Academic journal article Genetics

Cytonuclear Genic Incompatibilities Cause Increased Mortality in Male F^sub 2^ Hybrids of Nasonia Giraulti and N. Vitripennis

Academic journal article Genetics

Cytonuclear Genic Incompatibilities Cause Increased Mortality in Male F^sub 2^ Hybrids of Nasonia Giraulti and N. Vitripennis

Article excerpt

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^sub 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^sub 2^ hybrids with N. vitripennis cytoplasm account for most of the intrinsic hybrid inviability in this cross. The high mortality rate in F^sub 2^ hybrids with N. giraulti cytoplasm cannot be explained by the single identified TRDL alone, however.

UNDERSTANDING the genetic basis of reproductive barriers is one of the major challenges in evolutionary genetics and in speciation genetics in particular (Coyne and Orr 2004). Two frequently observed reproductive barriers that isolate species are intrinsic hybrid inviability and sterility. They can be caused by differences in ploidy levels, chromosomal organization, infection by endosymbionts, and genic incompatibilities (e.g., STEBBINS 1950; WERREN 1998; JOHNSON 2000; DELNERI et al. 2003). So far, only a few studies have identified genes that are incompatible in hybrids and provided insights to how negative genic interactions account for hybrid inviability and sterility (e.g., WITTBRODT et al. 1989; SCHARTL et al. 1994; MALITSCHEK et al. 1995; TING et al. 1998; BARBASH et al. 2003; PRESGRAVES et al. 2003; BRIDEAU et al. 2006). In general, however, little is known about the nature of genic incompatibilities that cause intrinsic postzygotic reproductive isolation (HUTTER 1997; COYNE and ORR 2004; ORR et al. 2004; ORR 2005). Three problems may account for this lack of knowledge: the difficulty of carrying out genetics between populations that are reproductively isolated (LEWONTIN 1974; ORR et al. 2004; Orr 2005), the complexity of genic incompatibilities that frequently involve more than just two genes (e.g., MULLER 1942; DOBZHANSKY 1975; CABOT et al. 1994; ORR and IRVING 2001), and the fact that genic incompatibilities tend to be recessive (Muller 1942; Tao and Hartl 2003; see also Coyne and Orr 2004).

The parasitic wasp genus Nasonia has two particular features that allow us to overcome these obstacles and facilitate speciation genetic studies: a haplodiploid sex determination and the ease with which its species can be crossed in the laboratory (Whiting 1967; Skinner and Werren 1980; Breeuwer and Werren 1990; see also Beukeboom and Desplan 2003). In arrhenotokous species, females develop from fertilized eggs and are diploid whereas males develop parthenogenetically from unfertilized eggs and are haploid. Since there are no intralocus interactions in haploidmales, alleles can easily be tested individually for their phenotypic effect in this sex. This significantly reduces the population sizes required to detect and map recessive alleles and epistatic loci in haploid F2 hybrid males (GADAU et al. 1999, 2002; WESTON et al. 1999; WILFERT et al. 2007). The genetics of genic incompatibilities can easily be explored in the genus Nasonia, since interspecific F1 hybrid females are viable and fertile while a certain percentage of their F2 hybrid male offspring are not (Breeuwer and Werren 1995). …

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