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Abstract In asexual reproduction, meiosis must be bypassed or altered to maintain ploidy from mother to daughter without fertilization. Most of the ways meiosis can be modified to this end are expected to reduce heterozygosity within individuals; however, many asexual species are highly heterozygous. Asexual reproduction is especially common among species of microscopic, desiccation-tolerant animals such as rotifers, nematodes, and tardigrades, but the cellular and genetic mechanisms underlying asexual reproduction have not been definitively documented in any species of tardigrade. Here, we show that the asexual tardigrade Hypsibius exemplaris fails to complete the cell division of meiosis I, followed by a complete meiosis II-like division, and reproduction proceeds without detectable loss of heterozygosity. We used a combined cytological and genomic approach to characterize the mechanism of reproduction and pattern of allele inheritance in this species. Furthermore, we identified heterozygous variants in a subset of transcriptionally active genes consistent with loss of function in one allele, suggesting that maintained heterozygosity in this species allowed divergence between alleles over time. This work establishes the meiotic mechanism and inheritance pattern of reproduction in H. exemplaris, which provides a framework for interpreting genetic variation in this organism as a laboratory model. Additionally, our finding that meiosis is modified in H. exemplaris via a mechanism that maintains heterozygosity across the genome adds to a growing list of asexual animals that have evolved to reproduce clonally despite the expected long-term costs. 

Tardigrades are microscopic animals that can survive exceptional levels of ionizing radiation or desiccation—DNA-damaging conditions that would kill most animals. Irradiation or radiomimetic drug treatment of the tardigrade Hypsibius exemplaris can induce remarkably high expression levels of DNA repair genes, primarily those in the base excision repair and nonhomologous end joining pathways. How tardigrades can repair widespread DNA damage without producing frequent, large-scale chromosome structural abnormalities, like chromosome translocations and fusions, is unknown. Here, we report the results of examining chromosome and nuclear architecture throughout the cell cycle in early embryos of H. exemplaris. We found that H. exemplaris chromosomes are maintained in an individualized form throughout the cell cycle. We were surprised to also find that each chromosome is housed in a fully or partially separate lamin-lined compartment, instead of all chromosomes being housed in a single, nearly spherical nuclear lamina and envelope. Our results reveal unusual chromosomal and nuclear organization in a tardigrade. We speculate that these unexpected features might limit chromosomal rearrangements during DNA damage repair in extreme conditions.