Widespread occurrence of XXY females in Drosophila mojavensis and related species

Bridges first reported that XXY individuals are fertile females in Drosophila melanogaster, arising at low frequency (~1/2000) through errors in chromosome segregation (BRIDGES 1914; BRIDGES 1916). Although widely used in genetic studies, XXY females are seldom found in wild-type strains or natural populations, presumably because natural selection keeps them at very low frequency. Here we show that many wild-type strains of D. mojavensis and its close relatives D. arizonae, D. navojoa, and D. wheeleri carry XXY and XXYY females at frequencies of up to 88%; males from these strains are frequently XYY or XYYY. Although field collections were hampered by population declines and safety concerns, we found one XXY female (out of 87) and one XYY male (out of 36) in a natural population of D. mojavensis, indicating that these genotypes also occur at appreciable frequencies in nature. XXY females are expected to produce XY-bearing and X-bearing eggs in equal proportions; instead, we found a 57:43 ratio. Mathematical modeling shows that this meiotic-drive advantage is sufficient to explain high frequencies of XXY females. It is universally accepted that Y evolution responds exclusively to male selection, yet in XXY-bearing species it also responds to female fitness.