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Cross-Contamination Explains “Inter and Intraspecific Horizontal Genetic Transfers” between Asexual Bdelloid Rotifers

2018; Elsevier BV; Volume: 28; Issue: 15 Linguagem: Inglês

10.1016/j.cub.2018.05.070

1879-0445

Christopher G. Wilson, Reuben W. Nowell, Timothy G. Barraclough,

Biocrusts and Microbial Ecology

A few metazoan lineages are thought to have persisted for millions of years without sexual reproduction. If so, they would offer important clues to the evolutionary paradox of sex itself [1Judson O.P. Normark B.B. Ancient asexual scandals.Trends Ecol. Evol. 1996; 11: 41-46Abstract Full Text PDF PubMed Scopus (383) Google Scholar, 2Normark B.B. Judson O.P. Moran N.A. Genomic signatures of ancient asexual lineages.Biol. J. Linn. Soc. Lond. 2003; 79: 69-84Crossref Scopus (170) Google Scholar]. Most “ancient asexuals” are subject to ongoing doubt because extant populations continue to invest in males [3Palmer S.C. Norton R.A. Taxonomic, geographic and seasonal distribution of thelytokous parthenogenesis in the Desmonomata (Acari: Oribatida).Exp. Appl. Acarol. 1991; 12: 67-81Crossref Scopus (57) Google Scholar, 4Smith R.J. Kamiya T. Horne D.J. Living males of the ‘ancient asexual’ Darwinulidae (Ostracoda: Crustacea).Proc. Biol. 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Occurrence and morphology of a phenotypic male of a gynogenetic fish.Science. 1959; 129: 1227-1229Crossref PubMed Scopus (18) Google Scholar]. However, males are famously unknown in bdelloid rotifers, a class of microscopic invertebrates comprising hundreds of species [10Hudson C.T. Gosse P.H. The Rotifera; or Wheel-Animalcules. Longmans, Green & Co., 1886Google Scholar, 11Mark Welch D.B. Ricci C. Meselson M. Bdelloid rotifers: progress in understanding the success of an evolutionary scandal.in: Schön I. Martens K. Dijk P. Lost Sex. Springer, 2009: 259-279Crossref Scopus (42) Google Scholar, 12Birky Jr., C.W. Positively negative evidence for asexuality.J. Hered. 2010; 101: S42-S45Crossref PubMed Scopus (23) Google Scholar]. Bdelloid genomes have acquired an unusually high proportion of genes from non-metazoans via horizontal transfer [13Gladyshev E.A. Meselson M. Arkhipova I.R. 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Micklem G. Tunnacliffe A. Boschetti C. Barraclough T.G. Comparative genomics of bdelloid rotifers: Insights from desiccating and nondesiccating species.PLoS Biol. 2018; 16: e2004830Crossref PubMed Scopus (48) Google Scholar]. This well-substantiated finding has invited speculation [13Gladyshev E.A. Meselson M. Arkhipova I.R. Massive horizontal gene transfer in bdelloid rotifers.Science. 2008; 320: 1210-1213Crossref PubMed Scopus (323) Google Scholar] that homologous horizontal transfer between bdelloid individuals also may occur, perhaps even “replacing” sex [14Flot J.F. Hespeels B. Li X. Noel B. Arkhipova I. Danchin E.G.J. Hejnol A. Henrissat B. Koszul R. Aury J.-M. et al.Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga.Nature. 2013; 500: 453-457Crossref PubMed Scopus (254) Google Scholar]. In 2016, Current Biology published an article claiming to supply evidence for this idea. Debortoli et al. [18Debortoli N. Li X. Eyres I. Fontaneto D. Hespeels B. Tang C.Q. Flot J.F. Van Doninck K. Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex.Curr. Biol. 2016; 26: 723-732Abstract Full Text Full Text PDF PubMed Scopus (61) Google Scholar] sampled rotifers from natural populations and sequenced one mitochondrial and four nuclear loci. Species assignments were incongruent among loci for several samples, which was interpreted as evidence of “interspecific horizontal genetic transfers.” Here, we use sequencing chromatograms supplied by the authors to demonstrate that samples treated as individuals actually contained two or more highly divergent mitochondrial and ribosomal sequences, revealing cross-contamination with DNA from multiple animals of different species. Other chromatograms indicate contamination with DNA from conspecific animals, explaining genetic and genomic evidence for “intraspecific horizontal exchanges” reported in the same study. Given the clear evidence of contamination, the data and findings of Debortoli et al. [18Debortoli N. Li X. Eyres I. Fontaneto D. Hespeels B. Tang C.Q. Flot J.F. Van Doninck K. Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex.Curr. Biol. 2016; 26: 723-732Abstract Full Text Full Text PDF PubMed Scopus (61) Google Scholar] provide no reliable support for their conclusions that DNA is transferred horizontally between or within bdelloid species.