Neighboring genes for DNA-binding proteins rescue male sterility in Drosophila hybrids

Abstract

Crosses between closely related animal species often result in male hybrids that are sterile, and the molecular and functional basis of genetic factors for hybrid male sterility is of great interest. Here, we report a molecular and functional analysis of HMS1, a region of 9.2 kb in chromosome 3 of Drosophila mauritiana, which results in virtually complete hybrid male sterility when homozygous in the genetic background of sibling species Drosophila simulans. The HMS1 region contains two strong candidate genes for the genetic incompatibility, agt and Taf1. Both encode unrelated DNA-binding proteins, agt for an alkyl-cysteine-S-alkyltransferase and Taf1 for a subunit of transcription factor TFIID that serves as a multifunctional transcriptional regulator. The contribution of each gene to hybrid male sterility was assessed by means of germ-line transformation, with constructs containing complete agt and Taf1 genomic sequences as well as various chimeric constructs. Both agt and Taf1 contribute about equally to HMS1 hybrid male sterility. Transgenes containing either locus rescue sterility in about one-half of the males, and among fertile males the number of offspring is in the normal range. This finding suggests compensatory proliferation of the rescued, nondysfunctional germ cells. Results with chimeric transgenes imply that the hybrid incompatibilities result from interactions among nucleotide differences residing along both agt and Taf1. Our results challenge a number of preliminary generalizations about the molecular and functional basis of hybrid male sterility, and strongly reinforce the role of DNA-binding proteins as a class of genes contributing to the maintenance of postzygotic reproductive isolation.postzygotic reproductive isolation | hybrid male sterility | gene conflict | transcription factor

Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species

“…Under this model, the genotypes at particular loci matters, as two (or more) weak alleles interact to produce an HMS effect greater than the sum of their individual effects (Cabot et al, 1994;Wu, 1995, Davis andWu and Hollocher, 1998). Lienard et al, 2016). (A) The plot shows the distribution of a hypothetical quantitative trait, fertility potential, for five hypothetical introgression genotypes shown beneath the x-axis.…”

“… Polygenic threshold model of HMS (adapted from Lienard et al, 2016 ). (A) The plot shows the distribution of a hypothetical quantitative trait, fertility potential, for five hypothetical introgression genotypes shown beneath the x -axis.…”

The chromosomal basis of species initiation:Prdm9as an anti-speciation gene

“…There is now diminishing support for the view that adverse genic interactions (epistasis), referred to as Dobzhansky-Muller incompatibilities, are as fundamental to speciation as meiotic chromosomal mismatches [12,53]. Interactions between fruit fly examples likely evolved late in the speciation process [9,54].…”

Speciation genes are more likely to have discordant gene trees

“…A growing number of so-called ‘speciation genes’ that isolate species in accordance with the DM model have emerged from the genetic analysis of reproductive isolation in hybrids (e.g. Ting et al 1998; Barbash et al 2003; Presgraves et al 2003; Bomblies et al 2007; Mihola et al 2009; Phadnis and Orr 2009; Barr and Fishman 2010; Lienard et al 2016). Combinations of alleles from different species at these genes cause hybrid infertility or inviability.…”