Meiotic drive

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Meiotic drive is a type of intragenomic conflict, whereby one or more loci within a genome will affect a manipulation of the meiotic process in such a way as to favor the transmission of one or more alleles over another, regardless of its phenotypic expression. More simply, meiotic drive is when one copy of a gene is passed on to offspring more than the expected 50% of the time. According to Buckler et al., "Meiotic drive is the subversion of meiosis so that particular genes are preferentially transmitted to the progeny. Meiotic drive generally causes the preferential segregation of small regions of the genome". [1]

Contents

Meiotic drive in plants

The first report of meiotic drive came from Marcus Rhoades who in 1942 observed a violation of Mendelian segregation ratios for the R locus - a gene controlling the production of the purple pigment anthocyanin in maize kernels - in a maize line carrying abnormal chromosome 10 (Ab10). [2] Ab10 differs from the normal chromosome 10 by the presence of a 150-base pair heterochromatic region called 'knob', which functions as a centromere during division (hence called 'neocentromere') and moves to the spindle poles faster than the centromeres during meiosis I and II. [3] The mechanism for this was later found to involve the activity of a kinesin-14 gene called Kinesin driver (Kindr). Kindr protein is a functional minus-end directed motor, displaying quicker minus-end directed motility than an endogenous kinesin-14, such as Kin11. As a result Kindr outperforms the endogenous kinesins, pulling the 150 bp knobs to the poles faster than the centromeres and causing Ab10 to be preferentially inherited during meiosis [4]

Meiotic drive in animals

The unequal inheritance of gametes has been observed since the 1950s, [5] in contrast to Gregor Mendel's First and Second Laws (the law of segregation and the law of independent assortment), which dictate that there is a random chance of each allele being passed on to offspring. Examples of selfish drive genes in animals have primarily been found in rodents and flies. These drive systems could play important roles in the process of speciation. For instance, the proposal that hybrid sterility (Haldane's rule) may arise from the divergent evolution of sex chromosome drivers and their suppressors. [6]

Meiotic drive in mice

Early observations of mouse t-haplotypes by Mary Lyon described numerous genetic loci on chromosome 17 that suppress X-chromosome sex ratio distortion. [7] [8] If a driver is left unchecked, this may lead to population extinction as the population would fix for the driver (e.g. a selfish X chromosome), removing the Y chromosome (and therefore males) from the population. The idea that meiotic drivers and their suppressors may govern speciation is supported by observations that mouse Y chromosomes lacking certain genetic loci produce female-biased offspring, implying these loci encode suppressors of drive. [9] Moreover, matings of certain mouse strains used in research results in unequal offspring ratios. One gene responsible for sex ratio distortion in mice is r2d2 (r2d2 – responder to meiotic drive 2), which predicts which strains of mice can successfully breed without offspring sex ratio distortion. [10]

Meiotic drive in flies

A stalk-eyed fly Stalk-eyed fly.jpg
A stalk-eyed fly

Selfish chromosomes of stalk-eyed flies have had ecological consequences. Driving X chromosomes lead to reductions in male fecundity and mating success, leading to frequency dependent selection maintaining both the driving alleles and wild-type alleles. [11]

Multiple species of fruit fly are known to have driving X chromosomes, of which the best-characterized are found in Drosophila simulans . Three independent driving X chromosomes are known in D. simulans, called Paris, Durham, and Winters. In Paris, the driving gene encodes a DNA modelling protein ("heterochromatin protein 1 D2" or HP1D2), where the allele of the driving copy fails to prepare the male Y chromosome for meiosis. [12] In Winters, the gene responsible ("Distorter on the X" or Dox) has been identified, though the mechanism by which it acts is still unknown. [13] The strong selective pressure imposed by these driving X chromosomes has given rise to suppressors of drive, of which the genes are somewhat known for Winters, Durham, and Paris. These suppressors encode hairpin RNAs which match the sequence of driver genes (such as Dox), leading host RNA interference pathways to degrade Dox sequence. [14] Autosomal suppressors of drive are known in Drosophila mediopunctata , [15] Drosophila paramelanica , [16] Drosophila quinaria , [17] and Drosophila testacea , [18] emphasizing the importance of these drive systems in natural populations.

