Cytogenetics and sex determination in collared lemmings

Abstract

Collared lemmings (Dicrostonyx groenlandicus rubricatus) from northeastern Alaska were found to have sex chromosomes that differ from those of their Siberian congeners, because of fusion to a particular pair of autosomes. But, as in Siberian lemmings, breeding experiments showed that sex determination involves an X-linked "male-repressor," which causes carriers to develop as fertile females, despite the presence of a Y chromosome. Genotypic frequencies in offspring are consistent with Mendelian expectations of such a system, hence natal sex ratios normally favor females. X-linkage of the male-repressor in Siberia and in Alaska indicates that the gene is probably located on the "original" arms of the X chromosome rather than on the fused autosomal arms, which differ on the two continents. One consequence of the autosomal fusion to the sex chromosomes is that deleterious recessive alleles on the autosome fused to the X chromosome are more resistant to selection than at truly autosomal loci. Another consequence is that, because males are heterozygous for loci fused to the sex chromosomes, they are more resistant to inbreeding depression than XX females. One inbred line produced a natal sex ratio of 67% males. The male-bias probably resulted from loss of the male-repressor and from a lethal carried on the formerly autosomal arm of the X chromosome. As inbreeding coefficients approached 0.3, the lethal would have been homozygous in half of the homogametic (female) zygotes. This phenomenon may explain the excess of males and XY females observed in earlier work. Also, if under the natural mating system, inbreeding depression limits fitness, then fusions of autosomal chromatin to the heterochromosomes could be an adaptation to reduce inbreeding depression in heterogametic individuals. Some other genetic features of collared lemmings do suggest endogamy. Female-biased sex ratios can evolve when mating occurs between neighboring individuals who are more related than if mating occurred randomly. Two proposed sources of such "viscous" gene flow in lemmings are cyclical changes in population density and mosaic habitat. Alternatively, could climate may favor winter aggregation and inhibit the dispersal of winter-born offspring, which would mature and mate with close relatives; dispersal and outbreeding would occur in summer. Thus, inbreeding would be seasonal rather than density-dependent and it is unnecessary to suppose discontinuous habitat.