Functional and evolutionary insights from the genomes of three parasitoid Nasonia species

Abstract

We report here genome sequences and comparative analyses of three closely related parasitoid wasps: Nasonia vitripennis, N. giraulti, and N. longicornis. Parasitoids are important regulators of arthropod populations, including major agricultural pests and disease vectors, and Nasonia is an emerging genetic model, particularly for evolutionary and developmental genetics. Key findings include the identification of a functional DNA methylation tool kit; hymenopteran-specific genes including diverse venoms; lateral gene transfers among Pox viruses, Wolbachia, and Nasonia; and the rapid evolution of genes involved in nuclear-mitochondrial interactions that are implicated in speciation. Newly developed genome resources advance Nasonia for genetic research, accelerate mapping and cloning of quantitative trait loci, and will ultimately provide tools and knowledge for further increasing the utility of parasitoids as pest insect-control agents.

Fig. 1

Phylogenetic relationships of Nasonia and the DNA methylation tool kit. (A) Nasonia relationships to other sequenced genomes (6). Right: DNA methyltransferase subfamilies (Dnmt1, Dnmt2, Dnmt3) in these taxa. (B) Relationships among the three sequenced Nasonia genomes. (C) Crossing scheme used for mapping scaffolds on the Nasonia chromosomes and for studies of nuclear-cytoplasmic incompatibility.

Fig. 2

A high-resolution recombination map of the five Nasonia chromosomes is shown (6), with estimated gene density and locations of visible markers, landmark genes, and QTL. The hybridization percentage to N. vitripennis alleles is shown among surviving adult N. vitripennis × N. giraulti F2 hybrid males with either N. vitripennis (green curve) or N. giraulti (orange curve) mitochondria. Dots specify genome regions with significant differences in the hybridization ratio between the reciprocal crosses (P < 0.01).

Fig. 3

Distribution of recognizable Nasonia orthologs and Nasonia-specific genes among gene models with expression sequencing support (6).

Fig. 4

PRANC domain proteins in Nasonia, Pox viruses, and Wolbachia. (A) Maximum-likelihood tree of PRANC-domain sequences found in Pox viruses, rickettsia (Wolbachia and Orientia), and parasitoids (N. vitripennis and Cotesia congregata). The tree was estimated using RaxML with 1000 bootstrap replicates and model settings estimated by ProtTest [see (6); alignment deposited in Tree-base with ID SN4709]. Bootstrap values above 50% are shown by the corresponding nodes. The phylogenetic relationships suggest lateral transfer from Wolbachia to the Nasonia lineage. (B) Representative domain arrangements for ANK-PRANC proteins.