Haldane's rule: Hybrid sterility affects the heterogametic sex first because sexual differentiation is on the path to species differentiation

Prevention of recombination is needed to preserve both phenotypic different iation between species and sexual phenotypic differentiation within species . For species differentiation (speciation), isolating barriers preventing r ecombination may be pre-zygotic (gamete transfer barriers), or post-zygotic (either a developmental barrier resulting in hybrid inviability, or a chro mosomal-pairing barrier resulting in hybrid sterility). The sterility barri er is usually the first to appear and, although often initially only manife st in the heterogametic sex (Haldane's rule), is finally manifest in both s exes. For sexual differentiation, the first and only barrier is chromosomal -pairing, and always applies to the heterogametic sex. For regions of sex c hromosomes affecting sexual differentiation there must be something analogo us to the process generating the hybrid sterility seen when allied species cross. Explanations for Haldane's rule have generally assumed that the chro mosomal-pairing barrier initiating evolutionary divergence into species is due to incompatibilities between gene products ("genic"), or sets of gene p roducts ("polygenic"), rather than between chromosomes per se ("chromosomal "). However, if chromosomal incompatibilities promoting incipient sexual di fferentiation could also contribute to the process of incipient speciation, then a step towards speciation would have been taken in the heterogametic sex. Thus, incipient speciation, manifest as hybrid sterility when "varieti es" are crossed, would appear at the earliest stage in the heterogametic se x, even in genera with homomorphic sex chromosomes (Haldane's rule for hybr id sterility). In contrast, it has been proposed that Haldane's rule for hy brid inviability needs differences in dosage compensation, so could not app ly to genera with homomorphic sex chromosomes. (C) 2000 Academic Press.