̽��ֱ�� of Cambridge - Andrew Gillis

Adult skates can spontaneously repair cartilage injuries

jg533 — Tue, 12 May 2020 08:14:11 +0000

Researchers have found that adult skates have the ability to spontaneously repair injured cartilage, using a type of cartilage stem cell. Human cartilage has very limited capacity for repair, and the finding may lead to new stem cell treatments for human cartilage injuries.

Ancient fish scales and vertebrate teeth share an embryonic origin

fpjl2 — Mon, 20 Nov 2017 20:05:34 +0000

In biology, one long-running debate has teeth: whether ancient fish scales moved into the mouth with the origin of jaws, or if the tooth had its own evolutionary inception.

Recent studies on species such as zebrafish showed scales and teeth developing from distinctly different clusters of cells in fish embryos, pouring cold water on ‘teeth from scales’ theories.

However, while most fish in the sea have bones, one ancient lineage – sharks, skates and rays – possess skeletons made entirely of cartilage.

These cartilaginous fish retain some primitive characteristics that have been lost in their bony counterparts, including small spiky scales embedded in their skin called ‘dermal denticles’ that bear a striking resemblance to jagged teeth.

Now, researchers at the ̽��ֱ�� of Cambridge have used fluorescent markers to track cell development in the embryo of a cartilaginous fish – a little skate in this case – and found that these thorny scales are in fact created from the same type of cells as teeth: neural crest cells.

̽��ֱ��findings, published in the journal PNAS, support the theory that, in the depths of early evolution, these ‘denticle’ scales were carried into the emerging mouths of jawed vertebrates to form teeth. Jawed vertebrates now make up 99% of all living vertebrates, from fish to mammals.

“ ̽��ֱ��scales of most fish that live today are very different from the ancient scales of early vertebrates,” says study author Dr Andrew Gillis from Cambridge’s Department of Zoology and the Marine Biological Laboratory in Woods Hole.

“Primitive scales were much more tooth-like in structure, but have been retained in only a few living lineages, including that of cartilaginous fishes such as skates and sharks.

“Stroke a shark and you’ll find it feels rougher than other fish, as shark skin is covered entirely in dermal denticles. There’s evidence that shark skin was actually used as sandpaper as early as the Bronze Age,” says Gillis.

“By labelling the different types of cells in the embryos of skate, we were able to trace their fates. We show that, unlike most fish, the denticle scales of sharks and skate develop from neural crest cells, just like teeth.

“Neural crest cells are central to the process of tooth development in mammals. Our findings suggest a deep evolutionary relationship between these primitive fish scales and the teeth of vertebrates.

“Early jawless vertebrates were filter feeders – sucking in small prey items from the water. It was the advent of both jaws and teeth that allowed vertebrates to begin processing larger and more complex prey.”

̽��ֱ��very name of these scales, dermal denticles, alludes to the fact that they are formed of dentine: a hard calcified tissue that makes up the majority of a tooth, sitting underneath the enamel.

̽��ֱ��jagged dermal denticles on sharks and skate – and, quite possibly, vertebrate teeth – are remnants of the earliest mineralised skeleton of vertebrates: superficial armour plating.

This armour would have perhaps peaked some 400 million years ago in now-extinct jawless vertebrate species, as protection against predation by ferocious sea scorpions, or even their early jawed kin.

̽��ֱ��Cambridge scientists hypothesise that these early armour plates were multi-layered: consisting of a foundation of bone and an outer layer of dentine – with the different layers deriving from different types of cells in unborn embryos.

These layers were then variously retained, reduced or lost in different vertebrate linages over the course of evolution. “This ancient dermal skeleton has undergone considerable reductions and modifications through time,” says Gillis.

“ ̽��ֱ��sharks and skate have lost the bony under-layer, while most fish have lost the tooth-like dentine outer layer. A few species, such as the bichir, a popular fish in home aquariums, have retained aspects of both layers of this ancient external skeleton.”

Latest findings support the theory that teeth in the animal kingdom evolved from the jagged scales of ancient fish, the remnants of which can be seen today embedded in the skin of sharks and skate.

This ancient dermal skeleton has undergone considerable reductions and modifications through time

Andrew Gillis

Andrew Gillis, Gillis Lab.

Dermal denticles on the tail of the Little Skate, as used in the latest research.

̽��ֱ��text in this work is licensed under a Creative Commons Attribution 4.0 International License. For image use please see separate credits above.

Yes

Deeper origin of gill evolution suggests 'active lifestyle' link in early vertebrates

fpjl2 — Thu, 09 Feb 2017 17:02:27 +0000

A new study has revealed that gills originated much deeper in evolutionary history than previously believed. ̽��ֱ��findings support the idea that gills evolved before the last common ancestor of all vertebrates, helping facilitate a "lifestyle transition" from immobile filter-feeder to actively swimming predator.

̽��ֱ��research, published today in the journal Current Biology, shows that gills develop from the same embryonic tissue in both jawed and jawless vertebrates - a lineage that split very early in our ancestral tree.

