Faculty Opinions recommendation of The contribution of female meiotic drive to the evolution of neo-sex chromosomes.

Segregation of chromosomes is a multistep process occurring both at mitosis and meiosis to ensure that daughter cells receive a complete set of genetic information. Critical components in the chromosome segregation include centromeres, kinetochores, components of sister chromatid and homologous chromosomes cohesion, microtubule organizing centres, and spindles. Based on the cytological work in the grasshopper Brachystola, it has been accepted for decades that segregation of homologs at meiosis is fundamentally random. This ensures that alleles on chromosomes have equal chance to be transmitted to progeny. At the same time mechanisms of meiotic drive and an increasing number of other examples of non-random segregation of autosomes and sex chromosomes provide insights into the underlying mechanisms of chromosome segregation but also question the textbook dogma of random chromosome segregation. Recent advances provide a better understanding of meiotic drive as a prominent force where cellular and chromosomal changes allow autosomes to bias their segregation. Less understood are mechanisms explaining observations that autosomal heteromorphism may cause biased segregation and regulate alternating segregation of multiple sex chromosome systems or translocation heterozygotes as an extreme case of non-random segregation. We speculate that molecular and cytological mechanisms of non-random segregation might be common in these cases and that there might be a continuous transition between random and non-random segregation which may play a role in the evolution of sexually antagonistic genes and sex chromosome evolution.

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Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

eLife ◽

10.7554/elife.35468 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 18

Author(s):

Colin D Meiklejohn ◽

Emily L Landeen ◽

Kathleen E Gordon ◽

Thomas Rzatkiewicz ◽

Sarah B Kingan ◽

...

Keyword(s):

Gene Flow ◽

Sex Chromosomes ◽

Population Genomics ◽

Sex Chromosome ◽

Hybrid Sterility ◽

Sequence Divergence ◽

Meiotic Drive ◽

Hybrid Male ◽

Local Sequence

During speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that a known drive element recently migrated between species and, rather than contributing to interspecific divergence, caused a strong reduction in local sequence divergence, undermining the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

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Recombination in the eggs and sperm in a simultaneously hermaphroditic vertebrate

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.1821 ◽

2016 ◽

Vol 283 (1844) ◽

pp. 20161821 ◽

Cited By ~ 7

Author(s):

L. Theodosiou ◽

W. O. McMillan ◽

O. Puebla

Keyword(s):

Local Adaptation ◽

Sex Chromosomes ◽

Meiotic Drive ◽

Reef Fishes ◽

High Density ◽

Linkage Maps ◽

Recombination Rates ◽

Reciprocal Crosses ◽

Link Type ◽

Few Data

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 sperm-specific 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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THE CONTRIBUTION OF FEMALE MEIOTIC DRIVE TO THE EVOLUTION OF NEO‐SEX CHROMOSOMES

Evolution ◽

10.1111/j.1558-5646.2012.01681.x ◽

2012 ◽

Vol 66 (10) ◽

pp. 3198-3208 ◽

Cited By ~ 32

Author(s):

Kohta Yoshida ◽

Jun Kitano

Keyword(s):

Sex Chromosomes ◽

Meiotic Drive

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Neo-sex chromosome evolution shapes sex-dependent asymmetrical introgression barrier

10.1101/2021.07.13.452191 ◽

2021 ◽

Author(s):

Silu Wang ◽

Matthew J Nalley ◽

Kamalakar Chatla ◽

Reema Aldaimalani ◽

Ailene MacPherson ◽

...

Keyword(s):

