Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

J.-F. Flot, B. Hespeels, X. Li, B. Noel, I. Arkhipova, E.G.J. Danchin, A. Hejnol, B. Henrissat, R. Koszul, J.-M. Aury, V. Barbe, R.-M. Barthélémy, J. Bast, G.A. Bazykin, O. Chabrol, A. Couloux, M. Da Rocha, C. Da Silva, E. Gladyshev, P. GouretO. Hallatschek, B. Hecox-Lea, K. Labadie, B. Lejeune, O. Piskurek, J. Poulain, F. Rodriguez, J.F. Ryan, O.A. Vakhrusheva, E. Wajnberg, B. Wirth, I. Yushenova, M. Kellis, A.S. Kondrashov, D.B.M. Welch, P. Pontarotti, J. Weissenbach, P. Wincker, O. Jaillon, K. Van Doninck

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Résumé

Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873), and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.
langue originaleAnglais
Pages (de - à)453-457
Nombre de pages5
journalNature
Volume500
Numéro de publication7463
Date de mise en ligne précoce21 juil. 2013
Les DOIs
étatPublié - 22 août 2013

Empreinte digitale

Meiosis
Chromosomes
Genome
Genes
Chromosome Pairing
Gene Conversion
DNA Transposable Elements
Tetraploidy
Carbohydrate Metabolism
Oocytes
Reproduction

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Flot, J.-F. ; Hespeels, B. ; Li, X. ; Noel, B. ; Arkhipova, I. ; Danchin, E.G.J. ; Hejnol, A. ; Henrissat, B. ; Koszul, R. ; Aury, J.-M. ; Barbe, V. ; Barthélémy, R.-M. ; Bast, J. ; Bazykin, G.A. ; Chabrol, O. ; Couloux, A. ; Da Rocha, M. ; Da Silva, C. ; Gladyshev, E. ; Gouret, P. ; Hallatschek, O. ; Hecox-Lea, B. ; Labadie, K. ; Lejeune, B. ; Piskurek, O. ; Poulain, J. ; Rodriguez, F. ; Ryan, J.F. ; Vakhrusheva, O.A. ; Wajnberg, E. ; Wirth, B. ; Yushenova, I. ; Kellis, M. ; Kondrashov, A.S. ; Welch, D.B.M. ; Pontarotti, P. ; Weissenbach, J. ; Wincker, P. ; Jaillon, O. ; Van Doninck, K. / Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Dans: Nature. 2013 ; Vol 500, Numéro 7463. p. 453-457.
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title = "Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga",
abstract = "Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873), and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3{\%} of the assembled sequence. Furthermore, 8{\%} of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.",
author = "J.-F. Flot and B. Hespeels and X. Li and B. Noel and I. Arkhipova and E.G.J. Danchin and A. Hejnol and B. Henrissat and R. Koszul and J.-M. Aury and V. Barbe and R.-M. Barth{\'e}l{\'e}my and J. Bast and G.A. Bazykin and O. Chabrol and A. Couloux and {Da Rocha}, M. and {Da Silva}, C. and E. Gladyshev and P. Gouret and O. Hallatschek and B. Hecox-Lea and K. Labadie and B. Lejeune and O. Piskurek and J. Poulain and F. Rodriguez and J.F. Ryan and O.A. Vakhrusheva and E. Wajnberg and B. Wirth and I. Yushenova and M. Kellis and A.S. Kondrashov and D.B.M. Welch and P. Pontarotti and J. Weissenbach and P. Wincker and O. Jaillon and {Van Doninck}, K.",
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doi = "10.1038/nature12326",
language = "English",
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pages = "453--457",
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Flot, J-F, Hespeels, B, Li, X, Noel, B, Arkhipova, I, Danchin, EGJ, Hejnol, A, Henrissat, B, Koszul, R, Aury, J-M, Barbe, V, Barthélémy, R-M, Bast, J, Bazykin, GA, Chabrol, O, Couloux, A, Da Rocha, M, Da Silva, C, Gladyshev, E, Gouret, P, Hallatschek, O, Hecox-Lea, B, Labadie, K, Lejeune, B, Piskurek, O, Poulain, J, Rodriguez, F, Ryan, JF, Vakhrusheva, OA, Wajnberg, E, Wirth, B, Yushenova, I, Kellis, M, Kondrashov, AS, Welch, DBM, Pontarotti, P, Weissenbach, J, Wincker, P, Jaillon, O & Van Doninck, K 2013, 'Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga', Nature, VOL. 500, Numéro 7463, p. 453-457. https://doi.org/10.1038/nature12326

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. / Flot, J.-F.; Hespeels, B.; Li, X.; Noel, B.; Arkhipova, I.; Danchin, E.G.J.; Hejnol, A.; Henrissat, B.; Koszul, R.; Aury, J.-M.; Barbe, V.; Barthélémy, R.-M.; Bast, J.; Bazykin, G.A.; Chabrol, O.; Couloux, A.; Da Rocha, M.; Da Silva, C.; Gladyshev, E.; Gouret, P.; Hallatschek, O.; Hecox-Lea, B.; Labadie, K.; Lejeune, B.; Piskurek, O.; Poulain, J.; Rodriguez, F.; Ryan, J.F.; Vakhrusheva, O.A.; Wajnberg, E.; Wirth, B.; Yushenova, I.; Kellis, M.; Kondrashov, A.S.; Welch, D.B.M.; Pontarotti, P.; Weissenbach, J.; Wincker, P.; Jaillon, O.; Van Doninck, K.

Dans: Nature, Vol 500, Numéro 7463, 22.08.2013, p. 453-457.

Résultats de recherche: Contribution à un journal/une revueArticle

TY - JOUR

T1 - Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

AU - Flot, J.-F.

AU - Hespeels, B.

AU - Li, X.

AU - Noel, B.

AU - Arkhipova, I.

AU - Danchin, E.G.J.

AU - Hejnol, A.

AU - Henrissat, B.

AU - Koszul, R.

AU - Aury, J.-M.

AU - Barbe, V.

AU - Barthélémy, R.-M.

AU - Bast, J.

AU - Bazykin, G.A.

AU - Chabrol, O.

AU - Couloux, A.

AU - Da Rocha, M.

AU - Da Silva, C.

AU - Gladyshev, E.

AU - Gouret, P.

AU - Hallatschek, O.

AU - Hecox-Lea, B.

AU - Labadie, K.

AU - Lejeune, B.

AU - Piskurek, O.

AU - Poulain, J.

AU - Rodriguez, F.

AU - Ryan, J.F.

AU - Vakhrusheva, O.A.

AU - Wajnberg, E.

AU - Wirth, B.

AU - Yushenova, I.

AU - Kellis, M.

AU - Kondrashov, A.S.

AU - Welch, D.B.M.

AU - Pontarotti, P.

AU - Weissenbach, J.

AU - Wincker, P.

AU - Jaillon, O.

AU - Van Doninck, K.

PY - 2013/8/22

Y1 - 2013/8/22

N2 - Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873), and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.

AB - Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873), and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.

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DO - 10.1038/nature12326

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JO - Nature

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