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 F2 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 F2 hybrids with N. vitripennis cytoplasm account for most of the intrinsic hybrid inviability in this cross. The high mortality rate in F2 hybrids with N. giraulti cytoplasm cannot be explained by the single identified TRDL alone, however.

Figure 1.—

Linkage map inferred from marker segregation data in a N. giraulti × N. vitripennis F₂ hybrid population of male embryos (N = 225). Recombination distances are shown in Haldane centimorgans. Bars near chromosomes specify the 95% confidence limits for the position of predicted TRDL; arrowheads point to the region with the highest posterior probability for the position of TRDL. Percentages indicate the estimated mortality caused by each TRDL in a population of F₂ hybrid males with [g] = N. giraulti and [v] = N. vitripennis cytoplasm, respectively.

Figure 2.—

Distribution of the interval size between consecutive markers in the N. vitripennis × N. giraulti chromosome map. The superimposed graph shows a normal distribution with a mean of 11.7 cM against which the observed interval size distribution was tested (K–S test, P < 0.01).

Figure 3.—

Density distributions of the posterior probability for (A) position and (B) effect of TRDL on chromosomes in adult male F₂ hybrids of N. giraulti and N. vitripennis. Each distribution was calculated from 20,000 Markov chain Monte Carlo samples taken from the stationary phase and assuming a Poisson prior (λ = 0.5) for the number of TRDL. Shown are density distributions for one TRDL on each of the depicted chromosomes; the posterior probabilities for these assumptions were 80.86, 72.79, 48.15, and 77.70% (see Table 1). The genotype of the cytoplasm of the population, in which marker transmission ratio distortion was seen, is indicated by [g] = N. giraulti and [v] = N. vitripennis, respectively. Underlined markers were tested for segregation ratio distortion in a second population of adult F₂ hybrid males to confirm the TRDL (see Figure 4).

Figure 4.—

Deviation of selected markers linked to predicted transmission ratio distorting loci in six populations of male F₂ hybrids of N. giraulti and N. vitripennis from the expected 50% N. vitripennis alleles. The genotype of the cytoplasm of a population is indicated by [g] = N. giraulti and [v] = N. vitripennis. Solid bars: deviation of the markers in the two populations ([g] and [v] cytoplasm, respectively) of adult wasps in the original experiment, which aimed to identify possible TRDL (asterisks indicate significance). Shaded bars: deviation of the same markers in two independent populations ([g] and [v] cytoplasm, respectively) of adult wasps studied in a second (confirmation) experiment (asterisks indicate significance). Open bars: deviation of markers in early (<16 hr old) hybrid embryos.