Jawed vertebrates - such as fish, birds and mammals - make up 99% of all living vertebrates, including us. Jawless vertebrates include the parasitic lamprey and scavenging hagfish: eel-like creatures that diverged from the ancestral line over 400 million years ago.

Previous work in this area involved slicing thin sections of fish embryos to chart organ growth. These "snapshots" of development led scientists to believe that gills were formed from different tissues: the internal 'endoderm' lining in jawless vertebrates, and the 'ectoderm' outer skin in the jawed.

As a result, since the mid-20th century it was thought that the ancient jawed and jawless lines evolved gills separately after they split, an example of 'convergent evolution' - where nature finds the same solution twice (such as the use of echolocation in both bats and whales, for example).

Biologists at the ̽��ֱ�� of Cambridge used fluorescent labelling to stain cell membranes in skate embryos, and tracked them through the dynamic development process. Their experiment has now shown that the gills of jawed vertebrates emerge from the same internal lining cells as their jawless relatives.

̽��ֱ��researchers say this is strong evidence that gills evolved just once, much earlier in evolutionary history - before the jawless divergence - and that the "crown ancestor" of all vertebrates was consequently a more anatomically complex creature.

̽��ֱ��findings pull the invention of gills closer to the "active lifestyle" shift in our early ancestors: the evolution from passive filter feeders to self-propelled ocean swimmers. Scientists say that gill development may have been a catalyst or consequence of this giant physiological leap.

"These findings demonstrate a single origin of gills that likely corresponds with a key stage in vertebrate evolution: when some of our earliest relatives transitioned from filtering particles out of water pumped through static bodies to actively swimming through the oceans," says lead author Dr Andrew Gillis, a Royal Society ̽��ֱ�� Research Fellow in Cambridge's Department of Zoology, and a Whitman Investigator at the Marine Biological Laboratory in Woods Hole, US.

"Gills provided vertebrates with specialist breathing organs in their head, rather than having to respire exclusively through skin all over the body. We can't say whether these early animals became more active and needed to evolve a new respiratory mechanism, or if it was gill evolution that allowed them to move faster.

"However, whether by demand or opportunity, our work suggests that the physiological innovation of gills occurred at the same time as the lifestyle transition from passive to active in some of our earliest ancestors."

While the jawed vertebrate lineage spawned the majority of vertebrate life that exists on Earth today - "evolutionarily speaking, we are all bony fish," says Gillis - lamprey and hagfish are the living remnants of a once extensive assemblage of primitively predatory jawless vertebrates.

"Lamprey are eel-like parasites that use their tooth-like organs and raspy tongue to latch onto fish and suck out the blood, while hagfish scavenge by taking bites out of dead matter," he says.

Gillis and colleagues used embryos of the little skate to track early gill development through cell tracing. ̽��ֱ��skate is a cartilaginous fish - an early-branching lineage of jawed vertebrates that includes the sharks and stingrays.

This made skate an excellent comparison point to try and infer the primitive anatomical and developmental conditions in the last common ancestor of jawed and jawless vertebrates.

̽��ֱ��embryonic work of the Gillis laboratory neatly complements paleontological research from their Cambridge colleague Prof Simon Conway Morris, who has spent much of his career studying fossils of the Cambrian period of rapid evolution - when most major animal groups originated.

In 2014, Conway Morris was part of the team that discovered Metaspriggina: one of the oldest-known vertebrate fossils, perhaps over 500 million years old, which displayed hints of a gill structure, as well as the muscle arrangement of an active swimmer.

"Our embryological research helps us understand exactly how the gill structures in early vertebrates such as Metaspriggina relate to the gills of living forms," says Gillis.

"Embryology can tell us about the evolutionary relationship between anatomical features in living animals, while palaeontology can pinpoint precisely when these features first appear in deep time. I think that this work nicely illustrates how these two areas of research can inform one another."

Fish embryo study indicates that the last common ancestor of vertebrates was a complex animal complete with gills – overturning prior scientific understanding and complementing recent fossil finds. ̽��ֱ��work places gill evolution concurrent with shift to self-propulsion in our earliest ancestors.

Our work suggests that the physiological innovation of gills occurred at the same time as the lifestyle transition from passive to active in some of our earliest ancestors

Andrew Gillis

Left: Early skate embryo labeled with fluorescent dye. Right: Image of a hatchling skate

̽��ֱ��text in this work is licensed under a Creative Commons Attribution 4.0 International License. For image use please see separate credits above.

Yes

Sonic hedgehog gene provides evidence that our limbs may have evolved from sharks’ gills

jeh98 — Tue, 19 Apr 2016 11:07:28 +0000

An idea first proposed 138 years ago that limbs evolved from gills, which has been widely discredited due to lack of supporting fossil evidence, may prove correct after all – and the clue is in a gene named for everyone’s favourite blue hedgehog.

Unlike other fishes, cartilaginous fishes such as sharks, skates and rays have a series of skin flaps that protect their gills. These flaps are supported by arches of cartilage, with finger-like appendages called branchial rays attached.

In 1878, influential German anatomist Karl Gegenbaur presented the theory that paired fins and eventually limbs evolved from a structure resembling the gill arch of cartilaginous fishes. However, nothing in the fossil record has ever been discovered to support this.