See also

Related Research Articles

<span class="mw-page-title-main">Meiosis</span> Cell division producing haploid gametes

Meiosis is a special type of cell division of germ cells in sexually-reproducing organisms that produces the gametes, the sperm or egg cells. It involves two rounds of division that ultimately result in four cells, each with only one copy of each chromosome (haploid). Additionally, prior to the division, genetic material from the paternal and maternal copies of each chromosome is crossed over, creating new combinations of code on each chromosome. Later on, during fertilisation, the haploid cells produced by meiosis from a male and a female will fuse to create a zygote, a cell with two copies of each chromosome again.

Selfish genetic elements are genetic segments that can enhance their own transmission at the expense of other genes in the genome, even if this has no positive or a net negative effect on organismal fitness. Genomes have traditionally been viewed as cohesive units, with genes acting together to improve the fitness of the organism. However, when genes have some control over their own transmission, the rules can change, and so just like all social groups, genomes are vulnerable to selfish behaviour by their parts.

<span class="mw-page-title-main">Chromosomal crossover</span> Cellular process

Chromosomal crossover, or crossing over, is the exchange of genetic material during sexual reproduction between two homologous chromosomes' non-sister chromatids that results in recombinant chromosomes. It is one of the final phases of genetic recombination, which occurs in the pachytene stage of prophase I of meiosis during a process called synapsis. Synapsis begins before the synaptonemal complex develops and is not completed until near the end of prophase I. Crossover usually occurs when matching regions on matching chromosomes break and then reconnect to the other chromosome.

<span class="mw-page-title-main">Genetic recombination</span> Production of offspring with combinations of traits that differ from those found in either parent

Genetic recombination is the exchange of genetic material between different organisms which leads to production of offspring with combinations of traits that differ from those found in either parent. In eukaryotes, genetic recombination during meiosis can lead to a novel set of genetic information that can be further passed on from parents to offspring. Most recombination occurs naturally and can be classified into two types: (1) interchromosomal recombination, occurring through independent assortment of alleles whose loci are on different but homologous chromosomes ; & (2) intrachromosomal recombination, occurring through crossing over.

<span class="mw-page-title-main">Y chromosome</span> Sex chromosome in the XY sex-determination system

The Y chromosome is one of two sex chromosomes in therian mammals and other organisms. Along with the X chromosome, it is part of the XY sex-determination system, in which the Y is the sex-determining because it is the presence or absence of Y chromosome that determines the male or female sex of offspring produced in sexual reproduction. In mammals, the Y chromosome contains the SRY gene, which triggers development of male gonads. The Y chromosome is passed only from male parents to male offspring.

Genetic linkage is the tendency of DNA sequences that are close together on a chromosome to be inherited together during the meiosis phase of sexual reproduction. Two genetic markers that are physically near to each other are unlikely to be separated onto different chromatids during chromosomal crossover, and are therefore said to be more linked than markers that are far apart. In other words, the nearer two genes are on a chromosome, the lower the chance of recombination between them, and the more likely they are to be inherited together. Markers on different chromosomes are perfectly unlinked, although the penetrance of potentially deleterious alleles may be influenced by the presence of other alleles, and these other alleles may be located on other chromosomes than that on which a particular potentially deleterious allele is located.

<span class="mw-page-title-main">Homologous chromosome</span> Chromosomes that pair in fertilization

A pair of homologous chromosomes, or homologs, is a set of one maternal and one paternal chromosome that pair up with each other inside a cell during fertilization. Homologs have the same genes in the same loci, where they provide points along each chromosome that enable a pair of chromosomes to align correctly with each other before separating during meiosis. This is the basis for Mendelian inheritance, which characterizes inheritance patterns of genetic material from an organism to its offspring parent developmental cell at the given time and area.

