Artículo

Stolle, E.; Pracana, R.; Howard, P.; Paris, C.I.; Brown, S.J.; Castillo-Carrillo, C.; Rossiter, S.J.; Wurm, Y. "Degenerative Expansion of a Young Supergene" (2019) Molecular Biology and Evolution. 36(3):553-561
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Long-term suppression of recombination ultimately leads to gene loss, as demonstrated by the depauperate Y and W chromosomes of long-established pairs of XY and ZW chromosomes. The young social supergene of the Solenopsis invicta red fire ant provides a powerful system to examine the effects of suppressed recombination over a shorter timescale. The two variants of this supergene are carried by a pair of heteromorphic chromosomes, referred to as the social B and social b (SB and Sb) chromosomes. The Sb variant of this supergene changes colony social organization and has an inheritance pattern similar to a Y or W chromosome because it is unable to recombine. We used high-resolution optical mapping, k-mer distribution analysis, and quantification of repetitive elements on haploid ants carrying alternate variants of this young supergene region. We find that instead of shrinking, the Sb variant of the supergene has increased in length by more than 30%. Surprisingly, only a portion of this length increase is due to consistent increases in the frequency of particular classes of repetitive elements. Instead, haplotypes of this supergene variant differ dramatically in the amounts of other repetitive elements, indicating that the accumulation of repetitive elements is a heterogeneous and dynamic process. This is the first comprehensive demonstration of degenerative expansion in an animal and shows that it occurs through nonlinear processes during the early evolution of a region of suppressed recombination. © The Author(s) 2018.

Registro:

Documento: Artículo
Título:Degenerative Expansion of a Young Supergene
Autor:Stolle, E.; Pracana, R.; Howard, P.; Paris, C.I.; Brown, S.J.; Castillo-Carrillo, C.; Rossiter, S.J.; Wurm, Y.
Filiación:School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
Departamento Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Division of Biology, Kansas State University, Manhattan, KS, United States
Institut für Biologie, Martin-Luther-University Halle-Wittenberg, Hoher Weg 8, Halle, Germany
Palabras clave:accumulation of repetitive elements; evolution of polygyny; fire ants; genome evolution; social chromosome; article; gene frequency; genome; haplotype; human; inheritance; nonhuman; polygyny; social structure; Solenopsis; Y chromosome
Año:2019
Volumen:36
Número:3
Página de inicio:553
Página de fin:561
DOI: http://dx.doi.org/10.1093/molbev/msy236
Título revista:Molecular Biology and Evolution
Título revista abreviado:Mol. Biol. Evol.
ISSN:07374038
CODEN:MBEVE
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_07374038_v36_n3_p553_Stolle

Referencias:

  • Arunkumar, R., Josephs, E.B., Williamson, R.J., Wright, S.I., Pollen-specific, but not sperm-specific, genes show stronger purifying selection and higher rates of positive selection than sporophytic genes in Capsella grandiflora (2013) Mol Biol Evol., 30 (11), pp. 2475-2486
  • Bachtrog, D., Evidence that positive selection drives Y-chromosome degeneration in Drosophila miranda (2004) Nat Genet., 36 (5), pp. 518-522