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Genetic Model ◽

Meiotic Drive ◽

Dependent Manner ◽

Sex Chromosome Evolution ◽

Hybrid Swarm ◽

Dual Roles ◽

Genotype Frequencies

It is increasingly recognized that sex chromosomes are not only the 'battlegrounds' between sexes, but also the 'Great Walls' fencing-off introgression between diverging lineages. Here we describe conflicting roles of nascent sex chromosomes on patterns of introgression in an experimental hybrid swarm. Drosophila nasuta and D. albomicans are recently diverged, fully fertile sister species that have different sex chromosome systems. The fusion between an autosome (Muller CD) with the ancestral X and Y gave rise to neo-sex chromosomes in D. albomicans, while Muller CDs remains unfused in D. nasuta. We found that a large block containing overlapping inversions on the neo-sex chromosome stood out as the strongest barrier to introgression. Intriguingly, the neo-sex chromosome introgression barrier is asymmetrical in a sex-dependent manner. Female hybrids showed significant D. albomicans biased introgression on Muller CD (neo-X excess), while males showed heterosis with excessive (neo-X, D. nasuta Muller CD) genotypes. While the neo-Y is a more compatible pairing partner of the neo-X, it also shows moderate levels of degeneration and may thus be selectively disfavored, and sex ratio assay revealed heterospecific meiotic drive. We used a population genetic model to dissect the interplay of sex chromosome drive, heterospecific pairing incompatibility between the neo-sex chromosomes and unfused Muller CD, neo-Y disadvantage, and neo-X advantage in generating the observed neo-X excess in females and heterozygous (neo-X, D. nasuta Muller CD) genotypes in males. We show that moderate neo-Y disadvantage and D. albomicans specific meiotic drive are required to counteract the effect of heterospecific meiotic drive observed in our cross, in concert with pairing incompatibility and neo-X advantage to explain observed genotype frequencies. Together, this hybrid swarm between a young species pair shed light onto the dual roles of neo-sex chromosome evolution in creating a sex-dependent asymmetrical introgression barrier at species boundary.

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Evolution of B Chromosomes: From Dispensable Parasitic Chromosomes to Essential Genomic Players

Frontiers in Genetics ◽

10.3389/fgene.2021.727570 ◽

2021 ◽

Vol 12 ◽

Author(s):

Martina Johnson Pokorná ◽

Radka Reifová

Keyword(s):

Sex Determination ◽

Significant Role ◽

Sex Chromosomes ◽

Meiotic Drive ◽

B Chromosomes ◽

Next Generation ◽

Multiple Copies ◽

Genomic Studies ◽

A Cell ◽

Eukaryotic Organisms

B chromosomes represent additional chromosomes found in many eukaryotic organisms. Their origin is not completely understood but recent genomic studies suggest that they mostly arise through rearrangements and duplications from standard chromosomes. They can occur in single or multiple copies in a cell and are usually present only in a subset of individuals in the population. Because B chromosomes frequently show unstable inheritance, their maintenance in a population is often associated with meiotic drive or other mechanisms that increase the probability of their transmission to the next generation. For all these reasons, B chromosomes have been commonly considered to be nonessential, selfish, parasitic elements. Although it was originally believed that B chromosomes had little or no effect on an organism’s biology and fitness, a growing number of studies have shown that B chromosomes can play a significant role in processes such as sex determination, pathogenicity and resistance to pathogens. In some cases, B chromosomes became an essential part of the genome, turning into new sex chromosomes or germline-restricted chromosomes with important roles in the organism’s fertility. Here, we review such cases of “cellular domestication” of B chromosomes and show that B chromosomes can be important genomic players with significant evolutionary impact.

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On the origin of sex chromosomes from meiotic drive

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2014.1932 ◽

2015 ◽

Vol 282 (1798) ◽

pp. 20141932 ◽

Cited By ~ 20

Author(s):

Francisco Úbeda ◽

Manus M. Patten ◽

Geoff Wild

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Meiotic Drive ◽

The Other ◽

Evolution Of Sex ◽

Dioecious Species

Most animals and many plants make use of specialized chromosomes (sex chromosomes) to determine an individual's sex. Best known are the XY and ZW sex-determination systems. Despite having evolved numerous times, sex chromosomes present something of an evolutionary puzzle. At their origin, alleles that dictate development as one sex or the other (primitive sex chromosomes) face a selective penalty, as they will be found more often in the more abundant sex. How is it possible that primitive sex chromosomes overcome this disadvantage? Any theory for the origin of sex chromosomes must identify the benefit that outweighs this cost and enables a sex-determining mutation to establish in the population. Here we show that a new sex-determining allele succeeds when linked to a sex-specific meiotic driver. The new sex-determining allele benefits from confining the driving allele to the sex in which it gains the benefit of drive. Our model requires few special assumptions and is sufficiently general to apply to the evolution of sex chromosomes in outbreeding cosexual or dioecious species. We highlight predictions of the model that can discriminate between this and previous theories of sex-chromosome origins.

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Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

10.1101/024711 ◽

2015 ◽

Cited By ~ 1

Author(s):

Colin D. Meiklejohn ◽

Emily L. Landeen ◽

Kathleen E. Gordon ◽

Thomas Rzatkiewicz ◽

Sarah B. Kingan ◽

...

Keyword(s):

Gene Flow ◽

Sex Chromosomes ◽

Population Genomics ◽

Sex Chromosome ◽

Hybrid Sterility ◽

Meiotic Drive ◽

Hybrid Male ◽

Selfish Genetic Elements ◽

Cryptic Sex

ABSTRACTDuring speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that, rather than contributing to interspecific divergence, a known drive element has recently migrated between species, caused a strong reduction in local divergence, and undermined the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

Download Full-text