Sight without eyes

By Lauren Sumner-Rooney, Research Fellow

Vision is among the most important innovations in animal evolution. The ability to see predators, prey, mates, and the environment transformed the way animals interact with each other and the world around them. Eyes can take many different forms, but this month saw the description of a visual system unlike almost any other known to science, found in a brittle star called Ophiocoma wendtii.

Brittle stars are marine invertebrates related to starfish. They have long, slender arms connected to a central disk, but no head, no brain, and – so we thought – no eyes. But recent experiments have shown that some brittle stars are able to see the world around them.

Ophiocoma wendtii is a common species found throughout the Caribbean Sea and the Gulf of Mexico. If you rummage around in coral rubble in shallow water, you’ll probably find Ophiocoma hiding underneath rocks and other debris, sheltering from their fishy predators. It has beautiful bright red tube feet (small, water-filled tentacles) and a neat party trick: it changes colour. During the day, the animals are a deep reddish-brown colour, but after dark they become beige with dark stripes.

The red brittle star, Ophiocoma wendtii

For more than thirty years, O. wendtii has been something of a mystery to scientists like myself who are interested in animal vision. It’s covered in light-sensing cells – thousands of them – and it hates being exposed to bright light, quickly dashing for cover if possible. However, it’s possible to head for dark, shadowy places without vision; you only need to be able to tell that one direction is brighter than the other. So, with a team of colleagues from Germany, Sweden and the USA, we set about giving the brittle stars an eye-test.

Lauren Sumner-Rooney, collecting specimens of Ophiocoma wendtii. Image: Jane Weinstock

We know that when they’re exposed to sunlight, O. wendtii try to hide underneath nearby rocks or other objects, so we designed a circular arena with a stimulus printed on one side – the idea is that the stimulus might resemble an object under which the animals can shelter, and the animal will move towards it.

We ran three experiments, changing the stimulus and background of the arena in each to test whether the brittle star can just see relative light or dark areas, or whether it can resolve finer points of contrast. To my surprise, O. wendtii moved towards the stimuli in all three experiments significantly more frequently than expected by random chance, as you can see in the video below. This was super exciting, as it represents not only the very first evidence of vision in these animals, but the second known example of any animal that can ‘see’ without having eyes (the first is a close relative, a sea urchin).

While O. wendtii is known to shelter during the day, we were also curious to test its behaviour at night. Running the same experiments again in natural darkness, we found that animals no longer moved towards any of the stimuli. There could be a whole number of reasons behind this, so we devised tests that eliminated several possibilities, and were left with a remaining explanation that the animal’s colour-change between night and day was somehow responsible.

Close-up of the arm plates of Ophiocoma wendtii

Colour-changing in the brittle star is controlled by the expansion and contraction of cells, called chromatophores, that are filled with pigment granules. These sit inside pores in the skeleton, alongside the light-sensing cells. During the day, the chromatophores expand, pushing up through the pores and spreading over the body surface. The pigment is spread over the outside of the animal, which looks dark brown as a result. During the night, the chromatophores contract, bringing all the pigment granules back inside the skeleton and giving a paler appearance.

The red brittle star, Ophiocoma wendtii. Image: Heather Stewart

We thought that during the day the pigment granules surrounding the light-sensing cells might block light reaching them from most directions. To test this, we constructed digital models of the visual system, creating 3D models of the light-sensing cells, the skeleton, and the pigment granules.

We found that in light-adapted systems, those with pigment, light could only reach the sensory cells from an angle of around 60° out of 360° which, though probably very coarse, could support vision. By removing the pigment from the models, vision was made impossible, as light could reach the sensory cells from too many different directions. It looked as though it was the chromatophores that made all the difference.

This is the first proposed example of whole-body colour change enabling and disabling vision in any animal, and raises many new questions about image formation and information processing. There are exciting parallels with the only other example of ‘extraocular’ (=without eyes) vision, the sea urchin we mentioned earlier: these sea urchins can also change colour in response to light levels, using similar chromatophores. Have they independently evolved a similar trick?

