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The tuatara genome: insights into vertebrate evolution from the sole survivor of an ancient reptilian order

Neil J. Gemmell, Kim Rutherford, Stefan Prost, Marc Tollis, David Winter, J. Robert Macey, David L. Adelson, Alexander Suh, Terry Bertozzi, José H. Grau, Chris Organ, Paul P. Gardner, Matthieu Muffato, Mateus Patricio, Konstantinos Billis, Fergal J Martin, Paul Flicek, Bent Petersen, Lin Kang, Pawel Michalak, Thomas R. Buckley, Melissa Wilson, Yuanyuan Cheng, Hilary Miller, Ryan K. Schott, Melissa Jordan, Richard Newcomb, José Ignacio Arroyo, Nicole Valenzuela, Tim A. Hore, Jaime Renart, Valentina Peona, Claire R. Peart, Vera M. Warmuth, Lu Zeng, R. Daniel Kortschak, Joy M. Raison, Valeria Velásquez Zapata, Zhiqiang Wu, Didac Santesmasses, Marco Mariotti, Roderic Guigó, Shawn M. Rupp, Victoria G. Twort, Nicolas Dussex, Helen Taylor, Hideaki Abe, James M. Paterson, Daniel G. Mulcahy, Vanessa L. Gonzalez, Charles G. Barbieri, Dustin P. DeMeo, Stephan Pabinger, Oliver Ryder, Scott V. Edwards, Steven L. Salzberg, Lindsay Mickelson, Nicola Nelson, Clive Stone, Ngatiwai Trust Board

Preprint posted on December 08, 2019 https://www.biorxiv.org/content/10.1101/867069v1

A genome as old as Gondwana: a recent preprint describes the huge tuatara genome, providing insights into amniote and reptile evolution.

Selected by Miguel V. Almeida

 

Background

Between 85-70 million years ago, the land mass now known as New Zealand (or Aotearoa, its Māori designation) parted from the supercontinent of Gondwana. A most notable lack of endemic mammal competitors, together with very late human colonization (it is thought that Māori people first arrived in New Zealand some 700-900 years ago), led to the extraordinary preservation of Gondwana-like fauna and flora in New Zealand. The reptile Sphenodon punctatus, also known as tuatara, is such a “living fossil” (Figure 1).

 

Figure 1. A male tuatara. Tuatara means “peaks on the back” in Māori. Picture from https://en.wikipedia.org/wiki/Tuatara

 

Tuatara are remarkably unique. These reptiles represent the only extant species of the ancient order Rhynchocephalia (Sphenodontia), which presumably originated in the Early Mesozoic, approximately 250 million years ago, and thrived throughout Gondwana. Nowadays, wild tuatara are restricted to 32 offshore islands in New Zealand, where their survival is challenged, for example, by ongoing climate change and predation by invasive mammal species. Their phylogenetic relationship amongst reptiles was ambiguous for a long time because of features shared with many groups. Nevertheless, tuatara have a set of fascinating adaptations that set them apart from other reptiles. For example, the tuatara can live for more than 100 years and have temperature-dependent sex determination (hence why climate change is a big issue). Māori find tuatara very significant, adding an extra cultural dimension to the relevance of this species. In fact, the Māori people give tuatara the status of taonga (meaning treasure) and consider them as the guardians of special places.

Now, Professor Neil J. Gemmell and colleagues report the sequencing and assembly of the tuatara genome, providing an amazing window into the past, namely into the early evolution of tetrapods, amniotes, and reptiles. Moreover, it provides an invaluable resource for the future conservation of this species.

 

Key findings

  • The tuatara genome is pretty up on the list of largest vertebrate genomes with an estimated 5 Giga base pairs (compared to 3 Giga base pairs in human).
  • Phylogenetic analysis comparing the genome of tuatara with other amniotes reveals that tuatara shared a common ancestor with snakes and lizards around 250 million years ago.
  • At least 64% of the tuatara genome is comprised of repetitive sequences, split between transposable elements (31%) and low copy number segmental duplications (33%). This high proportion of repeats is more similar to mammalian genomes, than reptilian genomes. The authors then took a closer look at the astonishing quantity and diversity of transposable elements, per family, identifying recent transposon activity and unique expansions.
  • Using post-bisulfite adaptor tagging, whole-genome DNA methylation levels of the tuatara genome were set at around 81% of methylated CpG sites, the highest DNA methylation levels of amniotes. The authors propose that these high DNA methylation levels may be a result of the high proportion of transposable elements present in the tuatara genome.
  • The authors identify ortholog and novel genes potentially related to the many adaptations of tuatara, regarding immunity, odor reception, thermal regulation, and selenium metabolism.
  • Contrary to what was previously thought, the tuatara genome is evolving relatively slowly, judging by DNA substitution rates. In fact, the tuatara genome seems to be the slowest-evolving genome amongst lepidosauria, the group including tuatara, lizards, and snakes.

 

What I like about this preprint?

In a recent visit to New Zealand, I was very happy to learn about the tuatara, an iconic animal for New Zealanders. As a fan of transposable elements, I became even happier after finding this preprint and learning about the unprecedented diversity and quantity of transposable elements present in the tuatara genome. The genome of this extraordinary animal, whose ancestors once roamed in Gondwana, will undoubtedly be a treasure-trove of great biological insights.

The somewhat sterile scientific literary style typically leaves no room for reporting more human aspects of scientific research. Another aspect I really enjoyed about this preprint is its unusual human and cultural dimension. As stated in the preprint, to perform this work, researchers had to reach out to, and work with the indigenous Māori communities, especially the Ngātiwai and Ngāti Koata, the Māori iwi (tribes) holding kaitiakitanga (guardianship) of the tuatara. Indigenous communities and researchers had to get together to clearly and transparently define the common goal: to know more about the tuatara in order to ultimately prevent its extinction.

 

Open questions

  • With the bounty of information that this genome provides, what do you think are the next steps in tuatara research?
  • With what you could already learn from its genome, which tuatara conservation strategies could be implemented? Given New Zealand’s strict conservation policies protecting its offshore islands, is reduction of inbreeding by introducing individuals from other islands an option?
  • Is there an expansion of genomically encoded DNA methyltransferase genes in tuatara? It is plausible that an unusually high number of DNA methyltransferases is required to establish the observed high levels of DNA methylation. Alternatively, there may be some more highly processive DNA methyltransferase(s).

 

Want to know more?

Tuatara: Biology and Conservation of a Venerable Survivor, Cree, 2014

 

Tuatara, Jones & Cree, 2012.

https://www.cell.com/current-biology/comments/S0960-9822(12)01303-6

 

Tags: amniote, evolution, genome sequencing, lepidosauria, new zealand, reptile, sphenodon punctatus, tetrapod, transposable elements, tuatara

Posted on: 20th December 2019

doi: https://doi.org/10.1242/prelights.15967

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