<span class="mw-page-title-main">Nondisjunction</span> Failure to separate properly during cell division

Nondisjunction is the failure of homologous chromosomes or sister chromatids to separate properly during cell division (mitosis/meiosis). There are three forms of nondisjunction: failure of a pair of homologous chromosomes to separate in meiosis I, failure of sister chromatids to separate during meiosis II, and failure of sister chromatids to separate during mitosis. Nondisjunction results in daughter cells with abnormal chromosome numbers (aneuploidy).

<span class="mw-page-title-main">Haldane's rule</span> Observation in evolutionary biology

Haldane's rule is an observation about the early stage of speciation, formulated in 1922 by the British evolutionary biologist J. B. S. Haldane, that states that if — in a species hybrid — only one sex is inviable or sterile, that sex is more likely to be the heterogametic sex. The heterogametic sex is the one with two different sex chromosomes; in therian mammals, for example, this is the male.

<span class="mw-page-title-main">Chromosomal inversion</span> Chromosome rearrangement in which a segment of a chromosome is reversed

An inversion is a chromosome rearrangement in which a segment of a chromosome becomes inverted within its original position. An inversion occurs when a chromosome undergoes a two breaks within the chromosomal arm, and the segment between the two breaks inserts itself in the opposite direction in the same chromosome arm. The breakpoints of inversions often happen in regions of repetitive nucleotides, and the regions may be reused in other inversions. Chromosomal segments in inversions can be as small as 1 kilobases or as large as 100 megabases. The number of genes captured by an inversion can range from a handful of genes to hundreds of genes. Inversions can happen either through ectopic recombination between repetitive sequences, or through chromosomal breakage followed by non-homologous end joining.

<span class="mw-page-title-main">Non-Mendelian inheritance</span> Type of pattern of inheritance

Non-Mendelian inheritance is any pattern in which traits do not segregate in accordance with Mendel's laws. These laws describe the inheritance of traits linked to single genes on chromosomes in the nucleus. In Mendelian inheritance, each parent contributes one of two possible alleles for a trait. If the genotypes of both parents in a genetic cross are known, Mendel's laws can be used to determine the distribution of phenotypes expected for the population of offspring. There are several situations in which the proportions of phenotypes observed in the progeny do not match the predicted values.

Gene conversion is the process by which one DNA sequence replaces a homologous sequence such that the sequences become identical after the conversion event. Gene conversion can be either allelic, meaning that one allele of the same gene replaces another allele, or ectopic, meaning that one paralogous DNA sequence converts another.

Intragenomic conflict refers to the evolutionary phenomenon where genes have phenotypic effects that promote their own transmission in detriment of the transmission of other genes that reside in the same genome. The selfish gene theory postulates that natural selection will increase the frequency of those genes whose phenotypic effects cause their transmission to new organisms, and most genes achieve this by cooperating with other genes in the same genome to build an organism capable of reproducing and/or helping kin to reproduce. The assumption of the prevalence of intragenomic cooperation underlies the organism-centered concept of inclusive fitness. However, conflict among genes in the same genome may arise both in events related to reproduction and altruism.

Transvection is an epigenetic phenomenon that results from an interaction between an allele on one chromosome and the corresponding allele on the homologous chromosome. Transvection can lead to either gene activation or repression. It can also occur between nonallelic regions of the genome as well as regions of the genome that are not transcribed.

<span class="mw-page-title-main">Heterogametic sex</span> Sex of a species in which the sex chromosomes are not the same

The heterogametic sex is the sex of a species where an individual's gametes have non-matching sex chromosomes. In humans, the heterogametic sex is the male sex, where each gamete's sex chromosomes are X and Y. This is in contrast to the female sex, where each gamete's sex chromosomes are X and X. This arrangement is understood within the XY sex-determination system.

<span class="mw-page-title-main">Meiotic recombination checkpoint</span>

The meiotic recombination checkpoint monitors meiotic recombination during meiosis, and blocks the entry into metaphase I if recombination is not efficiently processed.

Achiasmate Meiosis refers to meiosis without chiasmata, which are structures that are necessary for recombination to occur and that usually aid in the segregation of non-sister homologs. The pachytene stage of prophase I typically results in the formation of chiasmata between homologous non-sister chromatids in the tetrad chromosomes that form. The formation of a chiasma is also referred to as crossing over. When two homologous chromatids cross over, they form a chiasma at the point of their intersection. However, it has been found that there are cases where one or more pairs of homologous chromosomes do not form chiasmata during pachynema. Without a chiasma, no recombination between homologs can occur.