  • Bachtrog, D., A dynamic view of sex chromosome evolution (2006) Curr Opin Genet Dev., 16 (6), pp. 578-585
  • Bachtrog, D., Expression profile of a degenerating Neo-Y chromosome in Drosophila (2006) Curr Biol., 16 (17), pp. 1694-1699
  • Bachtrog, D., The temporal dynamics of processes underlying y chromosome degeneration (2008) Genetics, 179 (3), pp. 1513-1525
  • Bachtrog, D., Y-chromosome evolution: Emerging insights into processes of Y-chromosome degeneration (2013) Nat Rev Genet., 14 (2), pp. 113-124
  • Bachtrog, D., Hom, E., Wong, K.M., Maside, X., De Jong, P., Genomic degradation of a young y chromosome in Drosophila miranda (2008) Genome Biol., 9 (2), p. R30
  • Beaudry, F.E.G., Barrett, S.C.H., Wright, S.I., Genomic loss and silencing on the y chromosomes of Rumex (2017) Genome Biol Evol., 9 (12), pp. 3345-3355
  • Bull, J.J., Sex chromosomes in haploid dioecy: A unique contrast to Muller's theory for diploid dioecy (1978) Am Nat., 112 (983), pp. 245-250
  • Campbell, R.B., Hard selection in haploid species (1982) Theor Popul Biol., 21 (1), pp. 1-10
  • Charlesworth, B., Model for evolution of y chromosomes and dosage compensation (1978) Proc Natl Acad Sci USA., 75 (11), pp. 5618-5622
  • Charlesworth, B., Sniegowski, P., Stephan, W., The evolutionary dynamics of repetitive DNA in eukaryotes (1994) Nature, 371 (6494), pp. 215-220
  • Chibalina, M.V., Filatov, D.A., Plant y chromosome degeneration is retarded by haploid purifying selection (2011) Curr Biol., 21 (17), pp. 1475-1479
  • Coelho, S.M., Gueno, J., Lipinska, A.P., Cock, J.M., Umen, J.G., UV chromosomes and haploid sexual systems (2018) Trends Plant Sci., 23 (9), pp. 794-807
  • Combadao, J., Campos, P.R.A., Dionisio, F., Gordo, I., Small-world networks decrease the speed of Muller's ratchet (2007) Genet Res., 89 (1), pp. 7-18
  • Crowson, D., Barrett, S.C.H., Wright, S.I., Purifying and positive selection influence patterns of gene loss and gene expression in the evolution of a plant sex chromosome system (2017) Mol Biol Evol., 34 (5), pp. 1140-1154
  • Devos, K.M., Brown, J.K.M., Bennetzen, J.L., Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis (2002) Genome Res., 12, pp. 1075-1079
  • Dolgin, E.S., Charlesworth, B., The effects of recombination rate on the distribution and abundance of transposable elements (2008) Genetics, 178 (4), pp. 2169-2177
  • Dolgin, E.S., Charlesworth, B., Cutter, A.D., Population frequencies of transposable elements in selfing and outcrossing Caenorhabditis nematodes (2008) Genet Res., 90 (4), pp. 317-329
  • Engelstadter, J., Muller's ratchet and the degeneration of y chromosomes: A simulation study (2008) Genetics, 180 (2), pp. 957-967
  • Felsenstein, J., The evolutionary advantage of recombination (1974) Genetics, 78 (2), pp. 737-756
  • Gotzek, D., Clarke, J., Shoemaker, D., Mitochondrial genome evolution in fire ants (Hymenoptera: Formicidae) (2010) BMC Evol Biol., 10, p. 300
  • Gotzek, D., Ross, K.G., Genetic regulation of colony social organization in fire ants: An integrative overview (2007) Q Rev Biol., 82 (3), pp. 201-226
  • Goubert, C., Modolo, L., Vieira, C., ValienteMoro, C., Mavingui, P., Boulesteix, M., De novo assembly and annotation of the Asian tiger mosquito (Aedes albopictus) repeatome with dnaPipeTE from raw genomic reads and comparative analysis with the yellow fever mosquito (Aedes aegypti) (2015) Genome Biol Evol., 7 (4), pp. 1192-1205
