A single gene causes both male sterility and segregation distortion in Drosophila hybrids

Abstract

A central goal of evolutionary biology is to identify the genes and evolutionary forces that cause speciation, the emergence of reproductive isolation between populations. Despite the identification of several genes that cause hybrid sterility or inviability-many of which have evolved rapidly under positive Darwinian selection-little is known about the ecological or genomic forces that drive the evolution of postzygotic isolation. Here, we show that the same gene, Overdrive, causes both male sterility and segregation distortion in F1 hybrids between the Bogota and U.S. subspecies of Drosophila pseudoobscura. This segregation distorter gene is essential for hybrid sterility, a strong reproductive barrier between these young taxa. Our results suggest that genetic conflict may be an important evolutionary force in speciation.

Fig.1

A) The sepia region of the USA X-chromosome was introduced into an otherwise pure Bogota background using a criss-cross design: recombination occurs in females and the visible marker sepia was selected in males. Bogota material is colored black and USA material is colored white. Females have two X chromosomes, males have one X chromosome and one Y chromosome (denoted by a hook). B) When crossed to USA males, heterozygous introgression females produce two types of hybrid males. All sepia introgression hybrid males were fertile and showed normal segregation whereas control F₁ hybrid males were sterile and showed segregation distortion, as expected. C) Hybrid sterility and segregation distortion both mapped to a region spanning ∼20kb that included five predicted genes of which GA19777 is the fastest evolving.

Fig. 2

P{w⁺; GA19777^USA} rescues fertility in F₁ hybrid males as measured blind in a sperm motility assay. Three independent transgenic strains were tested; the total number of males tested per genotype is denoted by N. The two genotypes are identical except for presence/absence of the construct. P values were calculated using χ² tests with one degree of freedom.

Fig. 3

P{w⁺; GA19777^BOG} induces segregation distortion in sepia introgression hybrid males. Sepia introgression hybrid males that inherit the P{w⁺; GA19777^BOG} transgene show significantly female-biased progeny compared to males that do not inherit the transgene. The two genotypes are identical except for presence/absence of the construct. Segregation distortion is also accompanied by a reduction in the total number of progeny and, in the case of BOG1-2, in the number of daughters produced. Two independent transgenic strains (BOG1-1 and BOG1-2) were tested; N denotes the number of fathers tested per genotype; mean values along with S.E. (in brackets) are reported. P values were calculated using ANOVA. Transgene males were inferred from the presence of w⁺ individuals among F₁ and F₂ progeny. We modified the cross for the transgenic Bogota strain (BOG1-2): we first crossed introgression females to Bogota males heterozygous for P{w⁺; GA19777^BOG}. When crossed to USA white males, these females produce two types of hybrid sons: those that inherit a transgenic GA19777^BOG along with endogenous GA19777^USA and those that inherit only endogenous GA19777^USA. Importantly, with both BOG1-1 and BOG1-2, transgenic hybrid males produced (rare) white and wild-type sons in roughly equal numbers, showing that sex ratio distortion is not due to transgene-induced male lethality.