1. Stories of the tuatara – and why they are important…
I was one of those kids who brought home every snake, bird, rodent, and bug I could get my grubby li’l hands on. My mom was incredibly patient with me. She clearly did not relish having these slithering, flapping, skittering things sullying her meticulously clean house. Aside from the thrill of the chase and the capture, her wonderfully dramatic reactions and shrieks were probably half of my motivation. But she let me keep these critters nonetheless. What an amazing mom, huh?
How I would have hyperventilated over the chance to catch a tuatara, the last living descendant of a once-dominant and unique reptile order from hundreds of millions of years ago—and completely distinct from modern lizards despite looking like one. It’s what’s under the hood that counts.
And that’s what this post is about.
In Maori – the language of New Zealand’s indigenous people – the name tuatara means spiny back which exactly describes New Zealand’s endemic reptile. According to Maori tradition, the sea god Tangaroa had a son Punga, whose son Tu-te-wanawana married Tupari and produced a great many offspring, all considered repulsive. They included sharks and insects and lizards – and tuatara. Today tuatara are valued by the indigenous people of New Zealand as taonga, or treasured possessions.
A fascinating article revealing the complete tuatara genome has just been published in the journal Nature, which is groundbreaking in more than just the research itself. The Maori people are not only among the authors (represented by the Ngatiwai Trust Board)—already well out of the ordinary—but they are the senior authors on this paper.
The tuatara and its genome are important because they are the only living links to the group of reptiles from which dinosaurs, birds, mammals, and modern reptiles all evolved. They are the only remaining descendants of a diverse reptilian order called Rhynchocephalia that thrived on the former continent of Gondwanaland. Rhynchocephalia originated in the Middle Triassic period about quarter of a billion years ago. They are a parallel branch, the closest cousins, to the Squamata which includes true lizards and snakes. And they are not repulsive.
So, understanding the tuatara genome will give us unique and potentially profound insights into the evolution of tetrapods – four-limbed animals which includes us. Deep sequencing data may also provide insights into how to preserve this species – which is unique, treasured, and endangered.
2. How to build a tuatara…
Tuatara look like small lizards, but they are quite different. For example, they have a hook on their ribs called a uncinate process which is similar to that found in birds and crocodiles and fossil amphibians, but never found in modern lizards. Tuatara uniquely have two parallel rows of teeth in their upper jaw, into which the single row of teeth in the lower jaw fits. Their eggs incubate for more than twelve months, far longer than any other reptile. Tuataras are also much better adapter for cold than lizards, and their maximal activity is somewhere between 16-20C.
Other unique features of tuatara include extreme longevity (at least 80 years in the wild and over 100 years in captivity). Their eyes are remarkably adapted for nocturnal hunting, and unlike most nocturnal animals, their retinas are structured for good night-time color vision. The tuatara skull has a number of unique features which show their relation to ancient Rhynchocephalia, and difference from modern lizards. The most characteristic is the beak shape created by the front teeth that gave the group its name (Rhynchocephalia = beak-headed).
3. Looking inside a tuatara’s genome…
The tuatara has 18 pairs of chromosomes compared to humans with 23 pairs. The genome size (the number of letters in the DNA code in half of the paired chromosomes) is 5 billion letters for the tuatara, compared to 3.3 billion for the human. The tuatara has about 1.5 times as much genomic content as humans.
One of the main reasons for sequencing unique animals like the tuatara is to determine or confirm the phylogenetic tree, the evolutionary tree showing how current and extinct species are related. This new tuatara sequencing analysis confirms previous trees showing that Rhynchocephalians originated about 250-240 million years ago.
One of the fascinating details of a genome is how much apparent junk is in there. I say apparent junk because we don’t really know the purpose of most of the genome and some therefore assume it is junk. Why? The majority of the human genome (and of many other species) is comprised of repeat sequences. If you read an article mostly filled with “chromosome chromosome chromosome…”, you would probably guess that the repeats are junk and can be ignored. That is what we see filling up most of the human genome. The human genome contains more than 50% repeat elements. In biology, unlike in literature, we can’t be sure that repeats are junk.
The largest fraction of repeat elements in the human genome are transposable elements, sometimes called jumping genes. Transposable elements were discovered in corn in the late 1940s and early 1950s by Barbara McClintock while she was at Cold Spring Harbor Laboratory in New York. Her discovery was resisted or ignored by biologists for decades before it was finally accepted and shown to exist in all forms of life from bacteria to humans. Of the human transposable elements, LINEs (long interspersed elements) are the most prevalent, taking up over 20% of the human genome. All the various transposable elements together take up about 45% of the human genome.
This new study found that the tuatara genome is at least 64% repeat elements, about half of which is transposable elements. The interesting thing is that the type of transposable elements in tuatara is more similar to mammalian elements than to reptilian elements.
Meanwhile, other types of transposable elements common in lizards and birds today are not found in tuatara. One subfamily of transposable elements found in tuatara is absent from other reptiles but is common in the only two living examples of primitive mammals called monotremes, the platypus and echidna.
