Maternal effect as a cause of exceptions for Haldane's rule.

I N 1922, J. B. S. HALDANE stated: “When in the F, offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous [heterogametic or Xu] sex.” This is one of a few general rules in evolutionary biology. Indeed, many hybrid crosses obey HALDANE’S rule especially in sterility, but exceptions are not rare in inviability: Nine such cases are known in 23 Drosophila interspecific crosses that produce only one sex (Wu and DAVIS 1993). In this note, I will show that these exceptions are not accountable by the suggestion that “postzygotic isolation often involves a modest number of partially recessive alleles” (TUREILI and ORR 1995) but are mainly caused by the maternal effect. This has been repeatedly pointed out by many authors (e.g., PATTERSON and STONE 1952; SAWAMURA et al. 1993a,b; Wu and DAVIS 1993). It is important to emphasize this alternative “maternal effect model,” because a completely dominant allele(s) are involved in this incompatibility. There is no a p ~ o r i reason to assume that postmating isolation is caused by a loss-of-function type recessive allele(s) ( cJ: ORR 1993; TUFEI.L.I and ORR 1995; see WU et al. 1996). Table 1 lists exceptions to HALDANE’S rule on hybrid inviability from Drosophila studies. The inviability in cross (2) may be caused by the same system as cross ( l ) , since the maternal species is the same and the paternal species are close relatives. In at least four cases (crosses 3, 4, 7, and 8) hybrid females are viable in the reciprocal cross. These cases are not explicable by the involvement of a modest number of partially recessive alleles. When the X chromosome of species I (X, ) has slightly dominant deleterious alleles above a threshold but X, does not, XI X, should be inviable but ?& Yl viable, resulting in an exception for HALUANE’S rule in one of reciprocal crosses. But if this were the case, we would predict that both X , X, and X, Y2 are, in most of the cases, inviable in the reciprocal cross (at least, chromosomally equivalent XI& should be inviable). The inviability of hybrid males in the reciprocal cross (crosses 4 and 7) is supposed to be caused by a different system than hybrid female inviability (see SAWAMURA et al. 1993a,b for cross 7).