Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards

Abstract

Although bisexual reproduction has proven to be highly successful, parthenogenetic all-female populations occur frequently in certain taxa, including the whiptail lizards of the genus Aspidoscelis. Allozyme analysis revealed a high degree of fixed heterozygosity in these parthenogenetic species1,2, supporting the view that they originated from hybridization events between related sexual species. It has remained unclear how the meiotic program is altered to produce diploid eggs while maintaining heterozygosity. Here we show that meiosis commences with twice the number of chromosomes in parthenogenetic versus sexual species, a mechanism that provides the basis for generating gametes with unreduced chromosome content without fundamental deviation from the classic meiotic program. Our observation of synaptonemal complexes and chiasmata demonstrate that a typical meiotic program occurs and that heterozygosity is not maintained by bypassing recombination. Instead, fluorescent in situ hybridization probes that distinguish between homologues reveal that bivalents form between sister chromosomes, the genetically identical products of the first of two premeiotic replication cycles. Sister chromosome pairing provides a mechanism for the maintenance of heterozygosity, which is critical for offsetting the reduced fitness associated with the lack of genetic diversity in parthenogenetic species.

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Figure 1: Oocytes from parthenogenetic A. tesselata contain twice the amount of chromosomal DNA compared to sexual A. gularis.
Figure 2: Visualization of chiasmata and synaptonemal complexes in parthenogenetic A. tesselata and sexual A. tigris.
Figure 3: Meiosis in sexual and parthenogenetic Aspidoscelis species.
Figure 4: Internal telomeric repeats distinguish homologues in A. neomexicana and demonstrate sister chromosome pairing.

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Acknowledgements

We thank the staff of the Reptile Facility for their dedication to animal husbandry; C. Painter and his colleagues at the New Mexico Department of Game and Fish for scientific collection permits; F. Li for electron microscopy; the Stowers Institute Microscopy, Cytometry and Molecular Biology Facilities for support; and S. Hawley, J. Cole, C. Townsend and members of the Baumann and Blanchette laboratories for discussions and comments. We also thank S. Hawley for critical reading of the manuscript. This work was funded by the Stowers Institute for Medical Research, and the Pew Scholars Program in the Biological Sciences sponsored by the Pew Charitable Trusts. P.B. is an Early Career Scientist with the Howard Hughes Medical Institute.

Author Contributions A.A.L., W.B.N., D.P.B. and P.B. contributed extensively to the work presented in this paper. W.W. performed, and provided training in, microscopy and image data quantification.

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Correspondence to Peter Baumann.

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Supplementary Information

This file contains Supplementary Figures 1-3 with Legends and Supplementary Table 1. (PDF 1933 kb)

Supplementary Movie 1

This movie file shows an animation of the rendered chromosomes shown in Supplementary Figure 1b (see Supplementary Information file). (AVI 4740 kb)

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Lutes, A., Neaves, W., Baumann, D. et al. Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature 464, 283–286 (2010). https://doi.org/10.1038/nature08818

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