Article

Widespread maintenance of genome heterozygosity in Schmidteamediterranea

  • Nature Ecology & Evolution 1, Article number: 0019 (2016)
  • doi:10.1038/s41559-016-0019
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Abstract

Loss of heterozygosity through inbreeding or mitotic errors leads to reductions in progeny survival and fertility. Loss of heterozygosity is particularly exacerbated in geographically isolated populations, which are prone to inbreeding depression and faster rates of extinction. The regenerative capacities of the hermaphroditic biotype of the planarian Schmidtea mediterranea allowed us to perform a systematic genetic test of Mendelian segregation and study the loss of heterozygosity in the Spiralian superclade in general and planarians in particular. We discovered that ~300 Mb (~37.5%) of the genome retains heterozygosity even after ten generations of inbreeding, and show that these chromosomal regions have low diversity and recombination rates in wild populations. Our genetic and genomic analyses establish S. mediterranea as a genetically tractable system. The research also opens the door to study the evolutionary basis of non-Mendelian mechanisms, the adaptive advantages of chromosome structural heterozygotes and their potential relationship to the robust regenerative capacities of planarians.

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Acknowledgements

The authors thank D. Chao, R. Krumlauf, K. Golic, S. Hawley, T. Piotrowski, E. Jorgensen and D. Grunwald for comments, discussions and suggestions during the preparation of this manuscript. We thank H. Li, J. Vallandingham and M. Gogol for help with data analysis and visualization. We are grateful to M. Pala for the original gift in 1999 of the sexual specimens of S. mediterranea and the Stowers Institute Planarian Core facility for skilful maintenance of our planarian colony. We acknowledge S.M.C. Robb and P. Reddien for the initial establishment of the S2 line, A. Rossi for the discussions and S. Sánchez-Piotrowski for his help in specimen collection. This work was funded in part by the National Institutes of Health (NIH R37GM057260) to A.S.A.

Author information

Affiliations

  1. Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA

    • Longhua Guo
    • , Shasha Zhang
    • , Boris Rubinstein
    • , Eric Ross
    •  & Alejandro Sánchez Alvarado
  2. Molecular Biology Program, Department of Neurobiology and Anatomy, University of Utah, Salt Lake City, Utah 84112, USA

    • Longhua Guo
    •  & Alejandro Sánchez Alvarado
  3. Howard Hughes Medical Institute, Stowers Institute for Medical Research, Kansas City, Missouri 64110, USA

    • Eric Ross
    •  & Alejandro Sánchez Alvarado

Authors

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Contributions

L.G. and A.S.A. conceived and designed the project. L.G. performed the experiments and data analysis. S.Z. helped with worm culture, crosses and genotyping. E.R. helped with identifying SNPs from the (S2F5b)F6b family. L.G. and B.R. developed algorithms to analyse Mendelian inheritance in small families and performed correlation analysis. L.G. developed figures. L.G. and A.S.A. interpreted the data and prepared the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Alejandro Sánchez Alvarado.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Note, Supplementary References, Supplementary Figures 1–9

Excel files

  1. 1.

    Supplementary Table 1

    List of MI and non-MI SNPs identified

  2. 2.

    Supplementary Table 2

    Probes used in the SNPtype dynamic array

  3. 3.

    Supplementary Table 3

    Genotyping Primers used in RFLP or PCR/Sanger sequencing

  4. 4.

    Supplementary Table 4

    Genotyping raw data

Videos

  1. 1.

    Supplementary Video 1

    The mating behavior in Schmidtea mediterranea

  2. 2.

    Supplementary Video 2

    The arrested single cells in D5D/D5I unhatched egg capsules were haploid oocytes