Cytonuclear Genic Incompatibilities Cause Increased Mortality in Male F2 Hybrids of Nasonia giraulti and N. vitripennis

Abstract

The haplodiploid wasp genus Nasonia is a promising model for studying the evolution of genic incompatibilities due to the existence of interfertile species and haploid males. The latter allows for significantly reducing the sample size required to detect and map recessive dysfunctional genic interactions. We exploited these features to study the genetics of intrinsic hybrid inviability in male F 2 hybrids of Nasonia giraulti and N. vitripennis. Analyzing marker segregation in 225 hybrid embryos, we inferred a linkage map with 38 framework markers. The markers were tested for marker transmission ratio distortion (MTRD) and interchromosomal linkage disequilibrium in populations of embryonic and adult hybrids. We found evidence for four transmission ratio distorting loci (TRDL). Three TRDL showed a deficit of the N. giraulti allele in hybrids with N. vitripennis cytoplasm. A separate TRDL exhibited a deficiency of the N. vitripennis allele in hybrids with N. giraulti cytoplasm. We ascribe the observed MTRD in adult hybrids to cytonuclear genic incompatibilities causing differential mortality during development since hybrid embryos did not show MTRD. The identified cytonuclear genic incompatibilities in F 2 hybrids with N. vitripennis cytoplasm account for most of the intrinsic hybrid inviability in this cross. The high mortality rate in F 2 hybrids with N. giraulti cytoplasm cannot be explained by the single identified TRDL alone, however.

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

“…We initially selected two microsatellite markers per scaffold, one on either end, to be able to map and orient the scaffolds along the chromosomes. Although the microsatellite markers of the Nv100 series (see Supplementary Table 1) were specifically screened for polymorphisms within N. vitripennis, those of the Nv300 series were tailored to match and/or replace molecular markers that had been used by Niehuis et al (2008) to infer an N. giraulti  N. vitripennis framework map.…”

“…This allowed for a comparison of the recombination frequencies between embryos and adults within crosses and of embryos and adults between reciprocal crosses. All individuals had been genotyped for 38 single nucleotide polymorphism markers by Niehuis et al (2008).…”

“…This made it possible to homologize the earlier inferred linkage groups of Nasonia (Saul, 1993;Gadau et al, 1999) with its five chromosomes (Gokhman and Westendorf, 2000). 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).…”

“…Specifically, recombination frequencies may be increased or decreased when combining genomes of two species because of major genome reorganizations or the release of recombination suppressors (Trickett and Butlin, 1994;Zhang et al, 1999). Moreover, the recovery of alleles may be affected by nuclear-nuclear and nuclear-cytoplasmic genic incompatibilities, both of which are known to occur in Nasonia hybrids (Breeuwer and Werren, 1995;Gadau et al, 1999;Niehuis et al, 2008). Weston et al (1999) have presented a formal model, which suggested that hybrid mortality because of nucleo-nucleo genic incompatibilities can lead to pseudo-linkage and thus the inference of a false marker order.…”

“…Weston et al (1999) have presented a formal model, which suggested that hybrid mortality because of nucleo-nucleo genic incompatibilities can lead to pseudo-linkage and thus the inference of a false marker order. To test for marker transmission ratio distortion (MTRD) in Nasonia hybrids, Niehuis et al (2008) compared marker allele frequencies between embryos and adults. They found that some markers indeed show a significantly distorted recovery in adults compared with embryos and attributed the MTRD to mortality associated with particular genotypes during larval development.…”