Origin of males by genome loss in an autoparasitoid wasp

Abstract

Autoparasitoid wasps lay fertilized (female) eggs in homopteran nymphs and unfertilized (male) eggs in immature parasitoids, often in females of their own species. Autoparasitoid host relationships are generally obligate; a male egg will not develop in the homopteran host even if laid there. While sex is controlled by the female by selective fertilization of eggs, the sex ratio is constrained by the availability of the appropriate hosts. However, in a population of the autoparasitoid Encarsia pergandiella in Ithaca, NY, some of the males develop, like females, as primary parasitoids of whiteflies. A cytogenetic examination of eggs laid in whiteflies revealed that these ‘primary’ males are haploid, but develop from fertilized eggs. Following fertilization, one set of chromosomes becomes overcondensed and is lost, thus converting the fertilized (female) egg into a haploid (male) egg. Genetic analysis suggests that the production of primary males is heritable; males that develop from parasitoid hosts do not produce primary sons, whereas primary males do. However, the transmission and/or expression of the primary male trait is low and variable. Only about 50 per cent of primary male matings result in any primary sons, and only about 28 per cent of all offspring produced on whiteflies are male. X-irradiation of primary males had no effect on the number of primary sons produced but greatly reduced the number of daughters, suggesting that it is the paternal genome that is lost in the production of primary males. Paternal inheritance of genome loss has been described in one other parasitic wasp, Nasonia vitripennis (Walker). There, chromosome loss is caused by a supernumerary chromosome (PSR). A supernumerary chromosome was not observed in the primary male E. pergandiella. It is unknown how widespread primary male production is among populations of E. pergandiella and other autoparasitoids.