Some repeat elements found in tuatara called SINEs (short interspersed elements) are found in all amniotes (mammals, reptiles, and birds). A subfamily of these SINEs is called MIRs (mammalian-wide interspersed elements). Humans have hundreds of fossil (non-functional) MIRs which have found other uses in regulation of our DNA. But in the tuatara, these MIRs are active and may have recently modified the tuatara’s regulatory sequences.
About a third of the tuatara genome is comprised of what are called low-copy-number segmental duplications, which is where the DNA has mistakenly copied a large segment of DNA that may or may not contain a number of functional genes. Segmental duplications are one of the ways that major evolutionary changes can quickly occur. And in the tuatara, a major portion of its genome is composed of these types of random duplications. This results in the tuatara’s genome being about 2.4 times larger than the anole’s (a small lizard).
There are several reasons to focus on repeat elements in a genome.
First, the types and sequences of repeat elements provide direct evidence of evolutionary relationships with other species, and infers the relationships to ancestral species as well. We learned here that tuatara are indeed distinct from any other species alive today, with a blend of repeats formerly thought of as unique to reptiles or mammals. This confirms that the tuatara derives from an ancestral lineage at the root of the reptilian and mammalian branches.
Second, active repeats are known to influence the evolution of a species. And what we learned is that the tuatara has a large number of active transposable elements from which we infer that the species has recently seen functional modification of its genome.
4. Shiny new things in the tuatara genome…
One of the things we always want to see inside an animal’s genome is what makes the species novel or different. The tuatara doesn’t disappoint.
The tuatara is a very visual nocturnal predator. Most nocturnal animals lose the genes associated with daytime vision. The tuatara, in contrast, shows the lowest loss of vision genes of any amniote.
Tuatara odor receptor genes suggest a scent repertoire similar to birds and a reliance on smell for hunting and mating. Similarly, their genes for thermoregulation reflect the fact that tuatara have the lowest optimal temperature for any reptile.
Tortoises are the longest-lived reptile, but tuatara are right up there with them, able to live over 100 years. This may be due to genes that protect against free radicals, or reactive oxygen species. One group of such genes are selenoproteins. Humans have 25 selenoproteins, and the tuatara genome contains 26.
Tuatara also have a unique way that their eggs determine sex. High temperature incubation of eggs leads to male offspring. There are no clear sex chromosomes, and no observable sex-specific differences in the genome. Some tuatara genes are similar to those known to act in other animals in temperature-dependent sex determination and related processes.
5. Evolution of the tuatara…
This genome analysis confirms the fossil data and suggests that amniotes appeared about 312 million years ago and split into two groups: synapsids (including mammals) and sauropsids (including birds and reptiles).
The sauropsids in turn gave rise to two branches, archosaurs (including birds, crocodiles, and turtles), and lepidosaurs (including lizards, snakes, and tuatara).
The lepidosaurs, about 250 million years ago, split into squamata (lizards and snakes), and the once-diverse rhynchocephalian. The rhynchocephalian group has only one surviving member today, the tuatara.
The molecular rate of evolution in the tuatara was found to be extremely slow, especially compared to lizards and snakes. The tuatara had long been tagged with the mistaken moniker of a living fossil, because it looked almost exactly like fossils from hundreds of millions of years ago. The molecular rate of change seems to be in alignment with the slow change in the tuatara’s form. In contrast, amniotes in general seem to undergo rapid “punctuated evolution” characterized by rapid evolutionary change followed by periods of relative stasis.
A fascinating bit of analysis in this paper is the reconstruction of the population demographics based on the sequences from less than a dozen individuals from three distinct populations of tuatara. This showed a number of population crashes and recoveries (including one 10 million years ago) that agrees with the known geological history of New Zealand and sea-level changes.
This population genomics data will also provide guidance for conservation efforts to preserve this endangered species.
6. Evolution of human relations…
Perhaps one of the most surprising things about this study was not technical at all. It was the close collaboration between this international team of scientists and representatives of the indigenous Maori. The Maori were represented on the paper by Clive Stone and the Ngatiwai Trust Board, and placed as the senior authors of this paper, published in the prestigious journal Nature.
Scientists have a checkered history, with soaring accomplishments of human imagination and ingenuity one moment, counter-balanced with grim abuse of subjects and victims. The Tuskegee syphilis study on African American men is just one example of many in which lack of patient consent, full disclosure, competent treatment, and humane consideration combined into a horrific decade-long abuse of fellow humans under the guise of scientific research.
This genomic study of a small reptile has pioneered a way to improve relations of scientists with indigenous people, yet another long-abused minority. The research team involved the Maori in all decisions about the use of genome data from an animal native to their land. The authors even provide a template agreement for others to use in similar situations.
The protection of the last remaining species of a once dominant order, and an evolutionary step in human relations. That’s beautiful science.
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