EVOLUTION OF POSTMATING REPRODUCTIVE ISOLATION - THE COMPOSITE NATUREOF HALDANE RULE AND ITS GENETIC BASES

The patterns of postmating reproductive isolation in general follow Ha ldane's rule that the heterogametic sex is much more likely to become inviable or sterile than the homogametic sex. There are two approaches to explaining the rule. The first approach assumes that genic diverge nce affects both sexes equally but their difference in chromosome cons titution leads to the sex-dependent manifestation; for example, the he terogametic hybrids have a greater degree of X-autosome imbalance. The second approach assumes that genes affecting the heterogametic sex ha ve evolved more rapidly and the genotypic difference between sexes is unimportant. Neither approach in its search for a unitary genetic basi s of Haldane's rule has been successful. The major point of this artic le is that Haldane's rule is most likely a composite rule-the first ap proach is appropriate for hybrid inviability but is not sufficient for hybrid sterility, which requires the second approach in addition. Thr ee lines of evidence are presented: (1) genes causing hybrid inviabili ty generally do not behave in a sex-dependent manner and, thus, X-auto some imbalance is crucial; (2) interspecific crosses yielding sterilit y outnumber those yielding inviability by more than 10-fold in Drosoph ila and mammals; and (3) in Drosophila, genes causing hybrid male ster ility greatly outnumber genes causing male inviability. Several models pertaining to the faster evolution of hybrid sterility in the heterog ametic sex (than in the homogametic sex) are discussed. Finally, genes affecting the viability and fertility of interspecific hybrids seem t o belong in a class distinct from those represented in mutagenic studi es or those detected as intraspecific variations. The implications of this qualitative and quantitative break at the species level need to b e heeded.