Top image: Heather Stewart

On the trail of the Piltdown hoax

The latest display in our single-case Presenting… series takes a look at the famous Piltdown Man hoax, and Life Collections manager Mark Carnall tells us how the display came about…

Visiting researchers to the zoology collections at the Museum often give us an excuse to dig deeper into our own material, and one such recent enquiry led me into the intriguing story of the Piltdown Man hoax.

Professor Andrew Shortland from Cranfield University contacted us to enquire about the Piltdown Man material in our collections, as part of research for a book on hoaxes and forgeries in anthropology that he is writing with Professor Patrick Degryse of KU Leuven.

I knew we had some Piltdown material here thanks to this page written by Malgosia Nowak-Kemp, but I hadn’t had an excuse to investigate any further. The enquiry was also timely as we’d just transferred a collection of palaeoanthropology casts, models and reconstructions from our Earth collections to bring our human collections into one place. I knew from our move project team that there was some Piltdown material awaiting processing – perfect.

For those who don’t know the Piltdown Man story, a short history is in order. In the early 20th century, amateur fossil hunter Charles Dawson brought a collection of human remains excavated from gravel pits in Sussex to the attention of Arthur Smith Woodward, then Keeper of Geology at the British Museum (Natural History). Woodward and Dawson collected further material and presented the remains as those of Eoanthropus dawsoni (‘Dawson’s dawn man’), an important fossil human from Britain.

Group portrait of the Piltdown skull being examined. Back row (from left): F. O. Barlow, G. Elliot Smith, Charles Dawson, Arthur Smith Woodward. Front row: A. S. Underwood, Arthur Keith, W. P. Pycraft, and E. Ray Lankester. Charles Darwin looks on from a portrait on the wall. Image via Wikipedia.
R.F. Damon-produced endocast and associated label recording the presentation of this specimen to the Museum by Arthur Smith Woodward

The discovery looked set to put Britain on the map when it came to evidence of human evolution, but suspicions were quickly raised about the authenticity of the material. Such was the skill of the forgery – meticulous breaking, abrading and staining of various archaeological and historic specimens – that it wasn’t until dating techniques, chemical analyses and some experimental palaeoanthropology in 1953 that the hoax was conclusively put to bed.

In turned out that the Piltdown ‘remains’ were a mix of medieval bone, an orangutan jaw, and chimpanzee teeth maltreated to look like an evolutionary intermediate between humans and other apes.

For 40 years or so the hoax refused to go away and numerous casts, models and reconstructions of Piltdown Man were made, sold, exchanged and gifted to museums and universities. These included casts of the original material as well as reconstructions of the skull and even reconstructions of the endocast – a cast of the inside of the skull.

The Museum has a selection of this material, but as Professor Shortland examined the collections, two specimens stood out.

The first is an R. F. Damon-produced endocast presented to the Museum by Arthur Smith Woodward himself. Smith Woodward was known as an expert on fossil fish but published widely on zoological topics. As a scientist of some repute there’s been long-standing speculation about his role in the hoax. Was he wholly duped by Dawson, or was he in on the hoax from the beginning? If it’s the former, then the presentation of this endocast shows Smith Woodward disseminating research he presumably took some pride in. If it’s the latter, perhaps it was a way of cementing the hoax as legitimate by spreading specimens far and wide.

Joseph Weiner’s experimental fake created by modifying an orangutan jaw, alongside a cast of the Piltdown jaw

The second significant specimen is a worked orangutan jaw produced by Joseph Weiner, one of the three authors who debunked the hoax in a 1953 Nature paper titled The Solution of The Piltdown Problem. Weiner modified the orangutan jaw to replicate the original hoax specimen. Thanks to Professor Shortland’s knowledge of the hoax, he sent through a copy of Weiner’s book on the Piltdown Man where this exact specimen is pictured.

The Piltdown Man hoax wasn’t the first and certainly won’t be the last hoax, fake or forgery in the history of science, but it remains one of the most well-known and stands as a warning of the dangers of hubris in the discovery and description of the natural world.

The Weiner jaw and Damon endocast will be on display alongside other Piltdown Man material in our Presenting… case from 9 January to 8 March 2020.

