Polymorphic Y Chromosomes Harbor Cryptic Variation with Manifold Functional Consequences

Abstract

The paucity of polymorphisms in single-copy genes on the Y chromosome of Drosophila contrasts with data indicating that this chromosome has polymorphic phenotypic effects on sex ratio, temperature sensitivity, behavior, and fitness. We show that the Y chromosome of D. melanogaster harbors substantial genetic diversity in the form of polymorphisms for genetic elements that differentially affect the expression of hundreds of X-linked and autosomal genes. The affected genes are more highly expressed in males, more meagerly expressed in females, and more highly divergent between species. Functionally, they affect microtubule stability, lipid and mitochondrial metabolism, and the thermal sensitivity of spermatogenesis. Our findings provide a mechanism for adaptive phenotypic variation associated with the Y chromosome.

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

“…Genome-wide gene expression in genotypes differing only in Y chromosome origin revealed cryptic Y chromosome diversity (Lemos et al, 2008;Lemos et al, 2010;Jiang et al, 2010;Branco et al, 2013a). These include changes in the expression level of genes involved with functions as varied as metabolism, cell division, immune response and chromatin structure.…”

“…Moreover, these studies support the expectation that Y-linked variation preferentially affects genes with male-biased expression and modifies male fertility. Interestingly, YRV affects genes with greater expression divergence between D. melanogaster and D. simulans and higher level of expression polymorphism within species (Lemos et al, 2008;Sackton et al, 2011). It is reasonable to expect that YRV will modulate the evolution of fast-evolving genes and contribute to speciation and hybrid incompatibility in Drosophila.…”

“…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 .…”

“…Y-linked regulatory variation (YRV) is a source of gene expression diversity in Drosophila (Ashburner et al, 2005;Lemos et al, 2008). Moreover, analyses of Y chromosome variation in wild-type backgrounds and in genotypes with loss-of-function mutations revealed that the manifestation of YRV is exquisitely sensitive to the genomic background (Jiang et al, 2010;Branco et al, 2013a, b).…”

How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination

“…While Drosophila melanogaster has only 10-20 protein-coding loci on the Y chromosome, Lemos et al (2008) reported that it harbours substantial polymorphic regulatory variation that affects hundreds of X linked and autosomal loci with important functions.…”