Altered Localization of Hybrid Incompatibility Proteins in Drosophila.

Jacob Carter Cooper,Axel Imhof,Andrea Lukacs,Tamas Schauer,Shelley Reich,Nitin Phadnis,Amanda Marie Larracuente

doi:10.1093/molbev/msz105

Jacob Carter Cooper, Axel Imhof + Show 5 more

Open Access

https://doi.org/10.1093/molbev/msz105

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Abstract

Understanding the molecular basis of hybrid incompatibilities is a fundamental pursuit in evolutionary genetics. In crosses between Drosophila melanogaster females and Drosophila simulans males, an interaction between at least three genes is necessary for hybrid male lethality: Hmr mel, Lhr sim, and gfzf sim. Although HMR and LHR physically bind each other and function together in a single complex, the connection between gfzf and either of these proteins remains mysterious. Here, we show that GFZF localizes to many regions of the genome in both D. melanogaster and D. simulans, including at telomeric retrotransposon repeats. We find that GFZF localization at telomeres is significantly different between these two species, reflecting the rapid evolution of telomeric retrotransposon copy number composition between the two species. Next, we show that GFZF and HMR normally do not colocalize in D. melanogaster. In interspecies hybrids, however, HMR shows extensive mis-localization to GFZF sites, thus uncovering a new molecular interaction between these hybrid incompatibility factors. We find that spreading of HMR to GFZF sites requires gfzf sim but not Lhr sim, suggesting distinct roles for these factors in the hybrid incompatibility. Finally, we find that overexpression of HMR and LHR within species is sufficient to mis-localize HMR to GFZF binding sites, indicating that HMR has a natural low affinity for GFZF sites. Together, these studies provide the first insights into the different properties of gfzf between D. melanogaster and D. simulans, and uncover a molecular interaction between gfzf and Hmr in the form of altered protein localization.

Highlights

The formation of new species from a single ancestral population involves the evolution of reproductive isolating barriers (Dobzhansky 1937; Coyne and Orr 2004)
Different Localization Patterns of GFZF at D. melanogaster and D. simulans Telomeres Though gfzf is a chromatin associated factor that has many binding sites in the genome (Baumann et al 2018), it is not clear if this property is consistent between D. melanogaster and D. simulans
We performed immunostaining for natively expressed GFZF across multiple tissues, and found that it consistently localizes to the nucleus in D. melanogaster and D. simulans

Summary

Introduction

The formation of new species from a single ancestral population involves the evolution of reproductive isolating barriers (Dobzhansky 1937; Coyne and Orr 2004). Intrinsic postzygotic reproductive barriers, such as the sterility or inviability of hybrids, are caused by deleterious genetic interactions known as hybrid incompatibilities. When D. melanogaster females are crossed to D. simulans males, the hybrid F1 males die during larval development (Sturtevant 1919). These F1 hybrid males lack imaginal disc tissues, and do not undergo sufficient growth to trigger pupation; hybrid F1 females live to adulthood but are sterile (Sanchez and Dubendorfer 1983). These three alleles interact genetically to form a single hybrid incompatibility, and all three incompatible alleles must be simultaneously present for hybrid F1 male lethality. The D. melanogaster–D. simulans hybridization represents one of the best understood systems in terms of the identities of the genes involved in hybrid lethality (Barbash 2010)

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