Holocentric chromosomes are chromosomes that possess multiple kinetochores along their length rather than the single centromere typical of other chromosomes. They were first described in cytogenetic experiments in 1935. Since this first observation, the term holocentric chromosome has referred to chromosomes that: i) lack the primary constriction corresponding to the centromere observed in monocentric chromosomes; and ii) possess multiple kinetochores dispersed along the entire chromosomal axis, such that microtubules bind to the chromosome along its entire length and move broadside to the pole from the metaphase plate. Holocentric chromosomes are also termed holokinetic, because, during cell division, the sister chromatids move apart in parallel and do not form the classical V-shaped figures typical of monocentric chromosomes.

<i>Drosophila neotestacea</i> Species of fly

Drosophila neotestacea is a member of the testacea species group of Drosophila. Testacea species are specialist fruit flies that breed on the fruiting bodies of mushrooms. These flies will choose to breed on psychoactive mushrooms such as the Fly Agaric Amanita muscaria. Drosophila neotestacea can be found in temperate regions of North America, ranging from the north eastern United States to western Canada.

Non-random segregation of chromosomes is a deviation from the usual distribution of chromosomes during meiosis, that is, during segregation of the genome among gametes. While usually according to the 2nd Mendelian rule homologous chromosomes are randomly distributed among daughter nuclei, there are various modes deviating from this in numerous organisms that are "normal" in the relevant taxa. They may involve single chromosome pairs (bivalents) or single chromosomes without mating partners (univalents), or even whole sets of chromosomes, in that these are separated according to their parental origin and, as a rule, only those of maternal origin are passed on to the offspring. It also happens that non-homologous chromosomes segregate in a coordinated manner. As a result, this is a form of Non-Mendelian inheritance.

