scholarly journals Flavors of Non-Random Meiotic Segregation of Autosomes and Sex Chromosomes

Genes ◽  
2021 ◽  
Vol 12 (9) ◽  
pp. 1338
Author(s):  
Filip Pajpach ◽  
Tianyu Wu ◽  
Linda Shearwin-Whyatt ◽  
Keith Jones ◽  
Frank Grützner

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.

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Colin D Meiklejohn ◽  
Emily L Landeen ◽  
Kathleen E Gordon ◽  
Thomas Rzatkiewicz ◽  
Sarah B Kingan ◽  
...  

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.


Genetics ◽  
2001 ◽  
Vol 157 (1) ◽  
pp. 273-281 ◽  
Author(s):  
John E Tomkiel ◽  
Barbara T Wakimoto ◽  
Albert Briscoe

Abstract In recombination-proficient organisms, chiasmata appear to mediate associations between homologs at metaphase of meiosis I. It is less clear how homolog associations are maintained in organisms that lack recombination, such as male Drosophila. In lieu of chiasmata and synaptonemal complexes, there must be molecules that balance poleward forces exerted across homologous centromeres. Here we describe the genetic and cytological characterization of four EMS-induced mutations in teflon (tef), a gene involved in this process in Drosophila melanogaster. All four alleles are male specific and cause meiosis I-specific nondisjunction of the autosomes. They do not measurably perturb sex chromosome segregation, suggesting that there are differences in the genetic control of autosome and sex chromosome segregation in males. Meiotic transmission of univalent chromosomes is unaffected in tef mutants, implicating the tef product in a pairing-dependent process. The segregation of translocations between sex chromosomes and autosomes is altered in tef mutants in a manner that supports this hypothesis. Consistent with these genetic observations, cytological examination of meiotic chromosomes suggests a role of tef in regulating or mediating pairing of autosomal bivalents at meiosis I. We discuss implications of this finding in regard to the evolution of heteromorphic sex chromosomes and the mechanisms that ensure chromosome disjunction in the absence of recombination.


1984 ◽  
Vol 69 (1) ◽  
pp. 1-17
Author(s):  
D. Wise ◽  
P.J. Sillers ◽  
A. Forer

Single spindle fibres of Neocurtilla spermatocytes were irradiated by means of an ultraviolet microbeam. Irradiations were with monochromatic ultraviolet light. The single sex chromosome (the X1 univalent) reoriented after irradiation of its spindle fibre or of any of the spindle fibres associated with the heteromorphic bivalent (the X2Y bivalent): the X1 moved toward the Y half-spindle, and sometimes rotated as it moved. Irradiations of autosomal spindle fibres did not induce X1 movements, and hence the induction of reorientation is specific to irradiation of the spindle fibres associated with X1 or X2Y. In no case did the X2Y bivalent reorient; hence, the X1 is the active chromosome in ensuring that there is non-random segregation in Neocurtilla spermatocytes. The irradiations sometimes caused the X2Y bivalent to contrast, but the reorientation movements of the X1 were independent of the contraction of the X2Y bivalent. We suggest that the X1 and X2Y chromosomal spindle fibres form a network that is able to send signals to the X1 univalent to cause it to reorient.


2014 ◽  
Vol 86 (4) ◽  
pp. 1801-1812 ◽  
Author(s):  
WAGNER F. MOLINA ◽  
PABLO A. MARTINEZ ◽  
LUIZ A.C. BERTOLLO ◽  
CLAUDIO J. BIDAU

Mechanisms of accumulation based on typical centromeric drive or of chromosomes carrying pericentric inversions are adjusted to the general karyotype differentiation in the principal Actinopterygii orders. Here, we show that meiotic drive in fish is also supported by preferential establishment of sex chromosome systems and B chromosomes in orders with predominantly bi-brachial chromosomes. The mosaic of trends acting at an infra-familiar level in fish could be explained as the interaction of the directional process of meiotic drive as background, modulated on a smaller scale by adaptive factors or specific karyotypic properties of each group, as proposed for the orthoselection model.


