A comparison of genetic variability at X-linked and autosomal loci in kangaroos, man and Drosophila

Abstract

SUMMARY: This paper tests the hypothesis that haplodiploidy or X linkage leads to less genetic variability. Although haplodiploid organisms exhibit a low level of genetic variability the wide variation existing between different diploid organisms implies that factors other than the genetical system could also be responsible. In order to test the hypothesis critically it is necessary to compare the level of genetic variability between X-linked and autosomal genes within a closely related group of organisms. For kangaroos, the ascertainment bias for X-linked loci has been removed by assuming the correctness of Ohno's law of conservation of the mammalian X, i.e. that genes found to be X-linked in man can be assumed to be X-linked in kangaroos. For Man and Drosophila, it has been assumed that the percentage of the karyotype which is X chromosome can be used as the expectation for the percentage of X-linked polymorphisms. No difference between the two classes of loci is evident in kangaroos and man for percentage polymorphism. The data however have confidence limits which would allow autosomal loci to have three times greater percentage polymorphism. In Drosophila the published data of Prakash show that autosomal loci are polymorphic about twice as frequently as are their X-linked counterparts. Thus there may be a modest reduction in percentage polymorphism as a result of X-linkage (i.e. haplodiploidy). No reduction in the number of alleles per locus or average heterozygosity at those loci which are polymorphic is evident in kangaroos, man, or Drosophila. More data on more X-linked enzymes are necessary to establish firmly that there is a real reduction in percentage polymorphism and to estimate its extent. The kangaroo data are incompatible with the hypothesis that a large fraction of the variability is maintained by simple overdominance since overdominance is very unlikely in the quasi-haploid genetical system which results from the paternal X inactivation mode of dosage compensation used by kangaroos. This is the first report on level of enzymic variability in marsupials. 17% of autosomal loci and 18% of X-linked loci are polymorphic, average heterozygosity is 4% for autosomal and 4% for X-linked loci and number of alleles per locus is 1·25 for autosomal and 1·21 for X-linked loci. These figures are somewhat lower than for eutherian mammals.