elements, including vertical transmission of the virus within wasps, as well as virus replication in both female wasps and fruit fly hosts. Functional assays demonstrate that DlEPV is highly virulent within fly hosts, and wasps without DlEPV have severely reduced parasitism success compared to those with a typical viral load. Taken together, the data presented in this study illustrate a novel case of beneficial virus evolution, in which a virus of unique origin has undergone convergent evolution with other viral elements associated with parasitoid wasps to provide an analogous function throughout parasitism.IMPORTANCE Viruses are generally considered to be disease-causing agents, but several instances of beneficial viral elements have been identified in insects called parasitoid wasps. These virus-derived entities are passed on through wasp generations and enhance the success of the wasps' parasitic life cycle. Many parasitoid-virus partnerships studied to date exhibit common features among independent cases of this phenomenon, including a mother-to-offspring route of virus transmission, a restricted time and location for virus replication, and a positive effect of virus activity on wasp survival. Our characterization of Diachasmimorpha longicaudata entomopoxvirus (DlEPV), a poxvirus found in Diachasmimorpha longicaudata parasitoid wasps, represents a novel example of beneficial virus evolution. Here, we show that DlEPV exhibits functional similarities to known parasitoid viral elements that support its comparable role during parasitism. Our results also demonstrate unique differences that suggest DlEPV is more autonomous than other long-term viral associations described in parasitoid wasps.

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Comparative Genomics Sheds Light on the Convergent Evolution of Miniaturized Wasps.

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