Abigail Harris - artwork showing reconstruction of Cambrian ocean animal life

Cambrian creation

Abigail Harris - artwork showing reconstruction of Cambrian ocean animal life

by Abigail Harris

Over the past few months our researchers have been working with University of Plymouth illustration student Abigail Harris, who has delved into the weird and wonderful world of some of the earliest animals. Here, Abigail tells us about the process that led to the creation of her Cambrian artwork, inspired by our First Animals exhibition.

I first visited the Museum in April this year when I was given the opportunity to collaborate with scientists as part of a module in my BA in at the University of Plymouth. Things kicked off with a short talk about the Ediacaran and Cambrian geological periods, when Earth’s first animal life started to appear.

I quickly narrowed my interest down to fossils from the Cambrian period which are more complex life forms, more similar to life today. A collection of small fossils from the Chengjiang fossil site in Yunnan province, China was the inspiration for some initial observational drawings.

Abigail Harris - sketches for artwork showing reconstruction of Cambrian ocean animal life
A sketchbook page showing initial sketches and observations of Onychodictyon
Final illustration of Cotyledion

After returning to Plymouth University, I began to develop these initial sketches and observations, continuing to research the Chengjiang material and learning more about the characteristics of some of the creatures preserved as fossils.

I wanted to create an under-the-sea ecology reconstruction showing a diversity of life forms, focusing on Onychodictyon, Cotyledion, Cricocosmia, Luolishania, and Paradiagoniella.

A five-step process was used for each reconstruction. Initially, I would sketch the fossil as I saw it, then I would research the characteristics and features of that animal, making a list of things to include in my drawing. A second drawing would then include all of these characteristics, not just what was initially visible in the fossil.

These rough sketches were then sent to the scientists for feedback, helping me to redraw and paint the illustrations with watercolour, before scanning and digitally editing each painting. Lastly, I created a background and added my illustrations.

Initial under under the sea ecology reconstruction.

Although the reconstructions were not completely finished by the time of my project deadline, I returned to the Museum in July and was given a tour of the First Animals exhibition by Deputy Head of Research Imran Rahman, as well as the opportunity to discuss how to improve my artworks for accuracy.

Another round of sketching and painting led to the final piece, shown at the start of this article, complete with an added digital background of the seafloor, and darkened to reflect the murky world of a Cambrian ocean, 50 metres below the surface.

Exceptional Chinese fossils come to Oxford in new partnership

by Imran Rahman, Deputy Head of Research

China is world-famous for its unique and exceptionally preserved fossils, which range from some of the oldest animals on Earth, to spectacular feathered dinosaurs. We are therefore very excited to announce that the Museum, along with other institutions from across Europe, is a partner in a major new venture with Yunnan University in China: the International Joint Laboratory for Palaeobiology and Palaeoenvironment.

Collaboration between this Museum and Yunnan University dates back to the 1990s, driven by the work of Professor Derek Siveter – a former Senior Research Fellow and current Honorary Research Associate at the Museum. He collaborated with Professor Hou Xianguang, director of the International Joint Laboratory for Palaeobiology and Palaeoenvironment, to study fossils from the internationally renowned Chengjiang biota, which was discovered by Hou Xianguang in 1984.

Museum researchers Duncan Murdock, Jack Matthews and Derek Siveter (l-r) visit the Precambrian-Cambrian Section

The Chengjiang fossil site is important and exciting because it preserves both the soft and hard parts of a range of early animals. This fossil record captures the rapid diversification of life about 520 million years old – in an event referred to as the Cambrian explosion. Derek Siveter was instrumental in a successful bid to have the Chengjiang biota designated a UNESCO World Heritage site in 2012, preserving it for future generations.

In December 2018, Museum researchers Duncan Murdock, Imran Rahman and Jack Matthews travelled with Derek to Kunming, China, for the first meeting of the International Joint Laboratory for Palaeobiology and Palaeoenvironment. The lucky researchers spent three days on field trips to the region’s most spectacular fossil sites, including Lufeng World Dinosaur Valley and the Chengjiang biota itself, followed by two full days of scientific talks and discussions.

