Nuclear migration through ring canals and its role in clonal reproduction in unisexual whiptail lizards Aspidoscelis
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Abstract
Asexual reproduction is often seen as a "dead end" in evolutionary terms. However, parthenogenetic species of whiptail lizards in the genus Aspidoscelis are remarkable in their unique speciation through clonal reproduction. Multiple hybridization events have led to polyploid all-female lineages that maintain high levels of heterozygosity over generations. Adaptations in oogenesis, to produce ploidy-elevated oocytes, enable the production of unreduced eggs in the absence of male fertilization. In this study we present evidence of a series of events that facilitate the migration of whole nuclei through ring canals during Prophase I in Aspidoscelis lizards. This process results in allopolyploid oocytes, which allow for the pairing of identical chromosomes thus enabling the continuation of meiosis. The described observation is a well-known phenomenon in the plant kingdom, known as cytomixis, and can be seen as conserved strategy for clonal reproduction in asexual species. Our investigations into the co-localization patterns of SCP1 and SCP3—two major components of the synaptonemal complex—in pachytene-like and diplotene oocytes provide strong evidence for the necessity of nuclear migration events occurring prior to synapsis in parthenogenetic species with distinct genome compositions. This was confirmed in the diploid A. neomexicanus, triploid A. uniparens, and tetraploid A. townsendae. Furthermore, we demonstrate that in cases of a more “balanced” genome, comprising of two genomes each of the parental species, ploidy elevation is not always necessary. This is evidenced by the presence of non-ploidy-elevated diplotene oocytes in tetraploid Sono. As a consequence, a rare instance of ploidy loss from 4N to 2N within one generation due to the development of a non-elevated oocyte through meiosis was detected. Additionally, we noted chromosome abnormalities in another Sono individual, suggesting a transition from 4N to 3N. We hypothesize that atypical synapsis patterns between similar but non-identical homeologous chromosomes in Sono may result in an unequal distribution of genes or chromosome fragments in this individual. Overall, this study reveals a mechanism of nuclear migration, which allows for identical chromosome pairing in parthenogenetic Aspidoscelis lizards to produce offspring with maintained heterozygosity over generations. Furthermore, the study points out the influence of genome composition for meiosis and offspring.