  • Hobza, R., Cegan, R., Jesionek, W., Kejnovsky, E., Vyskot, B., Kubat, Z., Impact of repetitive elements on the y chromosome formation in plants (2017) Genes, 8 (11), p. 302
  • Hobza, R., Lengerova, M., Svoboda, J., Kubekova, H., Kejnovsky, E., Vyskot, B., An accumulation of tandem DNA repeats on the y chromosome in Silene latifolia during early stages of sex chromosome evolution (2006) Chromosoma, 115 (5), pp. 376-382
  • Immler, S., Otto, S.P., The evolutionary consequences of selection at the haploid gametic stage (2018) Am Nat., 192 (2), pp. 241-249
  • Ishizaki, K., Multicopy genes uniquely amplified in the y chromosome-specific repeats of the liverwort Marchantia polymorpha (2002) Nucleic Acids Res., 30 (21), pp. 4675-4681
  • Jay, P., Whibley, A., Frezal, L., Cara De, A.M.R., Nowell, R.W., Mallet, J., Dasmahapatra, K.K., Joron, M., Supergene evolution triggered by the introgression of a chromosomal inversion (2018) Curr Biol., 28 (11), pp. 1839-1845. , e3
  • Joseph, S., Kirkpatrick, M., Haploid selection in animals (2004) Trends Ecol Evol., 19 (11), pp. 592-597
  • Kaiser, V.B., Charlesworth, B., The effects of deleterious mutations on evolution in non-recombining genomes (2009) Trends Genet., 25 (1), pp. 9-12
  • Kaiser, V.B., Charlesworth, B., Muller's ratchet and the degeneration of the Drosophila miranda neo-Y Chromosome (2010) Genetics, 185 (1), pp. 339-348
  • Kawakatsu, T., Huang, S.-S.C., Jupe, F., Sasaki, E., Schmitz, R.J., Urich, M.A., Castanon, R., He, Y., Epigenomic diversity in a global collection of Arabidopsis thaliana accessions (2016) Cell, 166 (2), pp. 492-505
  • Kejnovsky, E., Michalovova, M., Steflova, P., Kejnovska, I., Manzano, S., Hobza, R., Kubat, Z., Vyskot, B., Expansion of microsatellites on evolutionary young y chromosome (2013) PLoS One, 8 (1), p. e45519
  • Keller, L., Ross, K.G., Selfish genes: A green beard in the red fire ant (1998) Nature, 394 (6693), pp. 573-575
  • Kortschak, R.D., Tsend-Ayush, E., Grützner, F., Analysis of SINE and LINE repeat content of y chromosomes in the platypus, Ornithorhynchus anatinus (2009) Reprod Fertil Dev., 21 (8), pp. 964-975
  • Krasovec, M., Chester, M., Ridout, K., Filatov, D.A., The mutation rate and the age of the sex chromosomes in Silene latifolia (2018) Curr Biol., 28 (11), pp. 1832-1838. , e4
  • Krieger, M.J.B., Ross, K.G., Identification of a major gene regulating complex social behavior (2002) Science, 295 (5553), pp. 328-332
  • Krieger, M.J.B., Ross, K.G., Molecular evolutionary analyses of the odorant-binding protein gene Gp-9 in fire ants and other Solenopsis species (2005) Mol Biol Evol., 22 (10), pp. 2090-2103
  • Kubat, Z., Hobza, R., Vyskot, B., Kejnovsky, E., Microsatellite accumulation on the y chromosome in Silene latifolia (2008) Genome, 51 (5), pp. 350-356
  • Lipinska, A.P., Toda, N.R.T., Heesch, S., Peters, A.F., Cock, J.M., Coelho, S.M., Multiple gene movements into and out of haploid sex chromosomes (2017) Genome Biol., 18 (1), p. 104
  • Long, E., Evans, C., Chaston, J., Udall, J.A., Genomic structural variations within five continental populations of Drosophila melanogaster (2018) G3, 8, pp. 3247-3253
  • Mahajan, S., Kh-C, W., Nalley, M.J., Gibilisco, L., Bachtrog, D., De novo assembly of a young Drosophila y chromosome using singlemolecule sequencing and chromatin conformation capture (2018) PLoS Biol., 16 (7), p. e2006348