The International Joint Laboratory is funded by the Ministry for Education of China and includes the University of Leicester, the Natural History Museum, London, the University of Munich, and the Bavarian State Collection of Zoology, along with Oxford University Museum of Natural History and Yunnan University.

The arthropod Haikoucaris ercaiensis. Sometimes referred to as a ‘short-great-appendage’ arthropod, Haikoucaris had a pair of prominent grasping appendages adjacent to the head (right-hand side of this image). Credit: Scott Billings
The arthropod Leanchoilia illecebrosa. Sometimes referred to as a ‘short-great-appendage’ arthropod, Leanchoilia illecebrosa had a pair of prominent grasping appendages adjacent to the head (right-hand side of this image). Credit: Scott Billings

A significant first outcome of this new partnership will be the loan of iconic Chengjiang fossil specimens from Kunming to Oxford for our First Animals exhibition which opens on 12 July and runs until February 2020. Most of these fossils have never been outside of China before, and some have never been seen by the public before. We invite you to visit First Animals to see these exceptional fossils first hand!

The arthropod Saperion glumaceum. Saperion had a flattened, segmented body and jointed appendages (not visible in this specimen). Credit: Scott Billings.
The arthropod Saperion glumaceum. Saperion had a flattened, segmented body and jointed appendages (not visible in this specimen). Credit: Scott Billings.

Top image: The comb jelly Galeactena hemispherica. Unlike modern comb jellies, which are soft-bodied animals, Galeactena and its relatives had hardened ‘spokes’ on the sides of the body (appearing as dark bands in this photograph). Credit: Scott Billings.

Lynn Margulis and the origins of multicellular life

To mark International Women’s Day Professor Judith Armitage, lead scientist on the Bacterial World exhibition, reflects on the ground-breaking – and controversial – work of evolutionary biologist Lynn Margulis

Iconoclastic, vivacious, intuitive, gregarious, insatiably and omnivorously curious, partisan, bighearted, fiercely protective of friends and family, mischievous, and a passionate advocate of the small and overlooked.

Lynn Margulis at the III Congress about Scientific Vulgarization in La Coruña, Spain, on November 9, 2005. Image: Jpedreira, CC BY-SA 2.5

These are all words used to describe evolutionary biologist and public intellectual Lynn Margulis. Intellectually precocious, Margulis got her first degree from the University of Chicago aged 19, but it was her exposure to an idea about the evolution of a certain type of cell that ignited a lifelong focus of her work.

This idea claimed that eukaryotic cells – cells with a nucleus, found in all plants and animals, but not bacteria – were first formed billions of years ago when one single-celled organism – a prokaryote – engulfed another to create a new type of cell. This theory, known as endosymbiosis, was laid down in a paper by Margulis in 1967. It brought her into conflict with others, including the so-called neo-Darwinists who believed in slow step-wise evolution driven by competition between organisms, not cooperation.

So what happened in the earliest evolution of these crucial cells? Initially, one bacterium ate a different, oxygen-using bacterium but didn’t digest it. Over time the two became interdependent and the bacterium took over almost all of the energy-generating processes of the host cell, becoming what we now call a mitochondrion. This allowed the cell to evolve into bigger cells and eventually form communities and develop into multicellular organisms.

Animal cells evolved when one single cell, possibly an archaeon, engulfed an aerobic bacterium – one that used oxygen to release energy. The bacterium evolved into the mitochondrion, the powerhouse of the cells of humans and other animals. A similar process created the chloroplasts found in plant cells.

These early mitochondria-containing organisms continued to eat other bacteria, and on more than one occasion they ate a photosynthesising cyanobacterium which evolved into a chloroplast, a structure now found inside plant cells.

The revolution in DNA sequencing that started in the 1970s, and continues today, eventually vindicated Margulis’ position on this ancient sequence of events. It revealed that chloroplasts and mitochondria both contain DNA with the same ancestry as cyanobacteria and proteobacteria respectively. In other words, both chloroplasts and mitochondria have evolved from ancient bacteria.

