Early events in speciation: polymorphism for hybrid male sterility in Drosophila

Abstract

Capturing the process of speciation early enough to determine the initial genetic causes of reproductive isolation remains a major challenge in evolutionary biology. We have found, to our knowledge, the first example of substantial intraspecific polymorphism for genetic factors contributing to hybrid male sterility. Specifically, we show that the occurrence of hybrid male sterility in crosses between Drosophila mojavensis and its sister species, Drosophila arizonae, is controlled by factors present at different frequencies in different populations of D. mojavensis. In addition, we show that hybrid male sterility is a complex phenotype; some hybrid males with motile sperm still cannot sire offspring. Because male sterility factors in hybrids between these species are not yet fixed within D. mojavensis, this system provides an invaluable opportunity to characterize the genetics of reproductive isolation at an early stage.

Fig. 1.

Map of the southwestern United States and northwestern Mexico showing the distributions of D. mojavensis and D. arizonae and the areas of sympatry. The distribution of D. arizonae continues south of the range of the map to Guatemala. The populations used in this study are marked with asterisks. The D. mojavensis populations are from DE, TO, OPNM, WC, and CI. The D. arizonae tester population is from PERA.

Fig. 2.

The average proportion of males with motile sperm (±1 SE) by population. Light bars represent the average across isofemale lines for hybrid F₁ males from the cross of female D. mojavensis from the population shown and male D. arizonae (PERA) (number of isofemale lines: CI n = 15; TO n = 13; DE n = 14; OPNM n = 6; WC n = 8). Dark bars are the average motility of males from the pure species cultures (number of males per population: CI n = 30; TO n = 30; DE n = 68; OPNM n = 95; PERA n = 77). Average male sperm motility drops from between 92% and 100% in all of the pure species stocks to between 54% and 84% when males are hybrids. There is also significant variation between populations for hybrid male motility (F = 3.06, df = 4/50.9, P = 0.0246).

Fig. 3.

The fraction of F₁ hybrid sons with motile sperm from the cross of female D. mojavensis and male D. arizonae averaged by mother within isofemale line. Isofemale lines are shown in ascending order of the average fraction of sons with motile sperm organized by population. The error bars indicate 1 SE above and below the mean. The number of females tested per isofemale line in ascending order of the average fraction of sons with motile sperm are as follows. DE: 3, 8, 7, 3, 13, 4, 3, 11, 5, 5, 7, 12, 10, and 2; OPNM: 3, 8, 7, 4, 11, 4, 2, and 2; CI: 6, 5, 10, 7, 11, 16, 7, 5, 11, 6, 18, 8, 9, 15, and 2; TO: 2, 9, 2, 6, 11, 4, 2, 3, 7, 4, 2, 6, and 5; and WC: 12, 6, 23, 7, 8, 3, 6, and 5. There is significant variation within isofemale line (Z = 6.86, P < 0.0001) and between isofemale lines (Z = 3.32, P = 0.0005) for hybrid male motility.