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

Brandvain, Yaniv; Coop, Graham

doi:10.1534/genetics.111.136721

Cited by 85 publications

(139 citation statements)

References 97 publications

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“…In sharp contrast with the situation in plants, only eight of the 164 species considered in the last review on heterochiasmy [8] are hermaphroditic animals, and we found just a few additional cases in the literature (table 1). In these studies, heterochiasmy estimates are derived from chiasma counts (i.e.…”

Section: Introductioncontrasting

confidence: 70%

“…that the centromeres are located close to the chromosome periphery. Among the different hypotheses put forward to explain heterochiasmy [6][7][8][9][10][11][12][13][14], meiotic drive stands out by precisely predicting heterogeneous patterns of heterochiasmy along chromosomes and stronger heterochiasmy close to the centromeres [8].…”

Section: Discussionmentioning

confidence: 99%

“…A variety of hypotheses including metabolic rate [9], dispersal [6,10], sexual selection [10,11], neutrality [6], haploid selection [7,12], and female meiotic drive (which may be viewed as a particular type of haploid selection) [8,13] have been put forward to explain the occurrence of heterochiasmy. Under the female meiotic drive hypothesis, alleles exploit asymmetric cell division during oogenesis to increase in frequency.…”

Section: Introductionmentioning

confidence: 99%

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Recombination in the eggs and sperm in a simultaneously hermaphroditic vertebrate

2016

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When there is no recombination (achiasmy) in one sex, it is in the heterogametic one. This observation is so consistent that it constitutes one of the few patterns in biology that may be regarded as a 'rule ' and Haldane (Haldane 1922 J. Genet. 12, 101-109. (doi:10.1007/BF02983075)) proposed that it might be driven by selection against recombination in the sex chromosomes. Yet differences in recombination rates between the sexes (heterochiasmy) have also been reported in hermaphroditic species that lack sex chromosomes. In plants-the vast majority of which are hermaphroditic-selection at the haploid stage has been proposed to drive heterochiasmy. Yet few data are available for hermaphroditic animals, and barely any for hermaphroditic vertebrates. Here, we leverage reciprocal crosses between two black hamlets (Hypoplectrus nigricans, Serranidae), simultaneously hermaphroditic reef fishes from the wider Caribbean, to generate high-density egg-and spermspecific linkage maps for each parent. We find globally higher recombination rates in the eggs, with dramatically pronounced heterochiasmy at the chromosome peripheries. We suggest that this pattern may be due to female meiotic drive, and that this process may be an important source of heterochiasmy in animals. We also identify a large non-recombining region that may play a role in speciation and local adaptation in Hypoplectrus.

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Section: Introductioncontrasting

confidence: 70%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Recombination in the eggs and sperm in a simultaneously hermaphroditic vertebrate

2016

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“…In addition to their relevance to an understanding of gene clusters, our results might also contribute to an enhanced understanding of the evolution of sex-specific recombination rates [26,27]. Previous models to explain sex-specific recombination rates require certain of the properties of our model and results, namely haploid (or pseudo-haploid) selection pressure and sex-specific LD.…”

Section: Discussionmentioning

confidence: 86%

Sexual and parental antagonism shape genomic architecture

Patten

Haig

2013

Proc. R. Soc. B.

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Populations with two sexes are vulnerable to a pair of genetic conflicts: sexual antagonism that can arise when alleles have opposing fitness effects on females and males; and parental antagonism that arises when alleles have opposing fitness effects when maternally and paternally inherited. This paper extends previous theoretical work that found stable linkage disequilibrium (LD) between sexually antagonistic loci. We find that LD is also generated between parentally antagonistic loci, and between sexually and parentally antagonistic loci, without any requirement of epistasis. We contend that the LD in these models arises from the admixture of gene pools subject to different selective histories. We also find that polymorphism maintained by parental antagonism at one locus expands the opportunity for polymorphism at a linked locus experiencing parental or sexual antagonism. Taken together, our results predict the chromosomal clustering of loci that segregate for sexually and parentally antagonistic alleles. Thus, genetic conflict may play a role in the evolution of genomic architecture.

