Diploid genomes of the booklouse reveal evolutionary consequences of asexuality

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Abstract

The "Meselson Effect" - a cornerstone of evolutionary theory predicting that asexual organisms accumulate mutations independently across haplotypes due to the absence of recombination - has long eluded robust empirical validation. Here, we address this gap using three high-quality diploid genome assemblies of the obligately parthenogenetic booklouse Liposcelis bostrychophila, a species characterized by apomictic meiosis and striking intraspecific variation. Combining Illumina, PacBio, and Hi-C sequencing, we generated three diploid genomes of three populations (Lb_1, Lb_2, Lb_3), revealing exceptionally high heterozygosity rates (1.67 - 3.92%) and minimal recombination - hallmarks of prolonged asexuality. Critically, in population Lb_2, intra-individual SNP divergence surpassed inter-population levels, directly demonstrating the Meselson Effect. Phylogenetic analyses of 7,029 genes revealed that while haplotypes within populations clustered as expected under sexual reproduction, nearly 15% of gene trees exhibited topologies consistent with asexual divergence - a signature of incipient Meselson-driven evolution. Comparative genomic analyses further revealed a twofold expansion of repetitive elements in asexual lineages compared to their sexual relatives (L. brunnea) and a widespread relaxation of purifying selection, particularly affecting transcription factor activities. We propose that relaxed selection on transcriptional regulators may act as a compensatory mechanism, buffering the functional consequences of escalating heterozygosity in non-recombining genomes. By integrating population genomics, phylogenomics, and selection analyses, this work not only provides the clearest evidence to date of the Meselson Effect but also establishes L. bostrychophila as a pivotal model for unraveling the genomic paradox of parthenogenesis

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