Diploid genomes of the booklouse reveal evolutionary consequences ofasexuality

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 uncovered a twofold expansion of repetitive elements in asexual lineages relative to their sexual relatives (L. brunnea) and 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. Significance StatementThe Meselson Effect, a theoretical prediction that asexual organisms should accumulate mutations independently in their two haplotypes, has been difficult to confirm empirically due to limited genomic data and contradictory findings in prior studies. Here, we provide strong evidence for the Meselson Effect in the parthenogenetic booklouse Liposcelis bostrychophila, using high-quality diploid genomes from three populations. We show that one population exhibits higher genetic divergence within individuals than between populations, a key signature of the Meselson Effect. Additionally, we found a possible novel compensatory mechanism for maintaining genomic stability in the face of increased heterozygosity. These findings advance our understanding of the genomic impacts under asexuality and establish L. bostrychophila as a model for studying the evolutionary consequences of parthenogenesis.