X-4 Translocations and Meiotic Drive in Drosophila melanogaster Males: Role of Sex Chromosome Pairing

Abstract

Males carrying certain X-4 translocations exhibit strongly skewed sperm recovery ratios. The X(P)4(D) half of the translocation disjoins regularly from the Y chromosome and the 4(P)X(D) half disjoins regularly from the normal 4. Yet the smaller member of each bivalent is recovered in excess of its pairing partner, apparently due to differential gametic lethality. Chromosome recovery probabilities are multiplicative; the viability of each genotype is the product of the recovery probability of its component chromosomes. Meiotic drive can also be caused by deficiency for X heterochromatin. In(1)sc(4L)sc(8R) males show the same size dependent chromosome recoveries and multiplicative recovery probabilities found in T(1;4)B(S) males. Meiotic drive in In(1)sc(4L)sc(8R) males has been shown to be due to X-Y pairing failure. Although pairing is regular in the T(X;4) males, the striking phenotypic parallels suggest a common explanation. The experiments described below show that the two phenomena are, in fact, one and the same. X-4 translocations are shown to have the same effect on recovery of independently assorting chromosomes as does In(1)sc(4L)sc(8R). Addition of pairing sites to the 4(P)X(D) half of the translocation eliminates drive. A common explanation-failure of the distal euchromatic portion of the X chromosome to participate in X:Y meiotic pairing-is suggested as the cause for drive. The effect of X chromosome breakpoint on X-4 translocation induced meiotic drive is investigated. It is found that translocations with breakpoints distal to 13C on the salivary map do not cause drive while translocations broken proximal to 13C cause drive. The level of drive is related to the position of the breakpoint-the more proximal the breakpoint the greater the drive.