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

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.