Author(s):  
Joanna L Rifkin ◽  
Felix E G Beaudry ◽  
Zoë Humphries ◽  
Baharul I Choudhury ◽  
Spencer C H Barrett ◽  
...  

Abstract Classical models suggest that recombination rates on sex chromosomes evolve in a stepwise manner to localize sexually antagonistic variants in the sex in which they are beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with preexisting recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus. This species has a polymorphic karyotype with a young neo-sex chromosome, resulting from a Robertsonian fusion between the X chromosome and an autosome, in part of its geographic range. We identified the shared and neo-sex chromosomes using comparative genetic maps of the two cytotypes. We found that sex-linked regions of both the ancestral and the neo-sex chromosomes are embedded in large regions of low recombination. Furthermore, our comparison of the recombination landscape of the neo-sex chromosome to its autosomal homolog indicates that low recombination rates mainly preceded sex linkage. These patterns are not unique to the sex chromosomes; all chromosomes were characterized by massive regions of suppressed recombination spanning most of each chromosome. This represents an extreme case of the periphery-biased recombination seen in other systems with large chromosomes. Across all chromosomes, gene and repetitive sequence density correlated with recombination rate, with patterns of variation differing by repetitive element type. Our findings suggest that ancestrally low rates of recombination may facilitate the formation and subsequent evolution of heteromorphic sex chromosomes.


2021 ◽  
Author(s):  
Silu Wang ◽  
Matthew J Nalley ◽  
Kamalakar Chatla ◽  
Reema Aldaimalani ◽  
Ailene MacPherson ◽  
...  

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.


2015 ◽  
Vol 282 (1798) ◽  
pp. 20141932 ◽  
Author(s):  
Francisco Úbeda ◽  
Manus M. Patten ◽  
Geoff Wild

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.


Genetics ◽  
1984 ◽  
Vol 106 (3) ◽  
pp. 403-422
Author(s):  
Bruce McKee

ABSTRACT In Drosophila melanogaster males, deficiency for X heterochromatin causes high X-Y nondisjunction and skewed sex chromosome segregation ratios (meiotic drive). Y and XY classes are recovered poorly because of sperm dysfunction. In this study it was found that X heterochromatic deficiencies disrupt recovery not only of the Y chromosome but also of the X and autosomes, that both heterochromatic and euchromatic regions of chromosomes are affected and that the "sensitivity" of a chromosome to meiotic drive is a function of its length. Two models to explain these results are considered. One is a competitive model that proposes that all chromosomes must compete for a scarce chromosome-binding material in Xh  - males. The failure to observe competitive interactions among chromosome recovery probabilities rules out this model. The second is a pairing model which holds that normal spermiogenesis requires X-Y pairing at special heterochromatic pairing sites. Unsaturated pairing sites become gametic lethals. This model fails to account for autosomal sensitivity to meiotic drive. It is also contradicted by evidence that saturation of Y-pairing sites fails to suppress meiotic drive in Xh  - males and that extra X-pairing sites in an otherwise normal male do not induce drive. It is argued that meiotic drive results from separation of X euchromatin from X heterochromatin.


2015 ◽  
Author(s):  
Colin D. Meiklejohn ◽  
Emily L. Landeen ◽  
Kathleen E. Gordon ◽  
Thomas Rzatkiewicz ◽  
Sarah B. Kingan ◽  
...  

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.


Open Biology ◽  
2021 ◽  
Vol 11 (9) ◽  
pp. 210074
Author(s):  
Frances E. Clark ◽  
Takashi Akera

Female meiotic drive is the phenomenon where a selfish genetic element alters chromosome segregation during female meiosis to segregate to the egg and transmit to the next generation more frequently than Mendelian expectation. While several examples of female meiotic drive have been known for many decades, a molecular understanding of the underlying mechanisms has been elusive. Recent advances in this area in several model species prompts a comparative re-examination of these drive systems. In this review, we compare female meiotic drive of several animal and plant species, highlighting pertinent similarities.


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