Y-chromosome effects onDrosophilageotaxis interact with genetic or cytoplasmic background

Stoltenberg, Scott F.; Hirsch, Jerry

doi:10.1006/anbe.1996.0351

Cited by 25 publications

(23 citation statements)

References 19 publications

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“…Finally, the Y-bybackground interaction effects on autosomal and Xlinked gene expression, as well as the existence of polymorphic variation between the two Y chromosomes in their effects on modulating genes proximal to the euchromatin-heterochromatin boundary in the X chromosome, were confirmed with a position-effect variegation assay. Y-linked genetic variation has been previously documented for sex ratio (Carvalho et al 1997;MontchampMoreau et al 2001), male courtship (Huttunen and Aspi 2003), geotaxis (Stoltenberg and Hirsch 1997), thermal sensitivity of spermatogenesis (Rohmer et al 2004), and fitness (Chippindale and Rice 2001). For many of these traits (male courtship, geotaxis, spermatogenesis, and fitness), significant Y-by-background interaction effects have also been detected.…”

Section: Discussionmentioning

confidence: 89%

YNot a Dead End: Epistatic Interactions BetweenY-Linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression inDrosophila melanogaster

2010

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The Y chromosome, inherited without meiotic recombination from father to son, carries relatively few genes in most species. This is consistent with predictions from evolutionary theory that nonrecombining chromosomes lack variation and degenerate rapidly. However, recent work has suggested a dynamic role for the Y chromosome in gene regulation, a finding with important implications for spermatogenesis and male fitness. We studied Y chromosomes from two populations of Drosophila melanogaster that had previously been shown to have major effects on the thermal tolerance of spermatogenesis. We show that these Y chromosomes differentially modify the expression of hundreds of autosomal and X-linked genes.Genes showing Y-linked regulatory variation (YRV) also show an association with immune response and pheromone detection. Indeed, genes located proximal to the euchromatin-heterochromatin boundary of the X chromosome appear particularly responsive to Y-linked variation, including a substantial number of odorant-binding genes. Furthermore, the data show significant regulatory interactions between the Y chromosome and the genetic background of autosomes and X chromosome. Altogether, our findings support the view that interpopulation, Y-linked regulatory polymorphisms can differentially modulate the expression of many genes important to male fitness, and they also point to complex interactions between the Y chromosome and genetic background affecting global gene expression.T HE Y chromosome is transmitted without sexual recombination from father to son. In the Y chromosome, as in other nonrecombining regions, complete linkage between genes results in the accumulation of deleterious alleles and the loss of genetic diversity due to the evolutionary processes of Muller's ratchet, background selection, and genetic hitchhiking (Bull 1983;Rice 1987;Charlesworth and Charlesworth 2000;Bachtrog et al. 2008). Consistent with theory, the Y chromosome of Drosophila melanogaster carries only 13 known protein-coding genes (Carvalho et al. 2001;Carvalho and Clark 2005;Koerich et al. 2008;Vibranovski et al. 2008;Krsticevic et al. 2010), whereas .5000 genes would be expected from typical gene densities in euchromatic regions.Six of the 13 genes discovered on the Y chromosome are male fertility factors that either encode structural components of spermatogenesis or regulate spermatogenesis-specific processes such as individualization (Carvalho et al. 2000(Carvalho et al. , 2009. Spermatogenesis in Drosophila males is extremely sensitive to heat, with males becoming sterile anywhere from 23°in heatsensitive species to 31°in heat-tolerant species (Chakir et al. 2002;David et al. 2005). In D. melanogaster, Rohmer et al. (2004) found that differences between Y chromosome lineages from tropical and temperate regions are responsible for much of the variation in thermal sensitivity of spermatogenesis. Since spermatogenesis is essential for male fitness, we expect a Y chromosome effect on thermal sensitivity to translate into effects on mal...

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Section: Discussionmentioning

confidence: 89%

YNot a Dead End: Epistatic Interactions BetweenY-Linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression inDrosophila melanogaster

2010

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“…Instead, most if not all of the~14 protein-coding genes present on the Y chromosomes of Drosophila melanogaster, D. simulans and other closely related species have male-specific functions and are exclusively expressed in the testis (Gepner and Hays, 1993;Carvalho et al, 2000;Carvalho et al, 2001;Vibranovski et al, 2008). Nevertheless, a suite of studies have shown that genetic variation present on the Y of Drosophila underlie phenotypic variation in male fitness (Chippindale and Rice, 2001;Yee et al, 2015), sex ratio distortion (Carvalho et al, 1997;Montchamp-Moreau et al, 2001;Branco et al, 2013a, b), tolerance to temperature extremes (Rohmer et al, 2004;David et al, 2005), behavior (Stoltenberg and Hirsch, 1997;Huttunen and Aspi, 2003), gene expression (Lemos et al, 2008;Sackton et al, 2011;Branco et al, 2013a, b) and chromatin states in somatic tissues .…”

