A Test of Double Interspecific Introgression of Nucleoporin Genes in Drosophila

Abstract

In interspecific hybrids between Drosophila melanogaster and Drosophila simulans, the D. simulans nucleoporin-encoding Nup96sim and Nup160sim can cause recessive lethality if the hybrid does not also inherit the D. simulans X chromosome. In addition, Nup160sim leads to recessive female sterility in the D. melanogaster genetic background. Here, we conducted carefully controlled crosses to better understandthe relationship between Nup96sim and Nup160sim. Nup96sim did not lead to female sterility in the D. melanogaster genetic background, and double introgression of Nup96sim and Nup160sim did not generally lead to lethality when one was heterozygous and the other homozygous (hemizygous). It appears that introgression of additional autosomal D. simulans genes is necessary to cause lethality and that the effect of the introgression is dominant to D. melanogaster alleles. Interestingly, the genetic background affected dominance of Nup96sim, and double introgression carrying homozygous Nup96sim and hemizygous Nup160sim resulted in lethality. Thus, Nup96sim and Nup160sim seem to be two components of the same incompatibility.

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

“…First, the lethality of our double-mutant hybrid males shows that Nup160 sim does not require the presence of Nup96 mel , nor does Nup96 sim require the presence of Nup160 mel (Table 3). (Sawamura et al 2014). The latter findings would seem to rule out the possibility that Nup96 sim is the dominant autosomal factor required for Nup160-mediated hybrid lethality (and vice versa).…”

“…The latter findings would seem to rule out the possibility that Nup96 sim is the dominant autosomal factor required for Nup160-mediated hybrid lethality (and vice versa). It is possible that a different autosome-encoded NPC protein, perhaps one of the other NUP107 subcomplex proteins or its interactors, is required for Nup160-and Nup96-mediated hybrid lethality (see also Sawamura et al 2014). Previous population genetics analyses showed that Nup160 experienced parallel bouts of recurrent adaptive protein evolution in D. melanogaster and, separately, in D. simulans (Tang and Presgraves 2009) (Table 5).…”

“…Lineage-specific Nup160-mediated hybrid lethality depends on Nup160 and autosomal background Previous work established that the Nup160 hybrid incompatibility is complex, requiring (1) hemizygosity (or homozygosity) for X mel , (2) hemizygosity (or homozygosity) for Nup160 sim , and (3) at least one unknown dominant factor in the D. simulans autosomes (Sawamura et al , 2010(Sawamura et al , 2014. Our finding that Nup160-mediated lethality occurs in D. simulans-D. melanogaster hybrid males but not in D. mauritiana-D. melanogaster hybrid males therefore raises two nonexclusive possibilities: D. simulans and D. mauritiana are functionally differentiated at Nup160 and/or at some other autosomal factor(s) essential for hybrid lethality.…”

Genetic Analyses ofElysMutations inDrosophilaShow Maternal-Effect Lethality and Interactions withNucleoporinGenes

“…Nup96 and Nup160 are also involved in reproductive isolation ( Presgraves et al 2003 ; Tang and Presgraves 2009 ; Sawamura et al 2010 ). Nup96 sim and Nup160 sim synergistically cause hybrid incompatibility ( Sawamura et al 2014 ), but the D. melanogaster alleles of Nup160 and Nup96 are not the dominant autosomal incompatibility partner of Nup96 sim and Nup160 sim , respectively ( Tang and Presgraves 2015 ). Then, what is (are) the incompatibility partner(s) of Nup96 sim and Nup160 sim ?…”

“…Thus, hemizygous Nup160 sim introgression causes female sterility (maternal-effect lethality) with a phenotype that is similar to the Elys mutations of D. melanogaster ( Figure 2 ). But Nup96 sim introgression does not cause female sterility ( Sawamura et al 2014 ) and Nup37 sim has not been tested.…”