References

  1. Buckler ES, Phelps-Durr TL, Buckler CS, Dawe RK, Doebley JF, Holtsford TP (September 1999). "Meiotic drive of chromosomal knobs reshaped the maize genome". Genetics. 153 (1): 415–26. doi:10.1093/genetics/153.1.415. PMC   1460728 . PMID   10471723.
  2. Rhoades MM (July 1942). "Preferential Segregation in Maize". Genetics. 27 (4): 395–407. doi:10.1093/genetics/27.4.395. PMC   1209167 . PMID   17247049.
  3. Rhoades, M.M.; Vilkomerson (1942). "On the anaphase movement of chromosomes". Proc. Natl. Acad. Sci. 28 (10): 433–436. Bibcode:1942PNAS...28..433R. doi: 10.1073/pnas.28.10.433 . PMC   1078510 . PMID   16588574.
  4. Dawe RK, Lowry EG, Gent JI, Stitzer MC, Swentowsky KW, Higgins DM, Ross-Ibarra J, Wallace JG, Kanizay LB, Alabady M, Qiu W, Tseng KF, Wang N, Gao Z, Birchler JA, Harkess AE, Hodges AL, Hiatt EN (May 2018). "A Kinesin-14 Motor Activates Neocentromeres to Promote Meiotic Drive in Maize". Cell. 173 (4): 839–850.e18. doi: 10.1016/j.cell.2018.03.009 . PMID   29628142.
  5. Sandler L, Novitski E (1957). "Meiotic Drive as an Evolutionary Force". The American Naturalist. 91 (857): 105–110. doi:10.1086/281969. S2CID   85014310.
  6. Helleu Q, Gérard PR, Montchamp-Moreau C (December 2014). "Sex chromosome drive". Cold Spring Harbor Perspectives in Biology. 7 (2): a017616. doi:10.1101/cshperspect.a017616. PMC   4315933 . PMID   25524548.
  7. Lyon MF (1984). "Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus". Cell. 37 (2): 621–628. doi:10.1016/0092-8674(84)90393-3. PMID   6722884. S2CID   21065216.
  8. Lyon MF (1986). "Male sterility of the mouse t-complex is due to homozygosity of the distorter genes". Cell. 44 (2): 357–363. doi:10.1016/0092-8674(86)90770-1. PMID   3943128. S2CID   30795392.
  9. Cocquet J, Ellis PJ, Yamauchi Y, Mahadevaiah SK, Affara NA, Ward MA, Burgoyne PS (November 2009). "The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis". PLOS Biology. 7 (11): e1000244. doi: 10.1371/journal.pbio.1000244 . PMC   2770110 . PMID   19918361.
  10. Didion JP, Morgan AP, Clayshulte AM, Mcmullan RC, Yadgary L, Petkov PM, Bell TA, Gatti DM, Crowley JJ, Hua K, Aylor DL, Bai L, Calaway M, Chesler EJ, French JE, Geiger TR, Gooch TJ, Garland T, Harrill AH, Hunter K, McMillan L, Holt M, Miller DR, O'Brien DA, Paigen K, Pan W, Rowe LB, Shaw GD, Simecek P, et al. (February 2015). "A multi-megabase copy number gain causes maternal transmission ratio distortion on mouse chromosome 2". PLOS Genetics. 11 (2): e1004850. doi: 10.1371/journal.pgen.1004850 . PMC   4334553 . PMID   25679959.
  11. Wilkinson GS, Johns PM, Kelleher ES, Muscedere ML, Lorsong A (November 2006). "Fitness effects of X chromosome drive in the stalk-eyed fly, Cyrtodiopsis dalmanni" (PDF). Journal of Evolutionary Biology. 19 (6): 1851–60. doi: 10.1111/j.1420-9101.2006.01169.x . PMID   17040382.
  12. Helleu Q, Gérard PR, Dubruille R, Ogereau D, Prud'homme B, Loppin B, Montchamp-Moreau C (April 2016). "Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive". Proceedings of the National Academy of Sciences of the United States of America. 113 (15): 4110–5. Bibcode:2016PNAS..113.4110H. doi: 10.1073/pnas.1519332113 . PMC   4839453 . PMID   26979956.
  13. Courret C, Gérard PR, Ogereau D, Falque M, Moreau L, Montchamp-Moreau C (December 2018). "X-chromosome meiotic drive in Drosophila simulans: a QTL approach reveals the complex polygenic determinism of Paris drive suppression". Heredity. 122 (6): 906–915. doi:10.1038/s41437-018-0163-1. PMC   6781156 . PMID   30518968.
  14. Lin CJ, Hu F, Dubruille R, Vedanayagam J, Wen J, Smibert P, Loppin B, Lai EC (August 2018). "The hpRNA/RNAi Pathway Is Essential to Resolve Intragenomic Conflict in the Drosophila Male Germline". Developmental Cell. 46 (3): 316–326.e5. doi:10.1016/j.devcel.2018.07.004. PMC   6114144 . PMID   30086302.
  15. de Carvalho AB, Klaczko LB (November 1993). "Autosomal suppressors of sex-ratio in Drosophila mediopunctata". Heredity. 71 ( Pt 5) (5): 546–51. doi: 10.1038/hdy.1993.174 . PMID   8276637.
  16. Stalker HD (February 1961). "The Genetic Systems Modifying Meiotic Drive in Drosophila Paramelanica". Genetics. 46 (2): 177–202. doi:10.1093/genetics/46.2.177. PMC   1210188 . PMID   17248041.
  17. Jaenike J (February 1999). "Suppression of Sex-Ratio Meiotic Drive and the Maintenance of Y-Chromosome Polymorphism in Drosophila". Evolution; International Journal of Organic Evolution. 53 (1): 164–174. doi: 10.1111/j.1558-5646.1999.tb05342.x . PMID   28565182.
  18. Keais GL, Hanson MA, Gowen BE, Perlman SJ (June 2017). "X chromosome drive in a widespread Palearctic woodland fly, Drosophila testacea". Journal of Evolutionary Biology. 30 (6): 1185–1194. doi: 10.1111/jeb.13089 . PMID   28402000.