The evolution of XY females in mammals

Abstract

SUMMARYSome lemmings have a large proportion of XY females in the population, as well as XX females and XY males. In this paper we first review the biological literature on XY females in mammals, with particular emphasis on the genetics and cytogenetics of this trait. We then consider population genetics models of the behaviour of this trait, and we show that there are serious discrepancies between predictions and observations regarding the sex ratio and the frequency of XY females; in several lemming populations the reported sex ratio is lower and XY females are more common than expected. Finally we consider evolutionary models to understand why XY females persist in these populations and how selection might act on other parts of the reproductive biology to modify the system.

Sex ratio, XY females and absence of inbreeding in a population of the Wood Lemming, Myopus schisticolor Lilljeborg, 1844

“…Until now such an increase has not been found in the Malaya Sosva population, so the reason for the excess of XY females is probably the meiotic drive of the Y chromosome in males (as in Dicrostonyx) and perhaps the preferential segregation of the X* in X*XO females. If this is so the equilibrium frequency of males must be less than 0.25 (Bull & Bulmer, 1981). The goodness-of-fit to 0.25 for the proportion of males in the population was tested, data being pooled on overwintered and year-born lemmings (Table 1).…”

“…In X*Y females of the Wood Lemming only X*bearing gametes are formed (Fredga et al, 1976(Fredga et al, , 1977 and in the males of the Varying Lemming the Y segregates have a ratio of 0.54-0.59 (Gileva, 1987). In both cases meiotic drive is observed to bring about a reduction in the proportion of males and an increase in the frequency of XY females (Bengtsson, 1977;Bull & Bulmer, 1981).…”

“…In natural populations and experimental colonies three female genotypes (X°X°, X*XO and X'Y) and a male genotype X°Y have been found. Such a nomenclature of genotypes was used first by Bull & Bulmer (1981), while original designations of Fredga et al, who had discovered an unusual sex-determining mechanism in Myopus, were XX, X*X, XY and XY, respectively (1976,1977).…”

“…Theoretical analysis has shown that inbreeding can prevent both X-linked and autosomal repressors of X* mutation from spreading and fixation, i.e. it can contribute to the maintenance of the X*Y female genotype and the excess of females in populations (Maynard Smith & Stenseth, 1976;Bull & Bulmer, 1981). Stenseth (1978) stated that in lemmings which exhibited drastic fluctuations in density, extensive inbreeding must have been common at phases both of low density and early increase.…”

Sex ratio evolution in lemmings

“…The wood lemming, Myopus schisticolor, and the varying lemming, Dicrostonyx torquatus, have two types of X chromosome, X° which behaves normally and X which suppresses the male-determining property of the Y chromosome (reviewed by Bull and Bulmer, 1981). All males are X°Y, while there are three female genotypes, X°X°, XX0 and XY.…”