Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes

Sawamura, Kyoichi; Yamamoto, Masatoshi

doi:10.1038/sj.hdy.6881800

Cited by 19 publications

(22 citation statements)

References 7 publications

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“…We can, however, exclude the possibility that Zhr, hlx, and hhl are involved in the same incompatibility, as Zhr mel is incompatible with a maternal factor(s) from D. simulans (Sawamura et al 1993;Carracedo et al 2000;Gérard and Presgraves 2012); hlx mau is incompatible with a recessive, autosomal Su(hlx) from both D. simulans and D. sechellia (Cattani and Presgraves 2009); and hhl mau is incompatible with a dominant, X-linked factor from D. melanogaster. The Table 4 mapping of Zhr, hlx, and now hhl to the heterochromatin is consistent with an emerging theme that Drosophila hybrid incompatibilities often involve functional divergence of heterochromatin (Sawamura et al 1995;Sawamura and Yamamoto 1997;Ferree and Barbash 2009) and genes whose products interact with heterochromatin (Barbash et al 2003;Brideau et al 2006;Bayes and Malik 2009). Pericentric heterochromatin is involved in functions such as meiotic and mitotic chromosome segregation (Karpen et al 1996) and the transcriptional regulation of flanking sequences like rDNA loci (Hilliker and Appels 1982;Karpen et al 1988).…”

Section: Location Of Hhlmentioning

confidence: 59%

“…The existence of hybrid lethal factors at the heterochromatic base of the X chromosome is consistent with an emerging theme in which hybrid incompatibilities in Drosophila involve heterochromatin (e.g., Zhr) (Sawamura and Yamamoto 1997;Ferree and Barbash 2009) or genes whose products interact with heterochromatin (e.g., Hmr, Lhr; Brideau et al 2006 and OdsH;Bayes and Malik 2009). Loci involved in hybrid incompatibilities map to the pericentromeric heterochromatin of the X chromosome between other species pairs as well (Moehring et al 2006;Cattani and Presgraves 2009).…”

mentioning

confidence: 67%

“…simulans hybrid genetic background, and the strength of the lethality depends on both temperature and genetic background. This is not the first hybrid lethality factor mapped to the pericentromeric heterochromatin of the X chromosome: Zhr from D. melanogaster (Sawamura et al 1995;Sawamura and Yamamoto 1997); a factor from D. santomea (Matute et al 2010); and hlx from D. mauritiana (Cattani and Presgraves 2009) all localize to this region.…”

Section: Location Of Hhlmentioning

confidence: 99%

“…In the reciprocal cross between D. simulans females and D. melanogaster males, hybrid males are produced while females usually die as embryos (Sturtevant 1920(Sturtevant , 1921Hadorn 1961). These normally lethal hybrid females are rescued by the D. simulans mutant allele of maternal hybrid rescue (mhr) (Sawamura et al 1993; see also Orr 1996;Carracedo et al 2000;Gérard and Presgraves 2012) or by the D. melanogaster mutant allele of Zygotic hybrid rescue, Zhr (Sawamura and Yamamoto 1997). The incompatible wild-type allele of Zhr is thought to correspond to a large block of 359-bp repetitive satellite DNA from D. melanogaster, and F 1 hybrid females die as a consequence of widespread mitotic defects (Ferree and Barbash 2009).…”

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confidence: 99%

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Incompatibility Between X Chromosome Factor and Pericentric Heterochromatic Region Causes Lethality in Hybrids Between Drosophila melanogaster and Its Sibling Species

Cattani

Presgraves

2012

Genetics

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The Dobzhansky-Muller model posits that postzygotic reproductive isolation results from the evolution of incompatible epistatic interactions between species: alleles that function in the genetic background of one species can cause sterility or lethality in the genetic background of another species. Progress in identifying and characterizing factors involved in postzygotic isolation in Drosophila has remained slow, mainly because Drosophila melanogaster, with all of its genetic tools, forms dead or sterile hybrids when crossed to its sister species, D. simulans, D. sechellia, and D. mauritiana. To circumvent this problem, we used chromosome deletions and duplications from D. melanogaster to map two hybrid incompatibility loci in F 1 hybrids with its sister species. We mapped a recessive factor to the pericentromeric heterochromatin of the X chromosome in D. simulans and D. mauritiana, which we call heterochromatin hybrid lethal (hhl), which causes lethality in F 1 hybrid females with D. melanogaster. As F 1 hybrid males hemizygous for a D. mauritiana (or D. simulans) X chromosome are viable, the lethality of deficiency hybrid females implies that a dominant incompatible partner locus exists on the D. melanogaster X. Using small segments of the D. melanogaster X chromosome duplicated onto the Y chromosome, we mapped a dominant factor that causes hybrid lethality to a small 24-gene region of the D. melanogaster X. We provide evidence suggesting that it interacts with hhl mau . The location of hhl is consistent with the emerging theme that hybrid incompatibilities in Drosophila involve heterochromatic regions and factors that interact with the heterochromatin. M ORE than 70 years ago, Dobzhansky (1937) and Muller (1942) proposed a simple two-locus model in which postzygotic isolation arises as a byproduct of divergence between effectively allopatric populations. Genes that function well in one species' genetic background might not be functional in a hybrid genetic background, rendering hybrids dead or sterile. Despite early acceptance of the Dobzhansky-Muller model, progress in identifying and characterizing factors involved in hybrid incompatibilities has remained slow. One of the reasons for the slow progress is that Drosophila melanogaster, with its many genetic tools, forms largely dead or sterile hybrids when crossed to its sister species D. simulans, D. sechellia, and D. mauritiana (Sturtevant 1920(Sturtevant , 1929Lachaise et al. 1986;Provine 1991;Barbash 2010).In general, three methods have been used to circumvent this problem. First, alleles that suppress postzygotic isolation, so-called hybrid rescue mutations, have been used to characterize hybrid inviability between D. melanogaster and its three sister species in the D. simulans complex. When D. melanogaster females are crossed to sibling species males, only hybrid females are produced while males die as larvae (Sturtevant 1920;Lachaise et al. 1986). These males are rescued by the D. melanogaster mutant allele of Hybrid male rescue (Hmr) (Hutter...

