Meiotic drive

Meiotic drive is a type of intragenomic conflict, whereby one or more loci within a genome will effect 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]

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.[2] This violation of mendelian segregation was later shown to be the result of an array of Kindr genes at present on the end of chromosome 10 which induce neocentromere activity in maize knobs, causing copies of maize chromosomes carrying knobs to preferentially reach the egg cell during female meiosis.[3]

Meiotic drive in animals

The unequal inheritance of gametes has been observed since the 1950s,[4] 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.[5]

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.[6][7] 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.[8] 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.[9]

Meiotic drive in flies
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.[10]

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.[11] In Winters, the gene responsible ("Distorter on the X" or Dox) has been identified, though the mechanism by which it acts is still unknown.[12] 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.[13] Autosomal suppressors of drive are known in Drosophila mediopunctata,[14] Drosophila paramelanica,[15] Drosophila quinaria,[16] and Drosophila testacea,[17] emphasizing the importance of these drive systems in natural populations.

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See also

References
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  2. Rhoades MM (July 1942). "Preferential Segregation in Maize". Genetics. 27 (4): 395–407. PMC 1209167. PMID 17247049.
  3. 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.
  4. Sandler L, Novitski E (1957). "Meiotic Drive as an Evolutionary Force". The American Naturalist. 91 (857): 105–110. doi:10.1086/281969.
  5. 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.
  6. 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.
  7. 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.
  8. 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.
  9. 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. Lay summary – Phys.org (February 11, 2015).
  10. 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.
  11. 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.
  12. 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.
  13. 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.
  14. 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.
  15. Stalker HD (February 1961). "The Genetic Systems Modifying Meiotic Drive in Drosophila Paramelanica". Genetics. 46 (2): 177–202. PMC 1210188. PMID 17248041.
  16. 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.
  17. 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.
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