Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

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 years1. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed...

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Main Authors: Kellis, Manolis, Jaillon, Olivier
Other Authors: Massachusetts Institute of Technology. Computer Science and Artificial Intelligence Laboratory
Format: Article
Language:en_US
Published: Nature Publishing Group 2014
Online Access:http://hdl.handle.net/1721.1/87072
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author Kellis, Manolis
Jaillon, Olivier
author2 Massachusetts Institute of Technology. Computer Science and Artificial Intelligence Laboratory
author_facet Massachusetts Institute of Technology. Computer Science and Artificial Intelligence Laboratory
Kellis, Manolis
Jaillon, Olivier
author_sort Kellis, Manolis
collection MIT
description 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 years1. 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 pairing2. 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)3, 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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spelling mit-1721.1/870722022-09-28T17:37:50Z Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga Kellis, Manolis Jaillon, Olivier Massachusetts Institute of Technology. Computer Science and Artificial Intelligence Laboratory Kellis, Manolis Jaillon, Olivier 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 years1. 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 pairing2. 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)3, 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. National Science Foundation (U.S.) (grant MCB-0821956) National Science Foundation (U.S.) (NSF grant MCB-1121334) German Research Foundation (grant HA 5163/2-1) Ministry of Education and Science of the Russian Federation (grant 11.G34.31.0008) National Science Foundation (U.S.) (NSF CAREER grant number 0644282) National Science Foundation (U.S.) (NSF grant MCB-0923676) Belgian National Foundation for Scientific Research (FRFC grant 2.4.655.09.F) University of Namur (start-up grant) 2014-05-21T19:52:52Z 2014-05-21T19:52:52Z 2013-07 2012-11 Article http://purl.org/eprint/type/JournalArticle 0028-0836 1476-4687 http://hdl.handle.net/1721.1/87072 Flot, Jean-François, Boris Hespeels, Xiang Li, Benjamin Noel, Irina Arkhipova, Etienne G. J. Danchin, Andreas Hejnol, et al. “Genomic Evidence for Ameiotic Evolution in the Bdelloid Rotifer Adineta Vaga.” Nature 500, no. 7463 (July 21, 2013): 453–457. en_US http://dx.doi.org/10.1038/nature12326 Nature Creative Commons Attribution- NonCommercial-Share Alike 3.0 Unported licence. http://creativecommons.org/licenses/by-nc-sa/3.0/ application/pdf Nature Publishing Group Nature
spellingShingle Kellis, Manolis
Jaillon, Olivier
Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga
title Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga
title_full Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga
title_fullStr Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga
title_full_unstemmed Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga
title_short Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga
title_sort genomic evidence for ameiotic evolution in the bdelloid rotifer adineta vaga
url http://hdl.handle.net/1721.1/87072
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