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Section: Location Of Hhlmentioning

confidence: 59%

mentioning

confidence: 67%

Section: Location Of Hhlmentioning

confidence: 99%

mentioning

confidence: 99%

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Incompatibility Between X Chromosome Factor and Pericentric Heterochromatic Region Causes Lethality in Hybrids Between Drosophila melanogaster and Its Sibling Species

Cattani

Presgraves

2012

Genetics

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“…Genetic dissection of reproductive barriers between nascent species is a powerful approach for revealing the causes of speciation. This strategy has been highly successful, particularly in Drosophila, where nine specific genes that cause reduced fitness in hybrids have been identified (Sawamura and Yamamoto 1997;Ting et al 1998;Barbash et al 2003;Presgraves et al 2003;Brideau et al 2006;Bayes and Malik 2009;Ferree and Barbash 2009;Phadnis and Orr 2009;Tang and Presgraves 2009). Despite this progress, several factors motivate additional genetic studies of postzygotic isolation.…”

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confidence: 99%

Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

et al. 2011

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Reproductive isolation between species is often caused by deleterious interactions among loci in hybrids. Finding the genes involved in these incompatibilities provides insight into the mechanisms of speciation. With recently diverged subspecies, house mice provide a powerful system for understanding the genetics of reproductive isolation early in the speciation process. Although previous studies have yielded important clues about the genetics of hybrid male sterility in house mice, they have been restricted to F 1 sterility or incompatibilities involving the X chromosome. To provide a more complete characterization of this key reproductive barrier, we conducted an F 2 intercross between wild-derived inbred strains from two subspecies of house mice, Mus musculus musculus and Mus musculus domesticus. We identified a suite of autosomal and X-linked QTL that underlie measures of hybrid male sterility, including testis weight, sperm density, and sperm morphology. In many cases, the autosomal loci were unique to a specific sterility trait and exhibited an effect only when homozygous, underscoring the importance of examining reproductive barriers beyond the F 1 generation. We also found novel two-locus incompatibilities between the M. m. musculus X chromosome and M. m. domesticus autosomal alleles. Our results reveal a complex genetic architecture for hybrid male sterility and suggest a prominent role for reproductive barriers in advanced generations in maintaining subspecies integrity in house mice.

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Speciation by postzygotic isolation: forces, genes and molecules

2000

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New species arise as reproductive isolation evolves between diverging populations. Here we review recent work in the genetics of postzygotic reproductive isolation—the sterility and inviability of species hybrids. Over the last few years, research has taken two new directions. First, we have begun to learn a good deal about the population genetic forces driving the evolution of postzygotic isolation. It has, for instance, become increasingly clear that conflict‐driven processes, like sexual selection and meiotic drive, may contribute to the evolution of hybrid sterility. Second, we have begun to learn something about the identity and molecular characteristics of the actual genes causing hybrid problems. Although molecular genetic data are limited, early findings suggest that “speciation genes” correspond to loci having normal functions within species and that these loci sometimes diverge as a consequence of evolution in gene regulation. BioEssays 22:1085–1094, 2000. © 2000 John Wiley & Sons, Inc.

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Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes

Cited by 19 publications

References 7 publications

Incompatibility Between X Chromosome Factor and Pericentric Heterochromatic Region Causes Lethality in Hybrids Between Drosophila melanogaster and Its Sibling Species

Incompatibility Between X Chromosome Factor and Pericentric Heterochromatic Region Causes Lethality in Hybrids Between Drosophila melanogaster and Its Sibling Species

Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

Speciation by postzygotic isolation: forces, genes and molecules

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