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 À 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.

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

“…While the NUP96 protein is highly conserved between D. simulans and D. mauritiana, the D. mauritiana allele of Nup96 has no hybrid-lethal effect, which suggests more complex genetic interactions leading to Nup96-dependent incompatibility (Barbash 2007).…”

Lineage-Specific Evolution of the Complex Nup160 Hybrid Incompatibility Between Drosophila melanogaster and Its Sister Species

“…In contrast, Nup160 2 /mau hybrid females and Nup160 2 /mau hybrid males show no reduced viability relative to control CyO/mau siblings (Table 1). Interestingly, the effects of Nup160-lethal in X mel Y sim and X mel Y sech hybrids but not in X mel Y mau hybrids-parallels that observed for Nup96 (Barbash 2007). These results together raised the possibility that the Nup160 and Nup96 hybrid incompatibilities may not be genetically independent.…”

“…Nup96 sim and Nup96 sech cause hybrid lethality when combined with hemizygous (or homozygous) X mel , but Nup96 mau does not Barbash 2007). However, the fact that Nup96 in D. simulans has experienced no nonsynonymous substitutions since its split from D. mauritiana implies that Nup96 sim and Nup96 mau are functionally equivalent .…”

“…However, the fact that Nup96 in D. simulans has experienced no nonsynonymous substitutions since its split from D. mauritiana implies that Nup96 sim and Nup96 mau are functionally equivalent . Therefore, at least one additional unknown autosomal factor must be present in D. simulans that is absent in D. mauritiana (Barbash 2007). These considerations suggest that some components of the Nup96 hybrid incompatibility also evolved after the split of the D. simulans clade species.…”

“…We find that Nup160-mediated lethality occurs in hybrids from crosses of D. melanogaster with D. simulans and D. sechellia but not D. mauritiana. Interestingly, the same holds for Nup96 (Barbash 2007). Second, we test whether D. simulans and D. mauritiana have functionally diverged at Nup160 and/or at a different, genetically unlinked autosomal locus required to kill D. melanogaster hybrids.…”