Recombination and Its Impact on the Genome of the Haplodiploid Parasitoid Wasp Nasonia

Abstract

Homologous meiotic recombination occurs in most sexually reproducing organisms, yet its evolutionary advantages are elusive. Previous research explored recombination in the honeybee, a eusocial hymenopteran with an exceptionally high genome-wide recombination rate. A comparable study in a non-social member of the Hymenoptera that would disentangle the impact of sociality from Hymenoptera-specific features such as haplodiploidy on the evolution of the high genome-wide recombination rate in social Hymenoptera is missing. Utilizing single-nucleotide polymorphisms (SNPs) between two Nasonia parasitoid wasp genomes, we developed a SNP genotyping microarray to infer a high-density linkage map for Nasonia. The map comprises 1,255 markers with an average distance of 0.3 cM. The mapped markers enabled us to arrange 265 scaffolds of the Nasonia genome assembly 1.0 on the linkage map, representing 63.6% of the assembled N. vitripennis genome. We estimated a genome-wide recombination rate of 1.4–1.5 cM/Mb for Nasonia, which is less than one tenth of the rate reported for the honeybee. The local recombination rate in Nasonia is positively correlated with the distance to the center of the linkage groups, GC content, and the proportion of simple repeats. In contrast to the honeybee genome, gene density in the parasitoid wasp genome is positively associated with the recombination rate; regions of low recombination are characterized by fewer genes with larger introns and by a greater distance between genes. Finally, we found that genes in regions of the genome with a low recombination frequency tend to have a higher ratio of non-synonymous to synonymous substitutions, likely due to the accumulation of slightly deleterious non-synonymous substitutions. These findings are consistent with the hypothesis that recombination reduces interference between linked sites and thereby facilitates adaptive evolution and the purging of deleterious mutations. Our results imply that the genomes of haplodiploid and of diploid higher eukaryotes do not differ systematically in their recombination rates and associated parameters.

A comparison of recombination frequencies in intraspecific versus interspecific mapping populations of Nasonia

“…However, it was still possible to use them to estimate pairwise recombination frequencies (see Table 1). In some instances, the two maps differed in marker order, in which case the STS map of Niehuis et al (2010) was used as template.…”

“…Of the 38 microsatellite loci on the intraspecific map that we matched to the molecular markers on the interspecific map , one was identical (Nv319) and the remaining 37 showed an average distance of 0.2% recombination (range 0-2.7% recombination, see Supplementary Table 2) based on the high-density linkage map published by Niehuis et al (2010).…”

“…An additional advantage of having the physical genome sequence of a study organism available is that one can use positional information to select markers with equal recombinational spacing across the genome (for example a marker every 20 cM), which greatly facilitates mapping of traits of interest. Moreover, one can compare local recombination frequencies with features of the physical map position to identify, for example, recombination hotspots, chromosomal inversions, and gene-rich genomic segments (Petes, 2001;Myers et al, 2005;Kulathinal et al, 2008;Niehuis et al, 2010;Werren et al, 2010).…”

“…Niehuis et al (2008) then published an interspecific N. vitripennis  N. giraulti map containing 38 molecular markers. The most recent linkage map for Nasonia is based on a large number of interspecific single nucleotide polymorphism markers identified from the annotated Nasonia genome sequences (1255 markers; Niehuis et al, 2010).…”

“…Considering the chromosome-anchored markers developed by Rü tten et al (2004), we were able to associate the original linkage groups of N. vitripennis distinguished by Saul (1993) with the five Nasonia chromosomes. We contrast recombination frequencies of homologous genomic segments between the intraspecific N. vitripennis cross and an interspecific N. vitripennis  N. giraulti mapping population of embryos that showed no MTRD using the data published by Niehuis et al (2010). We next compare recombination frequencies of embryos with those of adults in two interspecific crosses (that is N. vitripennis  N. longicornis and N. vitripennis  N. giraulti) to determine the effect of MTRD on recombination estimates and marker order.…”