Abstract
Hybrid incompatibilities (HIs) cause reproductive isolation between species and thus contribute to speciation. Several HI genes encode adaptively evolving proteins that localize to or interact with heterochromatin, suggesting that HIs may result from co-evolution with rapidly evolving heterochromatic DNA. Little is known, however, about the intraspecific function of these HI genes, the specific sequences they interact with, or the evolutionary forces that drive their divergence. The genes Hmr and Lhr genetically interact to cause hybrid lethality between Drosophila melanogaster and D. simulans, yet mutations in both genes are viable. Here, we report that Hmr and Lhr encode proteins that form a heterochromatic complex with Heterochromatin Protein 1 (HP1a). Using RNA-Seq analyses we discovered that Hmr and Lhr are required to repress transcripts from satellite DNAs and many families of transposable elements (TEs). By comparing Hmr and Lhr function between D. melanogaster and D. simulans we identify several satellite DNAs and TEs that are differentially regulated between the species. Hmr and Lhr mutations also cause massive overexpression of telomeric TEs and significant telomere lengthening. Hmr and Lhr therefore regulate three types of heterochromatic sequences that are responsible for the significant differences in genome size and structure between D. melanogaster and D. simulans and have high potential to cause genetic conflicts with host fitness. We further find that many TEs are overexpressed in hybrids but that those specifically mis-expressed in lethal hybrids do not closely correlate with Hmr function. Our results therefore argue that adaptive divergence of heterochromatin proteins in response to repetitive DNAs is an important underlying force driving the evolution of hybrid incompatibility genes, but that hybrid lethality likely results from novel epistatic genetic interactions that are distinct to the hybrid background.
Highlights
IntroductionTheir ability to reproduce with each other diminishes. Hybrid incompatibility (HI), the reduced viability and fertility of interspecific hybrids, is a major cause of reproductive isolation between nascent species and an important contributor to speciation
As populations diverge, their ability to reproduce with each other diminishes
It has been hypothesized that rapid changes in heterochromatic DNA drives the changes in these Hybrid incompatibilities (HIs) genes and the evolution of reproductive isolation
Summary
Their ability to reproduce with each other diminishes. Hybrid incompatibility (HI), the reduced viability and fertility of interspecific hybrids, is a major cause of reproductive isolation between nascent species and an important contributor to speciation. Many of the genes causing HI show evidence of adaptive evolution, typically manifest as excessive numbers of amino-acid-changing mutations compared to neutral expectations [1,2]. These data do not, imply that natural selection acts directly on HI phenotypes. Two or more loci diverge independently in two nascent species. If these species later interbreed, these diverged genes may interact to cause deleterious HI phenotypes. The key insight of the D-M model is that hybrid lethality and sterility evolve as byproducts of intraspecific divergence [1]
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