Nuclear genomic signals of the 'microturbellarian' roots of platyhelminth evolutionary innovation

  1. Christopher E Laumer  Is a corresponding author
  2. Andreas Hejnol
  3. Gonzalo Giribet
  1. Harvard University, United States
  2. University of Bergen, Norway

Abstract

Flatworms number among the most diverse invertebrate phyla, and represent the most biomedically significant branch of the major bilaterian clade Spiralia, but to date, deep evolutionary relationships within this group have been studied using only a single locus (the rRNA operon), leaving the origins of many key clades unclear. Here, using a survey of genomes and transcriptomes representing all free-living flatworm orders, we provide resolution of platyhelminth interrelationships based on hundreds of nuclear protein-coding genes, exploring phylogenetic signal through concatenation as well as recently developed consensus approaches. These analyses robustly support a modern hypothesis of flatworm phylogeny, one which emphasizes the primacy of the often-overlooked 'microturbellarian' groups in understanding the major evolutionary transitions within Platyhelminthes: perhaps most notably, we propose a novel scenario for the interrelationships between free-living and vertebrate-parasitic flatworms, providing new opportunities to shed light on the origins and biological consequences of parasitism in these iconic invertebrates.

Article and author information

Author details

  1. Christopher E Laumer

    Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    For correspondence
    claumer@oeb.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Andreas Hejnol

    Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  3. Gonzalo Giribet

    Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Alejandro Sánchez Alvarado, Howard Hughes Medical Institute, Stowers Institute for Medical Research, United States

Version history

  1. Received: November 5, 2014
  2. Accepted: March 6, 2015
  3. Accepted Manuscript published: March 12, 2015 (version 1)
  4. Version of Record published: April 16, 2015 (version 2)

Copyright

© 2015, Laumer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,390
    views
  • 1,024
    downloads
  • 132
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Christopher E Laumer
  2. Andreas Hejnol
  3. Gonzalo Giribet
(2015)
Nuclear genomic signals of the 'microturbellarian' roots of platyhelminth evolutionary innovation
eLife 4:e05503.
https://doi.org/10.7554/eLife.05503

Share this article

https://doi.org/10.7554/eLife.05503

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Kenneth Chiou, Noah Snyder-Mackler
    Insight

    Single-cell RNA sequencing reveals the extent to which marmosets carry genetically distinct cells from their siblings.

    1. Genetics and Genomics
    Can Hu, Xue-Ting Zhu ... Jin-Qiu Zhou
    Research Article

    Telomeres, which are chromosomal end structures, play a crucial role in maintaining genome stability and integrity in eukaryotes. In the baker’s yeast Saccharomyces cerevisiae, the X- and Y’-elements are subtelomeric repetitive sequences found in all 32 and 17 telomeres, respectively. While the Y’-elements serve as a backup for telomere functions in cells lacking telomerase, the function of the X-elements remains unclear. This study utilized the S. cerevisiae strain SY12, which has three chromosomes and six telomeres, to investigate the role of X-elements (as well as Y’-elements) in telomere maintenance. Deletion of Y’-elements (SY12), X-elements (SY12XYΔ+Y), or both X- and Y’-elements (SY12XYΔ) did not impact the length of the terminal TG1-3 tracks or telomere silencing. However, inactivation of telomerase in SY12, SY12XYΔ+Y, and SY12XYΔ cells resulted in cellular senescence and the generation of survivors. These survivors either maintained their telomeres through homologous recombination-dependent TG1-3 track elongation or underwent microhomology-mediated intra-chromosomal end-to-end joining. Our findings indicate the non-essential role of subtelomeric X- and Y’-elements in telomere regulation in both telomerase-proficient and telomerase-null cells and suggest that these elements may represent remnants of S. cerevisiae genome evolution. Furthermore, strains with fewer or no subtelomeric elements exhibit more concise telomere structures and offer potential models for future studies in telomere biology.