Inheritance of Gynandromorphism in the Parasitic Wasp Nasonia Vitripennis

By Kamping, Albert; Katju, Vaishali et al. | Genetics, March 2007 | Go to article overview

Inheritance of Gynandromorphism in the Parasitic Wasp Nasonia Vitripennis


Kamping, Albert, Katju, Vaishali, Beukeboom, Leo W., Werren, John H., Genetics


ABSTRACT

The parasitic wasp Nasonia vitripennis has haplo-diploid sex determination. Males develop from unfertilized eggs and are haploid, whereas females develop from fertilized eggs and are diploid. Females and males can be easily distinguished by their morphology. A strain that produces individuals with both male and female features (gynandromorphs) is studied. We provide data on female/male patterning within and between individuals, on environmental effects influencing the occurrence of gynandromorphism, and on its pattern of inheritance. A clear anterior/posterior pattern of feminization is evident in gynandromorphic individuals that developed from unfertilized haploid eggs. The proportion of gynandromorphic individuals can be increased by exposing the mothers to high temperature and also by exposing embryos at early stages of development. Selection for increased gynandromorph frequency was successful. Backcross and introgression experiments showed that a combination of a nuclear and a heritable cytoplasmic component causes gynandromorphism. Analyses of reciprocal F^sub 2^ and F^sub 3^ progeny indicate a maternal effect locus (gyn1) that maps to chromosome IV. Coupled with previous studies, our results are consistent with a N. vitripennis sex determination involving a maternal/zygotic balance system and/or maternal imprinting. Genetics and temperature effects suggest a temperature-sensitive mutation of a maternally produced masculinizing product that acts during a critical period in early embryogenesis.

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ALMOST all taxa contain species with two sexes: males and females. However, the genetic mechanisms underlying the establishment of the two sexes are quite diverse. From an evolutionary point of view, it is important to understand the genetics behind the various mechanisms. In many organisms sex determination relies on heteromorphic sex chromosomes. In mammals the presence of the Y chromosome is the primary determinant of maleness and in Drosophila the ratio of X chromosome to autosomes is the key factor for sex determination. Chromosomal sex determination also applies for birds and fish. This type of primary sex determination does not hold for the order Hymenoptera, which includes ants, bees, and wasps. These insects have a haplo-diploid sex determination system: haploid males arise from unfertilized eggs, while diploid females arise from fertilized eggs. However, diploid males and triploid females have also been reported (WHITING 1960), but never haploid females. It is unclear how this can be reconciled with the mechanism of sex determination.

The honeybee, a member of the Hymenoptera order, has single locus complementary sex determination (sl-CSD) (MACKENSEN 1955; LAIDLAW et al. 1956). BEYE et al. (2003) characterized the csd gene and found many alleles with different amino acid sequences. Heterozygotes for this gene develop into females, whereas hemi- and homozygotes develop into males. Inactivation of the csd gene also leads to development of males. The consequence of this mode of sex determination is the presence of diploid males, which can easily be generated by inbreeding under laboratory conditions. This type of sex determination was originally demonstrated 60 years ago for the parasitic wasp Bracon hebetor (WHITING 1943) and has now been confirmed for >60 species of Hymenoptera (STOUTHAMER et al. 1992; COOK 1993a,b; PERIQUET et al. 1993; BUTCHER et al. 2000; VANWILGENBURG et al. 2006). However, not all species generate diploid males by inbreeding and these therefore do not have sl-CSD. This has led to the development of alternative models for haplo-diploid sex determination, as discussed and reviewed by COOK (1993b), BEUKEBOOM (1995), and DOBSON and TANOUYE (1998).

Nasonia vitripennis, a small parasitic wasp, is one of the species that does not have sl-CSD (WHITING 1967; SKINNER and WERREN 1980), although, as in other Hymenoptera, it has a haplo-diploid system of sex determination. …

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