Section: Introductionmentioning

confidence: 99%

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

Araripe

Tao

Lemos³

2016

Heredity

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Y chromosomes display population variation within and between species. Co-evolution within populations is expected to produce adaptive interactions between Y chromosomes and the rest of the genome. One consequence is that Y chromosomes from disparate populations could disrupt harmonious interactions between co-evolved genetic elements and result in reduced male fertility, sterility or inviability. Here we address the contribution of 'heterospecific Y chromosomes' to fertility in hybrid males carrying a homozygous region of Drosophila mauritiana introgressed in the Drosophila simulans background. In order to detect Y chromosome-autosome interactions, which may go unnoticed in a single-species background of autosomes, we constructed hybrid genotypes involving three sister species: Drosophila simulans, D. mauritiana, and D. sechellia. These engineered strains varied due to: (i) species origin of the Y chromosome (D. simulans or D. sechellia); (ii) location of the introgressed D. mauritiana segment on the D. simulans third chromosome, and (iii) grandparental genomic background (three genotypes of D. simulans). We find complex interactions between the species origin of the Y chromosome, the identity of the D. mauritiana segment and the grandparental genetic background donating the chromosomes. Unexpectedly, the interaction of the Y chromosome and one segment of D. mauritiana drastically reduced fertility in the presence of Ysim, whereas the fertility is partially rescued by the Y chromosome of D. sechellia when it descends from a specific grandparental genotype. The restoration of fertility occurs in spite of an autosomal and X-linked genome that is mostly of D. simulans origin. These results illustrate the multifactorial basis of genetic interactions involving the Y chromosome. Our study supports the hypothesis that the Y chromosome can contribute significantly to the evolution of reproductive isolation and highlights the conditional manifestation of infertility in specific genotypic combinations.

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“…The Y chromosome has been shown to regulate organismal traits, such as male fertility (Chippindale and Rice, 2001), sex ratio distortion (Carvalho et al, 1997;Montchamp-Moreau et al, 2001), thermal adaptation (Rohmer et al, 2004) and behaviors (Stoltenberg and Hirsch, 1997;Huttunen and Aspi, 2003). The regulatory bases for these phenotypes have been suggested by genome-wide gene expression studies in D. melanogaster (Lemos et al, 2008Jiang et al, 2010;Paredes et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

Branco¹,

Tao

Hartl

et al. 2013

Heredity

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X-linked sex-ratio distorters that disrupt spermatogenesis can cause a deficiency in functional Y-bearing sperm and a femalebiased sex ratio. Y-linked modifiers that restore a normal sex ratio might be abundant and favored when a X-linked distorter is present. Here we investigated natural variation of Y-linked suppressors of sex-ratio in the Winters systems and the ability of these chromosomes to modulate gene expression in Drosophila simulans. Seventy-eight Y chromosomes of worldwide origin were assayed for their resistance to the X-linked sex-ratio distorter gene Dox. Y chromosome diversity caused males to sire B63% to B98% female progeny. Genome-wide gene expression analysis revealed hundreds of genes differentially expressed between isogenic males with sensitive (high sex ratio) and resistant (low sex ratio) Y chromosomes from the same population. Although the expression of about 75% of all testis-specific genes remained unchanged across Y chromosomes, a subset of post-meiotic genes was upregulated by resistant Y chromosomes. Conversely, a set of accessory gland-specific genes and mitochondrial genes were downregulated in males with resistant Y chromosomes. The D. simulans Y chromosome also modulated gene expression in XXY females in which the Y-linked protein-coding genes are not transcribed. The data suggest that the Y chromosome might exert its regulatory functions through epigenetic mechanisms that do not require the expression of protein-coding genes. The gene network that modulates sex ratio distortion by the Y chromosome is poorly understood, other than that it might include interactions with mitochondria and enriched for genes expressed in post-meiotic stages of spermatogenesis.

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Y-chromosome effects onDrosophilageotaxis interact with genetic or cytoplasmic background

Cited by 25 publications

References 19 publications

YNot a Dead End: Epistatic Interactions BetweenY-Linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression inDrosophila melanogaster

YNot a Dead End: Epistatic Interactions BetweenY-Linked Regulatory Polymorphisms and Genetic Background Affect Global Gene Expression inDrosophila melanogaster

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

Natural variation of the Y chromosome suppresses sex ratio distortion and modulates testis-specific gene expression in Drosophila simulans

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