Evidence of Susceptibility and Resistance to Cryptic X-Linked Meiotic Drive in Natural Populations of Drosophila Melanogaster

Reed, Floyd A.; Reeves, Riona; Aquadro, Charles F.

doi:10.1111/j.0014-3820.2005.tb01778.x

Cited by 13 publications

(11 citation statements)

References 89 publications

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“…In drive systems, driver haplotypes are expected to fix within populations and are observed only where genotypic selection against them prevents fixation (22). Where this countervailing force is absent, drivers become fixed in a population and are detectable only in interpopulation crosses (23)(24)(25)(26)(27). In C. elegans, homozygotes of both haplotypes are fit, and incompatible haplotypes co-occur globally.…”

Section: Discussionmentioning

confidence: 99%

Widespread Genetic Incompatibility in C. Elegans Maintained by Balancing Selection

Seidel

Rockman

Kruglyak

2008

Science

265

354

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Natural selection is expected to eliminate genetic incompatibilities from interbreeding populations. We have identified a globally distributed incompatibility in the primarily selfing species Caenorhabditis elegans that has been maintained despite its negative consequences for fitness. Embryos homozygous for a naturally occurring deletion of the zygotically acting gene, zeel-1, arrest if their sperm parent carries an incompatible allele of a second, paternal effect locus, peel-1. The two interacting loci are tightly linked, with incompatible alleles occurring in linkage disequilibrium in two common haplotypes. These haplotypes exhibit elevated sequence divergence, and population genetic analyses of this region indicate that natural selection is preserving both haplotypes in the population. Our data suggest that long-term maintenance of a balanced polymorphism has permitted the incompatibility to persist despite gene flow across the rest of the genome.Caenorhabditis elegans is a globally distributed species of free-living, bacteria-eating nematode. Although rare males contribute at a low rate to outcrossing, C. elegans occurs primarily as inbred, self-fertilizing hermaphrodites (1-4). A wild isolate from Hawaii, CB4856, has been identified among well-studied isolates as the most divergent at the sequence level from the standard laboratory strain, N2, derived from an isolate from Bristol, England (5-7). As a result of this sequence divergence, the Hawaiian strain is widely used to map mutations induced in the Bristol background. Genetic incompatibility between Bristol and HawaiiWe generated recombinant inbred lines (RILs) from the tenth generation of an advanced intercross between Bristol and Hawaii to study natural genetic variation in C. elegans, and we genotyped the RILs at 1450 single nucleotide polymorphism markers (8). We noted that a region on the left arm of chromsome I exhibited a dramatic deficit of Hawaii alleles among the RILs. Of 239 RILs, only five carried the Hawaii allele at the most skewed marker, and simulations of the intercross pedigree indicated that this allele frequency skew could not have arisen by drift, suggesting that selection had acted during construction of the RILs (Fig. S1). We then crossed Hawaii to a Bristol strain carrying a visible marker located 10cM from the most skewed RIL marker, and we examined F2 progeny produced by self-fertilizing F1 hermaphrodites. Surprisingly, approximately 25% of F2 progeny arrested as embryos, and embryonic lethality segregated opposite the visible marker (Table 1). F2 lethality was not an effect of the marker: self-fertilizing F1 hermaphrodites derived from reciprocal crosses between Hawaii and wildtype Bristol produced 25% dead embryos, as did F1 hermaphrodites mated to F1 males (Fig. 1).

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Section: Discussionmentioning

confidence: 99%

Widespread Genetic Incompatibility in C. Elegans Maintained by Balancing Selection

Seidel

Rockman

Kruglyak

2008

Science

265

354

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“…Currently, our knowledge of the distribution of meiotic drivers and their fitness effects is very incomplete and is likely biased toward the overrepresentation of strong drivers with extreme fitness effects. However, there is mounting evidence supporting the existence of subtle transmission ratio distorters (e.g., Zöllner et al 2004;Reed et al 2005;Aparicio et al 2010;Axelsson et al 2010) (however, the mechanism of distortion in these cases is often unknown). Similarly, although there is ample evidence that the recombination rate, as well as the strength and direction of heterochiasmy, varies across species, few allelic variants that influence sex-specific recombination rates have been identified.…”

Section: Discussionmentioning

confidence: 99%

Scrambling Eggs: Meiotic Drive and the Evolution of Female Recombination Rates

2012

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Theories to explain the prevalence of sex and recombination have long been a central theme of evolutionary biology. Yet despite decades of attention dedicated to the evolution of sex and recombination, the widespread pattern of sex differences in the recombination rate is not well understood and has received relatively little theoretical attention. Here, we argue that female meiotic drivers-alleles that increase in frequency by exploiting the asymmetric cell division of oogenesis-present a potent selective pressure favoring the modification of the female recombination rate. Because recombination plays a central role in shaping patterns of variation within and among dyads, modifiers of the female recombination rate can function as potent suppressors or enhancers of female meiotic drive. We show that when female recombination modifiers are unlinked to female drivers, recombination modifiers that suppress harmful female drive can spread. By contrast, a recombination modifier tightly linked to a driver can increase in frequency by enhancing female drive. Our results predict that rapidly evolving female recombination rates, particularly around centromeres, should be a common outcome of meiotic drive. We discuss how selection to modify the efficacy of meiotic drive may contribute to commonly observed patterns of sex differences in recombination.

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“…The presence of X-linked meiotic drivers inside Africa could cause the replacement of Y chromosomes and shape patterns of local adaptation. Although the frequency of X-linked male meiotic drive is unknown in D. melanogaster (see Hanks 1968;Hurst 1996;Reed et al 2005 for possible evidence of such drive in this species), cryptic X-linked meiotic drive is common in other Drosophila species (Gershenson 1928;James and Jaenike 1990;Orr and Irving 2005;MontchampMoreau et al 2006;Tao et al 2007). Another possibility is that effects of Y chromosome polymorphism on gene expression (Lemos et al 2008 may influence the adaptive evolution of the African Y chromosome.…”

Section: Recent Selection On African Y Chromosomesmentioning

confidence: 99%

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

Larracuente

Clark

2013

Genetics

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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,...

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Evidence of Susceptibility and Resistance to Cryptic X-Linked Meiotic Drive in Natural Populations of Drosophila Melanogaster

Cited by 13 publications

References 89 publications

Widespread Genetic Incompatibility in C. Elegans Maintained by Balancing Selection

Widespread Genetic Incompatibility in C. Elegans Maintained by Balancing Selection

Scrambling Eggs: Meiotic Drive and the Evolution of Female Recombination Rates

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

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