  • Mank, J.E., Sex chromosome dosage compensation: Definitely not for everyone (2013) Trends Genet., 29 (12), pp. 677-683
  • Ming, R., Wang, J., Moore, P.H., Paterson, A.H., Sex chromosomes in flowering plants (2007) Am J Bot., 94 (2), pp. 141-150
  • Na, J.-K., Wang, J., Ming, R., Accumulation of interspersed and sexspecific repeats in the non-recombining region of papaya sex chromosomes (2014) BMC Genomics, 15, p. 335
  • Nipitwattanaphon, M., Wang, J., Dijkstra, M.B., Keller, L., A simple genetic basis for complex social behaviour mediates widespread gene expression differences (2013) Mol Ecol., 22 (14), pp. 3797-3813
  • Nipitwattanaphon, M., Wang, J., Ross, K.G., Riba-Grognuz, O., Wurm, Y., Khurewathanakul, C., Keller, L., Effects of ploidy and sex-locus genotype on gene expression patterns in the fire ant Solenopsis invicta (2014) Proc Biol Sci., 281 (1797), p. 20141776
  • Peichel, C.L., Ross, J.A., Matson, C.K., Dickson, M., Grimwood, J., Schmutz, J., Myers, R.M., Kingsley, D.M., The master sexdetermination locus in threespine sticklebacks is on a nascent y chromosome (2004) Curr Biol., 14 (16), pp. 1416-1424
  • Pracana, R., Levantis, I., Martnez-Ruiz, C., Stolle, E., Priyam, A., Wurm, Y., Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins (2017) Evol Lett., 1 (4), pp. 199-210
  • Pracana, R., Priyam, A., Levantis, I., Nichols, R.A., Wurm, Y., The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB (2017) Mol Ecol., 26 (11), pp. 2864-2879
  • Puterova, J., Kubat, Z., Kejnovsky, E., Jesionek, W., Cizkova, J., Vyskot, B., Hobza, R., The slowdown of y chromosome expansion in dioecious Silene latifolia due to DNA loss and Male-specific silencing of retrotransposons (2018) BMC Genomics, 19, p. 153
  • Reugels, A.M., Kurek, R., Lammermann, U., Bünemann, H., Megaintrons in the dynein gene DhDhc7(Y) on the heterochromatic y chromosome give rise to the giant threads loops in primary spermatocytes of Drosophila hydei (2000) Genetics, 154, pp. 759-769
  • Rice, W.R., Sex chromosomes and the evolution of sexual dimorphism (1984) Evolution, 38 (4), p. 735
  • Rizzon, C., Marais, G., Gouy, M., Biemont, C., Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome (2002) Genome Res., 12 (3), pp. 400-407
  • Roehl, A.C., Vogt, J., Mussotter, T., Zickler, A.N., Spöti, H., Högel, J., Chuzhanova, N.A., Mautner, V.-F., Intrachromosomal mitotic nonallelic homologous recombination is the major molecular mechanism underlying type-2 NF1 deletions (2010) Hum Mutat., 31 (10), pp. 1163-1173
  • Ross, M.T., Grafham, D.V., Coffey, A.J., Scherer, S., McLay, K., Muzny, D., Platzer, M., Bird, C.P., The DNA sequence of the human X chromosome (2005) Nature, 434 (7031), pp. 325-337
  • Sandler, G., Beaudry, F.E.G., Barrett, S.C.H., Wright, S.I., The effects of haploid selection on y chromosome evolution in two closely related dioecious plants (2018) Evol Lett., 2 (4), pp. 368-377
  • Schwander, T., Libbrecht, R., Keller, L., Supergenes and complex phenotypes (2014) Curr Biol., 24 (7), pp. R288-R294
  • Shanks, M.E., May, C.A., Dubrova, Y.E., Balaresque, P., Rosser, Z.H., Adams, S.M., Jobling, M.A., Complex germline and somatic mutation processes at a haploid human minisatellite shown by single-molecule analysis (2008) Mutat Res., 648 (1-2), pp. 46-53
