Nup96-dependent hybrid lethality occurs in a subset of species from the simulans clade of Drosophila

Abstract

The cross of Drosophila melanogaster females to D. simulans males typically produces lethal F(1) hybrid males. F(1) male lethality is suppressed when the D. simulans Lhr(1) hybrid rescue strain is used. Viability of these F(1) males carrying Lhr(1) is in turn substantially reduced when the hybrids are heterozygous for some mutant alleles of the D. melanogaster Nup96 gene. I show here that similar patterns of Nup96-dependent lethality occur when other hybrid rescue mutations are used to create F(1) males, demonstrating that Nup96 does not reduce hybrid viability by suppressing the Lhr(1) rescue effect. The penetrance of this Nup96-dependent lethality does not correlate with the penetrance of the F(1) hybrid rescue, arguing that these two phenomena reflect genetically independent processes. D. simulans, together with two additional sister species, forms a clade that speciated after the divergence of their common ancestor from D. melanogaster. I report here that Nup96(-) reduces F(1) viability in D. melanogaster hybrids with one of these sister species, D. sechellia, but not with the other, D. mauritiana. These results suggest that Nup96-dependent lethality evolved after the speciation of D. melanogaster from the common ancestor of the simulans clade and is caused by an interaction among Nup96, unknown gene(s) on the D. melanogaster X chromosome, and unknown autosomal gene(s), at least some of which have diverged in D. simulans and D. sechellia but not in D. mauritiana. The genetic properties of Nup96 are also discussed relative to other hybrid lethal genes.

Figure 1.—

Viability effects tested in this study. Only the sex and third chromosomal genotypes are shown. “Rescue” represents either the In(1)AB or the Df(1)Hmr⁻ hybrid rescue mutation. FM6/Y hybrid sons are lethal since they do not carry a rescue mutation. Four surviving genotypes can be compared for viability with and without the Nup96⁻ mutation. (A) Comparison of F₁ hybrid females that have high viability due to the rescue mutation to confirm that Nup96⁻ does not cause lethality in females. (B) Comparison of F₁ hybrid females that have low viability due to the presence of D. melanogaster Hmr⁺ (Barbash et al. 2000). This genotype provides a more sensitive assay for possible effects of Nup96⁻ in female hybrids than the genotype in A. (C) Comparison of F₁ hybrid males carrying the D. melanogaster X chromosome to test whether Nup96-dependent lethality occurs with hybrid rescue mutations other than Lhr¹. (D) Comparison of F₁ hybrid males carrying the sibling-species X chromosome to confirm that lethality occurs only with the D. melanogaster X. This class of exceptional males is generated by nondisjunction in the female parents and was observed at high rates, presumably due to the presence of two balancer chromosomes. “Rescue”/FM6/Y hybrid females would also be produced by nondisjunction and were previously shown to be semiviable (Barbash et al. 2000). Such females would be distinguishable from FM6/X⁺ regular females by visible markers in crosses with Df(1)Hmr⁻ in Table 2; however, no such females were observed in this study.

Figure 2.—

Three evolutionary events leading to Nup96-dependent hybrid lethality. (1) Lethality requires X-linked gene(s) that have diverged on the D. melanogaster lineage because lethality occurs in hybrids with the D. melanogaster but not with the D. simulans or D. sechellia X chromosome (Presgraves et al. 2003; this study). (2) The divergence of Nup96 is inferred to have occurred before the divergence of D. simulans and D. mauritiana because all replacement substitutions in D. simulans are also found in D. mauritiana (Presgraves et al. 2003). (3) Results presented in this study suggest that additional genetic changes must have evolved to cause lethality only in D. melanogaster/D. simulans and D. melanogaster/D. sechellia hybrids but not in D. melanogaster/D. mauritiana hybrids.