TY - JOUR

T1 - Stepwise emergence of recombination suppression precedes fissiparous asexuality in the planarian Schmidtea mediterranea

AU - Brand, Jeremias N

AU - Patil, Ajinkya Bharatraj

AU - Pandolfini, Luca

AU - Zadesenets, Kira

AU - Rubtsov, Nikolay

AU - Robledillo, Laura

AU - Zhang, Meng

AU - Marques, André

AU - Rink, Jochen C

N1 - Brand, J.N., Patil, A.B., Pandolfini, L. et al. Stepwise emergence of recombination suppression precedes fissiparous asexuality in the planarian Schmidtea mediterranea. Nat Commun 17, 5588 (2026). https://doi.org/10.1038/s41467-026-74605-9 The authors thank Rick Kluiver, Jens Krull, Claudia Koch, and the MPI-NAT animal caretakers for worm care; Delia Niehaus, Fruzsina Ficze, and Til Schubert for DNA extractions; Fruzsina Ficze also for Hi-C preparations and COI barcoding; the IIT Genomics Facility (Diego Vozzi, Yeraldin Castillo Spelorzi, and Edoardo Henzen) for Nanopore sequencing support; Sylke Winkler and Nils Stein for supervising sequencing experiments; Tom Brown and Martin Pippel for assistance with genome assembly; Andrei Rozanski, Ferenc Kagan, and Elham Bavafaye Haghighi for bioinformatics support; Miquel Vila-Farré and Thomas Brochier for field collection support; and Leonard Drees for dsRNA production. The authors thank Leushkin Evgeny and Michael Hiller for help with the TOGA analysis. The authors also thank the Leibniz Institute of Plant Genetics and Crop Plant Research and the Dresden Concept Facilities for supporting sequencing experiments. Field collections in Menorca were conducted under GOIB permit 37077. J.N.B. was supported by the Swiss National Science Foundation (SNFS) Grant P500PB_206673. J.C.R. received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement number 649024), from the Max Planck Society, and from the German Research Foundation (DFG) graduate school GRK 2984: Evolutionary Genomics: Consequences of Biodiverse Reproductive Systems (EvoReSt) and personal project RI 2449/51. L.P. was supported by intramural funding of the Istituto Italiano di Tecnologia. K.S.Z. was supported by the Ministry of Education and Science of the Russian Federation (projects FWNR-2022-0015 and FSUS-2024-0018), and the results included in this manuscript were obtained before 24/02/2022.

PY - 2026/6/26

Y1 - 2026/6/26

N2 - A central paradox in evolutionary biology is the rarity of asexual reproduction, often attributed to developmental constraints and long-term costs. Yet, fissiparous asexuality-where animals split and regenerate-is widespread among planarians, hinting at genomic features predisposing them to asexuality. We investigate the genomic underpinnings and evolutionary consequences of asexuality in the planarian Schmidtea mediterranea, which exists as both obligately fissiparous and sexual strains. We generate a haplotype-phased genome assembly of the asexual strain and collect population genomic data to uncover extensive heterozygous chromosomal rearrangements affecting all chromosomes. We show that these rearrangements arose in a sexually reproducing ancestor without directly disrupting reproductive genes but instead progressively suppressing recombination across the genome. The asexual genome exhibits minimal deleterious mutation accumulation, indicating a low cost of asexuality. Population-genomic data indicate that persistent asexuality originated recently (0.17-0.4 Ma), however the young age is insufficient to explain the low mutational burden. Instead, planarians may exploit the lack of a single-cell bottleneck in fissiparous reproduction to mitigate the costs of asexuality. Altogether, our results are consistent with a model in which stepwise recombination suppression due to structural rearrangements eroded the benefits of sex and enabled the emergence of fissiparous asexuality in S. mediterranea.

AB - A central paradox in evolutionary biology is the rarity of asexual reproduction, often attributed to developmental constraints and long-term costs. Yet, fissiparous asexuality-where animals split and regenerate-is widespread among planarians, hinting at genomic features predisposing them to asexuality. We investigate the genomic underpinnings and evolutionary consequences of asexuality in the planarian Schmidtea mediterranea, which exists as both obligately fissiparous and sexual strains. We generate a haplotype-phased genome assembly of the asexual strain and collect population genomic data to uncover extensive heterozygous chromosomal rearrangements affecting all chromosomes. We show that these rearrangements arose in a sexually reproducing ancestor without directly disrupting reproductive genes but instead progressively suppressing recombination across the genome. The asexual genome exhibits minimal deleterious mutation accumulation, indicating a low cost of asexuality. Population-genomic data indicate that persistent asexuality originated recently (0.17-0.4 Ma), however the young age is insufficient to explain the low mutational burden. Instead, planarians may exploit the lack of a single-cell bottleneck in fissiparous reproduction to mitigate the costs of asexuality. Altogether, our results are consistent with a model in which stepwise recombination suppression due to structural rearrangements eroded the benefits of sex and enabled the emergence of fissiparous asexuality in S. mediterranea.

KW - Animals

KW - Planarians/genetics

KW - Reproduction, Asexual/genetics

KW - Recombination, Genetic

KW - Haplotypes

KW - Genome, Helminth

KW - Mutation

UR - https://www.scopus.com/pages/publications/105042974964

U2 - 10.1038/s41467-026-74605-9

DO - 10.1038/s41467-026-74605-9

M3 - Article

C2 - 42362522

VL - 17

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 5588

ER -