  • Skaletsky, H., Kuroda-Kawaguchi, T., Minx, P.J., Cordum, H.S., Hillier, L., Brown, L.G., Repping, S., Bieri, T., Themale-specific region of the human y chromosome is a mosaic of discrete sequence classes (2003) Nature, 423 (6942), pp. 825-837
  • Stevison, L.S., Hoehn, K.B., Noor, M.A.F., Effects of inversions on withinand between-species recombination and divergence (2011) Genome Biol Evol., 3, pp. 830-841
  • Sudmant, P.H., Rausch, T., Gardner, E.J., Handsaker, R.E., Abyzov, A., Huddleston, J., Zhang, Y., Mh-Y, F., An integrated map of structural variation in 2, 504 human genomes (2015) Nature, 526 (7571), pp. 75-81
  • Sun, H., Ding, J., Piednoel, M., Schneeberger, K., FindGSE: Estimating genome size variation within human and Arabidopsis using k-mer frequencies (2018) Bioinformatics, 34 (4), pp. 550-557
  • Thompson, M.J., Jiggins, C.D., Supergenes and their role in evolution (2014) Heredity, 113 (1), pp. 1-8
  • Wang, J., Jemielity, S., Uva, P., Wurm, Y., Graff, J., Keller, L., An annotated cDNA library and microarray for large-scale gene-expression studies in the ant Solenopsis invicta (2007) Genome Biol., 8 (1), p. R9
  • Wang, J., Na, J.-K., Yu, Q., Gschwend, A.R., Han, J., Zeng, F., Aryal, R., Zhang, W., Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution (2012) Proc Natl Acad Sci USA., 109 (34), pp. 13710-13715
  • Wang, J., Ross, K.G., Keller, L., Genome-wide expression patterns and the genetic architecture of a fundamental social trait (2008) PLoS Genet., 4 (7), p. e1000127
  • Wang, J., Wurm, Y., Nipitwattanaphon, M., Riba-Grognuz, O., Huang, Y.-C., Shoemaker, D., Keller, L., A Y-like social chromosome causes alternative colony organization in fire ants (2013) Nature, 493 (7434), pp. 664-668
  • Wright, A.E., Dean, R., Zimmer, F., Mank, J.E., How to make a sex chromosome (2016) Nat Commun., 7, p. 12087
  • Wright, A.E., Harrison, P.W., Montgomery, S.H., Pointer, M.A., Mank, J.E., Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosome (2014) Evolution, 68 (11), pp. 3281-3295
  • Wurm, Y., Wang, J., Riba-Grognuz, O., Corona, M., Nygaard, S., Hunt, B.G., Ingram, K.K., Gotzek, D., The genome of the fire ant Solenopsis invicta (2011) Proc Natl Acad Sci USA., 108 (14), pp. 5679-5684

Citas:

---------- APA ----------
Stolle, E., Pracana, R., Howard, P., Paris, C.I., Brown, S.J., Castillo-Carrillo, C., Rossiter, S.J.,..., Wurm, Y. (2019) . Degenerative Expansion of a Young Supergene. Molecular Biology and Evolution, 36(3), 553-561.
http://dx.doi.org/10.1093/molbev/msy236
---------- CHICAGO ----------
Stolle, E., Pracana, R., Howard, P., Paris, C.I., Brown, S.J., Castillo-Carrillo, C., et al. "Degenerative Expansion of a Young Supergene" . Molecular Biology and Evolution 36, no. 3 (2019) : 553-561.
http://dx.doi.org/10.1093/molbev/msy236
---------- MLA ----------
Stolle, E., Pracana, R., Howard, P., Paris, C.I., Brown, S.J., Castillo-Carrillo, C., et al. "Degenerative Expansion of a Young Supergene" . Molecular Biology and Evolution, vol. 36, no. 3, 2019, pp. 553-561.
http://dx.doi.org/10.1093/molbev/msy236
---------- VANCOUVER ----------
Stolle, E., Pracana, R., Howard, P., Paris, C.I., Brown, S.J., Castillo-Carrillo, C., et al. Degenerative Expansion of a Young Supergene. Mol. Biol. Evol. 2019;36(3):553-561.
http://dx.doi.org/10.1093/molbev/msy236