Genetic Dissection of Hybrid Incompatibilities Between Drosophila Simulans and D. Mauritiana. Iii. Heterogeneous Accumulation of Hybrid Incompatibilities, Degree of Dominance, and Implications for Haldane's Rule

Abstract

The genetic basis of Haldane's rule was investigated through estimating the accumulation of hybrid incompatibilities between Drosophila simulans and D. mauritiana by means of introgression. The accumulation of hybrid male sterility (HMS) is at least 10 times greater than that of hybrid female sterility (HFS) or hybrid lethality (HL). The degree of dominance for HMS and HL in a pure D. simulans background is estimated as 0.23-0.29 and 0.33-0.39, respectively; that for HL in an F 1 background is unlikely to be very small. Evidence obtained here was used to test the Turelli-Orr model of Haldane's rule. Composite causes, especially, faster-male evolution and recessive hybrid incompatibilities, underlie Haldane's rule in heterogametic male taxa such as Drosophila (XY male and XX female). However, if faster-male evolution is driven by sexual selection, it contradicts Haldane's rule for sterility in heterogametic-female taxa such as Lepidoptera (ZW female and ZZ male). The hypothesis of a faster-heterogametic-sex evolution seems to fit the current data best. This hypothesis states that gametogenesis in the heterogametic sex, instead of in males per se, evolves much faster than in the homogametic sex, in part because of sex-ratio selection. This hypothesis not only explains Haldane's rule in a simple way, but also suggests that genomic conflicts play a major role in evolution and speciation.

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

“…simulans stocks w; e (kindly provided by J Coyne) and simB (w; nt; III) were described in Tao et al, (2003). In the simB stock, the third chromosome is isogenic to the third chromosome of the highly inbred stock 13w 1 X 1 JJ (constructed by sib-pair mating for 20 generations from 13w- Liu et al, 1996).…”

“…In the simB stock, the third chromosome is isogenic to the third chromosome of the highly inbred stock 13w 1 X 1 JJ (constructed by sib-pair mating for 20 generations from 13w- Liu et al, 1996). This chromosome does not carry a phenotypic marker, while the first and second chromosomes carry markers white (w) and net (nt), respectively (Tao et al, 2003). Drosophila mauritiana stocks (w; P [w+]) contain independent Pelement inserts on the third chromosome, which carry a functional copy of the gene white (True et al, 1996).…”

“…Drosophila mauritiana stocks (w; P [w+]) contain independent Pelement inserts on the third chromosome, which carry a functional copy of the gene white (True et al, 1996). Numerical identifiers of each of these stocks are according to Tao et al (2003). These stocks were used elsewhere for the construction of introgression lines that allowed the fine mapping of sex-ratio distorter and suppressor genes (Dox and Nmy- Tao et al, 2007a, b), as well as one candidate gene for hybrid male sterility (agt- Araripe et al, 2010).…”

“…Aided by molecular markers, these introgressed segments of D. mauritiana are well delimited (see Tao et al, 2001Tao et al, , 2003. We crossed seven pairs of introgression lines, each carrying a different segment of D. mauritiana's chromosome 3, in order to produce homozygotes of certain portions of these segments.…”

The role of spermatogonially expressed germ cell-specific genes in mammalian meiosis

“…Genetic studies in Drosophila demonstrated an excess of hybrid sterility loci on the X chromosome, a phenomenon referred to as Flarge X-effect_ (Orr & Coyne 1989, Tao et al 2003. Several X-linked hybrid sterility loci were also reported in mice (Oka et al 2004, Storchova et al 2004.…”