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“…It should also be noted that the linkage-disequilibrium method can yield only estimates for historical populationlevel and sex-averaged crossover rates. Thus, this method is not suitable for examining the variation of recombination rate between individuals and sexes (e.g., Coop and Przeworski 2007;Kong et al 2010;Brandvain and Coop 2012;Comeron et al 2012;Bauer et al 2013). Furthermore, it is well known that crossover, the reciprocal exchange of DNA between homologous chromosomes, only represents a small proportion (often ,20%) of the total recombination events, with the rest generating nonreciprocal, gene-conversion events (Langley et al 2000;Malkova et al 2004;Morrell et al 2006;Mancera et al 2008;Yang et al 2012;Lynch et al 2014).…”

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confidence: 99%

A Male-Specific Genetic Map of the MicrocrustaceanDaphnia pulexBased on Single-Sperm Whole-Genome Sequencing

Ackerman

Long

et al. 2015

Genetics

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Genetic linkage maps are critical for assembling draft genomes to a meaningful chromosome level and for deciphering the genomic underpinnings of biological traits. The estimates of recombination rates derived from genetic maps also play an important role in understanding multiple aspects of genomic evolution such as nucleotide substitution patterns and accumulation of deleterious mutations. In this study, we developed a high-throughput experimental approach that combines fluorescence-activated cell sorting, whole-genome amplification, and shortread sequencing to construct a genetic map using single-sperm cells. Furthermore, a computational algorithm was developed to analyze singlesperm whole-genome sequencing data for map construction. These methods allowed us to rapidly build a male-specific genetic map for the freshwater microcrustacean Daphnia pulex, which shows significant improvements compared to a previous map. With a total of mapped 1672 haplotype blocks and an average intermarker distance of 0.87 cM, this map spans a total genetic distance of 1451 Kosambi cM and comprises 90% of the resolved regions in the current Daphnia reference assembly. The map also reveals the mistaken mapping of seven scaffolds in the reference assembly onto chromosome II by a previous microsatellite map based on F 2 crosses. Our approach can be easily applied to many other organisms and holds great promise for unveiling the intragenomic and intraspecific variation in the recombination rates.KEYWORDS meiosis; fluorescence-activated cell sorting; single cell; whole-genome amplification C ONSTRUCTING a genetic linkage map that encompasses as much genomic sequence as possible is critical for current endeavors of de novo genomic assembly (e.g., Kawakami et al. 2014; International Cassava Genetic Map Consortium (ICGMC) 2015) and for deciphering the genomic underpinnings of the biological traits in the species of interest (Lynch and Walsh 1998). Genetic maps can be utilized in several ways to help achieve these goals. At the very least, a linkage map with an adequate number of genetic markers can serve as the backbone for orienting and assembling segments of DNA (i.e., scaffolds) into chromosomes. The developed genetic markers can also be used in QTL association mapping and genomic-scanning efforts to investigate genetic loci underlying ecological tolerance, adaptation, and disease. Furthermore, a linkage map provides genome-wide estimates of the meiotic recombination rate, which plays a significant role in the distribution of genetic diversity (Nachman 2001), rate of adaptation (Bachtrog and Charlesworth 2002), accumulation of deleterious mutations (Hussin et al. 2015), and nucleotide substitution (Duret and Arndt 2008).Currently, the most common approach for constructing a genetic linkage map is based on genotyping a large number of molecular markers (e.g., SNPs, microsatellites) from a large number of offspring (usually on the order of hundreds) derived from various kinds of crossing schemes (e.g., backcrosses, F 2 s, reco...

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

Cited by 85 publications

References 97 publications

Recombination in the eggs and sperm in a simultaneously hermaphroditic vertebrate

Recombination in the eggs and sperm in a simultaneously hermaphroditic vertebrate

Sexual and parental antagonism shape genomic architecture

A Male-Specific Genetic Map of the MicrocrustaceanDaphnia pulexBased on Single-Sperm Whole-Genome Sequencing

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