A THEORETICAL ANALYSIS OF THE EFFECTS OF SEX CHROMOSOME ANEUPLOIDY ON X AND Y CHROMOSOME MEIOTIC DRIVE.

Extra sex chromosomes are normally detrimental to the individual carrying them. In XY (or WZ) sex determining systems, an extra X chromosome in the homogametic sex generates enough X-autosome imbalance to usually cause inviability, or at least sterility. On the other hand, extra Y chromosomes are sometimes tolerated, although in mammals and other higher organisms where the Y is actively involved in sexual development, XXY individuals are generally sterile. In Drosophila and perhaps other invertebrates where the Y is largely genetically inert, a single extra Y may be permitted in both sexes, while two extra copies is only fertile in XXYY females (Cooper, 1956), if at all. Even if XXY and XYY genotypes were perfectly viable and fertile, abnormal meiotic segregation and the consequent production of unbalanced gametes would lead to enough zygotic lethality to reduce their overall fitness (see Fig. 1). Thus we expect sex chromosome aneuploids in nature to be rare, primarily arising from recurrent spontaneous nondisjunction events. However, the literature records many cases of unusual accessory or sex chromosome constitutions found in both plants and animals (particularly insects, see White, 1973) which must have faced at least a transient period of aneuploidy during the process of their establishment. The genetic forces which might be responsible for this form of karyotype evolution are at present largely in the realm of speculation (White, 1978). I recently (Lyttle, 1981a) reported an experimental population of Drosophila melanogaster in which such aneuploids were present at high frequency. This population had been segregating for a type of Y chromosome meiotic drive (pseudo-Y or pY drive, Lyttle, 1977), which operates by coupling the Y chromosome to the autosomal drive element Segregation distorter (SD) by reciprocal translocation. Normally, pY drive males produce only male offspring, as potential daughters are removed both by the SD mediated dysfunction of X;SD+ gametes and the concomitant lethality of the hypoploid zygotes arising from fertilization events involving X;SD sperm. Since the pY drive was expected to push the male frequency to near 100% of the population, the observed high frequency of aneuploids was interpreted as a strategy for reducing this deviation of the population sex ratio from the optimal 1:1 value. This would occur because XYY males and XXY females, owing to their production of gametes with unusual sex chromosome combinations, have proportionately more daughters than do their XY and XX counterparts under the conditions of pY drive (Lyttle, 1981a). That is, since the y2 portion of the translocation carries the large missing piece of the SD chromosome, its added presence in XY;SD sperm can rescue usually hypoploid zygotes to give autosomally euploid XXY females. To investigate this apparent selection for aneuploidy, I constructed a simple discrete generation model which included effects of chromosomal segregation, fitness, and meiotic drive, the latter defined as the excess recovery in the gametes of one member of a pair of heterozygous alleles or heteromorphic chromosomes (cf. Sandler and Novitski, 1957; Zimmering et al., 1970). The resulting equations gave pre1 This research was supported by Public Health Service Grant GM 24083.