Now, researchers have reinvestigated Gegenbaur’s ideas using the latest genetic techniques on embryos of the little skate – a fish from the very group that first inspired the controversial theory over a century ago – and found striking similarities between the genetic mechanism used in the development of its gill arches and those in human limbs.

Scientists say it comes down to a critical gene in limb development called ‘Sonic hedgehog’, named for the videogame character by a research team at Harvard Medical School.

̽��ֱ��new research shows that the functions of the Sonic hedgehog gene in human limb development, dictating the identity of each finger and maintaining growth of the limb skeleton, are mirrored in the development of the branchial rays in skate embryos. ̽��ֱ��findings are published today in the journal Development.

Dr Andrew Gillis, from the ̽��ֱ�� of Cambridge’s Department of Zoology and the Marine Biological Laboratory, who led the research, says that it shows aspects of Gegenbaur’s theory may in fact be correct, and provides greater understanding of the origin of jawed vertebrates – the group of animals that includes humans.

“Gegenbaur looked at the way that these branchial rays connect to the gill arches and noticed that it looks very similar to the way that the fin and limb skeleton articulates with the shoulder,” says Gillis. “ ̽��ֱ��branchial rays extend like a series of fingers down the side of a shark gill arch.”

“ ̽��ֱ��fact that the Sonic hedgehog gene performs the same two functions in the development of gill arches and branchial rays in skate embryos as it does in the development of limbs in mammal embryos may help explain how Gegenbaur arrived at his controversial theory on the origin of fins and limbs.”

In mammal embryos, the Sonic hedgehog gene sets up the axis of the limb in the early stages of development. “In a hand, for instance, Sonic hedgehog tells the limb which side will be the thumb and which side will be the pinky finger,” explains Gillis. In the later stages of development, Sonic hedgehog maintains outgrowth so that the limb grows to its full size.

To test whether the gene functions in the same way in skate embryos, Gillis and his colleagues inhibited Sonic hedgehog at different points during their development.

They found that if Sonic hedgehog was interrupted early in development, the branchial rays formed on the wrong side of the gill arch. If Sonic hedgehog was interrupted later in development, then fewer branchial rays formed but the ones that did grow, grew on the correct side of the gill arch – showing that the gene works in a remarkably similar way here as in the development of limbs.

“Taken to the extreme, these experiments could be interpreted as evidence that limbs share a genetic programme with gill arches because fins and limbs evolved by transformation of a gill arch in an ancestral vertebrate, as proposed by Gegenbaur,” says Gillis. “However, it could also be that these structures evolved separately, but re-used the same pre-existing genetic programme. Without fossil evidence this remains a bit of a mystery – there is a gap in the fossil record between species with no fins and then suddenly species with paired fins – so we can’t really be sure yet how paired appendages evolved.”

“Either way this is a fascinating discovery, because it provides evidence for a fundamental evolutionary link between branchial rays and limbs,” says Gillis. “While palaeontologists look for fossils to try to reconstruct the evolutionary history of anatomy, we are effectively trying to reconstruct the evolutionary history of genetic programmes that control the development of anatomy.”

Paired appendages, such as arms and hands in humans, are one of the key anatomical features that distinguish jawed vertebrates from other groups. “There is a lot of interest in trying to understand the origins of jawed vertebrates, and the origins of novel features like fins and limbs,” says Gillis.

“What we are learning is that many novel features may not have arisen suddenly from scratch, but rather by tweaking and re-using a relatively small number of ancient developmental programmes.”

Gillis and his colleagues are further testing Gegenbaur’s theory by comparing the function of more genes involved the development of skates’ unusual gills and mammalian limbs.

“Previous studies haven’t found compelling developmental genetic similarities between gill arch derivatives and paired appendages – but these studies were done in animals like mice and zebrafish, which don’t have branchial rays,” says Gillis.

“It is useful to study cartilaginous fishes, not only because they were the group that first inspired Gegenbaur’s theory, but also because they have a lot of unique features that other fishes don’t – and we are finding that we can learn a lot about evolution from these unique features.”

“Many researchers look at mutant mice or fruit flies to understand the genetic control of anatomy. Our approach is to study and compare the diverse anatomical forms that can be found in nature, in order to gain insight into the evolution of the vertebrate body.”

This research was funded by the Royal Society, the Isaac Newton Trust and a research award from the Marine Biological Laboratory.

Inset images: Skeletal preparation of an embryonic bamboo shark (Andrew Gillis); A skate embryo that has been stained for expression of the Shh gene - staining can be seen as dark purple strips running down the length of each gill arch (Andrew Gillis); Late stage skate embryo (Andrew Gillis).

Latest analysis shows that human limbs share a genetic programme with the gills of cartilaginous fishes such as sharks and skates, providing evidence to support a century-old theory on the origin of limbs that had been widely discounted.

̽��ֱ��branchial rays extend like a series of fingers down the side of a shark gill arch

Andrew Gillis

Head skeletons of skate and shark showing gill arch appendages in red.

̽��ֱ��text in this work is licensed under a Creative Commons Attribution 4.0 International License. For image use please see separate credits above.

Yes