Surprising Differences in the Variability of Y Chromosomes in African and Cosmopolitan Populations ofDrosophila melanogaster

Abstract

The nonrecombining Drosophila melanogaster Y chromosome is heterochromatic and has few genes. Despite these limitations, there remains ample opportunity for natural selection to act on the genes that are vital for male fertility and on Y factors that modulate gene expression elsewhere in the genome. Y chromosomes of many organisms have low levels of nucleotide variability, but a formal survey of D. melanogaster Y chromosome variation had yet to be performed. Here we surveyed Y-linked variation in six populations of D. melanogaster spread across the globe. We find surprisingly low levels of variability in African relative to Cosmopolitan (i.e., non-African) populations. While the low levels of Cosmopolitan Y chromosome polymorphism can be explained by the demographic histories of these populations, the staggeringly low polymorphism of African Y chromosomes cannot be explained by demographic history. An explanation that is entirely consistent with the data is that the Y chromosomes of Zimbabwe and Uganda populations have experienced recent selective sweeps. Interestingly, the Zimbabwe and Uganda Y chromosomes differ: in Zimbabwe, a European Y chromosome appears to have swept through the population.T HE Drosophila melanogaster Y chromosome is highly functionally specialized in male-related activities (Hardy et al. 1981;Kennison 1981;Goldstein et al. 1982). Although it comprises 13% of the male genome (40 Mb;Hoskins et al. 2002), the D. melanogaster Y chromosome has only 13 known protein-coding genes (Goldstein et al. 1982;Carvalho et al. 2000Carvalho et al. , 2001Vibranovski et al. 2008;Krsticevic et al. 2010), all thought to be active only in primary spermatocytes in the testis (Hardy et al. 1981). The remainder of the Y chromosome is heterochromatic and dense in repetitive elements (Hoskins et al. 2002).Although the D. melanogaster Y chromosome is highly repetitive and gene poor, several lines of evidence suggest that it harbors functionally important variation (Chippindale and Rice 2001;Rohmer et al. 2004;Lemos et al. 2008;Lemos et al. 2010). The Y chromosome has contributed to variation in thermotolerance across D. melanogaster populations (Rohmer et al. 2004), has epistatic effects on male fitness (Chippindale and Rice 2001), and has epigenetic effects on the expression of genes across the genome (Lemos et al. 2008Jiang et al. 2010), including specifically in the male germline (Zhang 2000). The functional variation on the Y chromosome has been somewhat of a paradox because, while there is evidence for structural polymorphism (Lyckegaard and Clark 1989), the haploid transmission of the Y chromosome makes it far more difficult to maintain substantial levels of genetic variation (Clark 1987). In one small survey of Y chromosomal variation in a protein-coding gene, kl-5 (DhcYh3), only a single segregating site was discovered in 11 lines of D. melanogaster and no variants were found in 10 lines of Drosophila simulans (Zurovcova and Eanes 1999). A more recent study in a closely related species, D. simulans,...

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

“…These phenotypes, including fertility and YRV, may emerge from nongenic elements on the Y chromosome heterochromatin and may be under selection Francisco and Lemos, 2014). The piRNA pathway is a candidate to mediate Y chromosome effects in hybrids (Castillo et al, 2011;Kelleher et al, 2012) and could reconcile the low polymorphism in Y-linked protein-coding sequences (Zurovcova and Eanes, 1999;Larracuente and Clark, 2013) with YRV. Differences in the extensive blocks of heterochromatin are given by the kinds and quantities of satellite DNA and transposable elements.…”

Genetic Diversity on the Sex Chromosomes

“…Y chromosome diversity is exceedingly low across all D. melanogaster populations studied, some of which can be explained by population demography, but not in African populations, where recent selective sweeps are proposed to explain the low Y-linked diversity in populations from Zimbambwe and Uganda (Larracuente and Clark 2013). Diversity is also reported to be much lower than neutral expectations in D. subobscura and D. madeirensis and is inferred to be due to linked selection—either background selection or hitchhiking—because corresponding X/A ratios in these species are not consistent with extreme variance in male reproductive success (Herrig et al.…”

Within‐population Y‐linked genetic variation for lifespan in Drosophila melanogaster

“…In accordance with above scenario, the Y chromosome of Drosophila melanogaster features just 13 protein‐coding genes (Carvalho et al ., ; Carvalho & Clark, ; Koerich et al ., ; Vibranovski et al ., ; Krsticevic et al ., ), which all exhibit very low levels of nucleotide polymorphism within populations (Zurovcova & Eanes, ; Larracuente & Clark, ). The Y chromosome is, furthermore, completely heterochromatic (densely packed DNA which typically suppresses expression) (Hoskins et al ., ), and although males which lack a Y chromosome (XO) are infertile, they are viable and only have minor changes to their phenotype (Bridges, ).…”