Margulis’ enthusiastic support for these ideas led her to think about the role of biology in the geology of Earth and some of its major changes, in particular the oxygenation of the atmosphere by cyanobacteria around 2.5 billion years ago. Mitochondria use oxygen, and so must have evolved from bacterial ancestors that arose after the cyanobacteria started to produce oxygen through photosynthesis.

Margulis met Gaia theorist James Lovelock soon after her seminal publication on endosymbiosis. At the time, Lovelock was looking at the composition of the atmosphere and factors causing change, including oxygen levels. He was starting to think of the Earth as a system – Gaia as it became known – where the planetary environment is regulated and kept stable by biological activity.

This meeting brought together two scientific outliers. Together they produced highly controversial articles on the “atmosphere as a biological contrivance”. Lovelock believed in concentrating on examining the systems as they are now, while Margulis brought deep time and evolutionary depth into the picture.

Margulis’ ideas were not always right, and she was enormously controversial in her time, but she made people think again. And in doing so she moved our understanding of things as apparently academically distant as the evolution of tiny cells billions of years ago to the stability of Earth’s environment today.

Top image: Euglena, a single cell eukaryotic. By Deuterostome [CC BY-SA 3.0]

Life’s big bang?

by Harriet Drage and Scott Billings

You may have heard of the Cambrian Explosion, an ‘event’, starting roughly 540 million years ago, when all the major animal groups suddenly appear in the fossil record, an apparent explosion of life and evolution.

But was there really an evolutionary explosion of all these animal groups, or is the lack of evidence from earlier periods due to some peculiarity of the fossilisation process? The debate has rumbled on for a number of years.

Now, a new study from our research team, the University of Oxford’s Department of Zoology, and the University of Lausanne, claims that the early Cambrian saw the origins and evolution of the largest and most important animal group on Earth – the euarthropods – in a paper which challenges two major pictures of animal evolution.

Euarthropoda contains the insects, crustaceans, spiders, trilobites, and a huge diversity of other forms alive and extinct. They comprise over 80 percent of all animal species on the planet and are key components of all of Earth’s ecosystems, making them the most important group since the dawn of animals over 500 million years ago.

Exceptionally preserved soft-bodied fossils of the Cambrian predator and stem-lineage euarthropod Anomalocaris canadensis from the Burgess Shale, Canada. Top left: Frontal appendage showing segmentation similar to modern-day euarthropods. Bottom right: Full body specimen showing one pair of frontal appendages (white arrows) and mouthparts consisting of plates with teeth (black arrow) on the head. Images: A. Daley.

A team based at the museum, and now at Lausanne, conducted the most comprehensive fossil analysis ever undertaken on early euarthropods, to try and establish whether these animals really did emerge in the early Cambrian period, or whether fossilisation just didn’t occur in any earlier periods.

In an article published today in the Proceedings of the National Academy of Sciences they show that, taken together, the total fossil record does show a gradual radiation of euarthropods during the early Cambrian, 540-500 million years ago, challenging other ideas that suggest either a rapid explosion of forms, or a much slower evolution that has not been preserved in the fossil record.

Each of the major types of fossil evidence has its limitation and they are incomplete in different ways, but when taken together they are mutually illuminating
Professor Allison Daley

Reconstruction of the Cambrian predator and stem-lineage euarthropod Anomalocaris canadensis, based on fossils from the Burgess Shale, Canada. Reconstruction by Natalia Patkiewicz.

By looking at a huge range of fossil material the researchers ruled out the possibility that Pre-Cambrian rocks older than around 541 million years would not have preserved early euarthropods. The only plausible explanation left is that the origins of this huge animal group didn’t evolve until about 540 million years ago, an estimate which also matches the most recent molecular dating.

The timing of the origin of Euarthropoda is very important as it affects how we view and interpret the evolution of the group and its effects on the planet. By working out which groups developed first we can trace the evolution of physical characteristics, such as limbs.

Exploring all the evidence like this allows us to make an informed estimate about the origins of key animal groups, leading to a better understanding of the evolution of early life on Earth.

Model of the Cambrian stem lineage euarthropod Peytoia, based on fossils from the Burgess Shale. Top left: Closeup of the mouth parts and frontal appendages. Bottom right: Overall view of the body. Model and image: E. Horn.