Abstract
Speciation often involves the evolution of incompatible gene interactions that cause sterility or lethality in hybrids between populations. These so-called hybrid incompatibilities occur between two or more functionally divergent loci. We show that the nucleoporin 160kDa (Nup160) gene of the fruitfly Drosophila simulans is incompatible with one or more factors on the D. melanogaster X chromosome, causing hybrid lethality. Nup160 encodes a nuclear pore complex protein and shows evidence of adaptive evolution. Furthermore, the protein encoded by Nup160 directly interacts with that of another hybrid lethality gene, Nup96, indicating that at least two lethal hybrid incompatibility genes have evolved as byproducts of divergent coevolution among interacting components of the Drosophila nuclear pore complex.
MeSH Terms
Animals
Chromosome Mapping
Crosses, Genetic
Drosophila/genetics,physiology
Drosophila Proteins/genetics,metabolism
Drosophila melanogaster/genetics,physiology
Evolution, Molecular
Female
Genes, Insect
Genetic Speciation
Hybridization, Genetic
Male
Molecular Sequence Data
Mutation
Nuclear Pore Complex Proteins/genetics,metabolism
Selection, Genetic
X Chromosome/genetics
Chemicals
Drosophila Proteins
Nuclear Pore Complex Proteins
nuclear pore complex protein 96
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Tang Shanwu
Department of Biology, University of Rochester, Rochester, NY 14627, USA.
Presgraves Daven C
References (31)
31 references, click to expand
-
The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions.
EMBO J. 2007 Apr 4;26(7):1853-64
PMID: 17363900
-
Adaptive protein evolution at the Adh locus in Drosophila.
Nature. 1991 Jun 20;351(6328):652-4
PMID: 1904993
-
The dominance theory of Haldane's rule.
Genetics. 1995 May;140(1):389-402
PMID: 7635302
-
Distinctly different sex ratios in African and European populations of Drosophila melanogaster inferred from chromosomewide single nucleotide polymorphism data.
Genetics. 2007 Sep;177(1):469-80
PMID: 17660560
-
A rapidly evolving MYB-related protein causes species isolation in Drosophila.
Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5302-7
PMID: 12695567
-
Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export.
J Cell Biol. 2001 Oct 29;155(3):339-54
PMID: 11684705
-
Nup96-dependent hybrid lethality occurs in a subset of species from the simulans clade of Drosophila.
Genetics. 2007 May;176(1):543-52
PMID: 17409061
-
A fine-scale genetic analysis of hybrid incompatibilities in Drosophila.
Genetics. 2003 Mar;163(3):955-72
PMID: 12663535
-
Hitchhiking under positive Darwinian selection.
Genetics. 2000 Jul;155(3):1405-13
PMID: 10880498
-
Pervasive and largely lineage-specific adaptive protein evolution in the dosage compensation complex of Drosophila melanogaster.
Genetics. 2007 Nov;177(3):1959-62
PMID: 18039888
-
Gene transposition as a cause of hybrid sterility in Drosophila.
Science. 2006 Sep 8;313(5792):1448-50
PMID: 16960009
-
Peering through the pore: nuclear pore complex structure, assembly, and function.
Dev Cell. 2003 Jun;4(6):775-89
PMID: 12791264
-
Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila.
Science. 2006 Nov 24;314(5803):1292-5
PMID: 17124320
-
The population genetics of speciation: the evolution of hybrid incompatibilities.
Genetics. 1995 Apr;139(4):1805-13
PMID: 7789779
-
Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus.
Nature. 1989 Oct 5;341(6241):415-21
PMID: 2797166
-
A rapidly evolving homeobox at the site of a hybrid sterility gene.
Science. 1998 Nov 20;282(5393):1501-4
PMID: 9822383
-
Sex chromosomes and speciation in Drosophila.
Trends Genet. 2008 Jul;24(7):336-43
PMID: 18514967
-
A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac.
Nat Genet. 2004 Mar;36(3):283-7
PMID: 14981521
-
Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila.
Nature. 2003 Jun 12;423(6941):715-9
PMID: 12802326
-
PATTERNS OF SPECIATION IN DROSOPHILA.
Evolution. 1989 Mar;43(2):362-381
PMID: 28568554
-
Species-specific positive selection of the male-specific lethal complex that participates in dosage compensation in Drosophila.
Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15412-7
PMID: 17878295
-
Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans.
Mol Biol Evol. 2001 Mar;18(3):279-90
PMID: 11230529
-
Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila.
Mol Cell. 2006 Mar 17;21(6):811-23
PMID: 16543150
-
The two tempos of nuclear pore complex evolution: highly adapting proteins in an ancient frozen structure.
Genome Biol. 2005;6(10):R85
PMID: 16207356
-
Nucleoporin levels regulate cell cycle progression and phase-specific gene expression.
Dev Cell. 2008 Nov;15(5):657-67
PMID: 19000832
-
Does genetic conflict drive rapid molecular evolution of nuclear transport genes in Drosophila?
Bioessays. 2007 Apr;29(4):386-91
PMID: 17373698
-
The "hitchhiking effect" revisited.
Genetics. 1989 Dec;123(4):887-99
PMID: 2612899
-
Positive selection at the binding sites of the male-specific lethal complex involved in dosage compensation in Drosophila.
Genetics. 2008 Oct;180(2):1123-9
PMID: 18780755
-
The hitch-hiking effect of a favourable gene.
Genet Res. 1974 Feb;23(1):23-35
PMID: 4407212
-
Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96.
Mol Biol Evol. 2007 Jan;24(1):306-14
PMID: 17056646
-
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
Genetics. 1989 Nov;123(3):585-95
PMID: 2513255