Population genomics of sexual and asexual lineages in fissiparous ribbon worms (Lineus, Nemertea): hybridization, polyploidy and the Meselson effect.
Comparative population genetics in asexual vs. sexual species offers the opportunity to investigate the impact of asexuality on genome evolution. Here, we analyse coding sequence polymorphism and divergence patterns in the fascinating Lineus ribbon worms, a group of marine, carnivorous nemerteans with unusual regeneration abilities, and in which asexual reproduction by fissiparity is documented. The population genomics of the fissiparous L. pseudolacteus is characterized by an extremely high level of heterozygosity and unexpectedly elevated πN /πS ratio, in apparent agreement with theoretical expectations under clonal evolution. Analysis of among-species allele sharing and read-count distribution, however, reveals that L. pseudolacteus is a triploid hybrid between Atlantic populations of L. sanguineus and L. lacteus. We model and quantify the relative impact of hybridity, polyploidy and asexuality on molecular variation patterns in L. pseudolacteus and conclude that (i) the peculiarities of L. pseudolacteus population genomics result in the first place from hybridization and (ii) the accumulation of new mutations through the Meselson effect is more than compensated by processes of heterozygosity erosion, such as gene conversion or gene copy loss. This study illustrates the complexity of the evolutionary processes associated with asexuality and identifies L. pseudolacteus as a promising model to study the first steps of polyploid genome evolution in an asexual context.
Institute of Evolutionary Sciences, University Montpellier, CNRS, IRD, EPHE, Place Eugène Bataillon, 34095, Montpellier, France.|Department of Organismal Biology, Systematic Biology, Uppsala University, PO Box 256, SE-751 05, Uppsala, Sweden.
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Ament-Velásquez
Institute of Evolutionary Sciences, University Montpellier, CNRS, IRD, EPHE, Place Eugène Bataillon, 34095, Montpellier, France.
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E
Figuet
Institute of Evolutionary Sciences, University Montpellier, CNRS, IRD, EPHE, Place Eugène Bataillon, 34095, Montpellier, France.
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M
Ballenghien
Department of Biology, Indiana University, 107 S Indiana Ave, Bloomington, IN, 47405, USA.|Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St. & Constitution Ave. NW, Washington, DC, 20560, USA.
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0000-0002-9947-9036
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Zattara
Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th St. & Constitution Ave. NW, Washington, DC, 20560, USA.
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JL
Norenburg
Institut de Ciències del Mar, CSIC Barcelona, Passeig Marítim, 08003, Barcelona, Spain.
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Fernández-Álvarez
Laboratoire de Biologie Cellulaire et Moléculaire, Université de Reims Champagne-Ardenne, 9 Boulevard de la Paix, 51100, Reims, France.
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J
Bierne
Institute of Evolutionary Sciences, University Montpellier, CNRS, IRD, EPHE, Place Eugène Bataillon, 34095, Montpellier, France.
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0000-0003-1856-3197
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Bierne
Institute of Evolutionary Sciences, University Montpellier, CNRS, IRD, EPHE, Place Eugène Bataillon, 34095, Montpellier, France.
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Galtier
D000818:Animals; D005075:Biological Evolution; D004272:DNA, Mitochondrial / Q000235:genetics; D005828:Genetics, Population; D005838:Genotype; D006579:Heterozygote; D006824:Hybridization, Genetic; D007448:Invertebrates / Q000235:genetics*; D010802:Phylogeny; D011123:Polyploidy; D012098:Reproduction / Q000235:genetics; D012100:Reproduction, Asexual / Q000235:genetics; D059467:Transcriptome
D004272:DNA, Mitochondrial
clonality; coding sequences; hybridization; polyploidy; population genomics