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The mysterious power of metamorphosis
Metamorphosis Nature’s most transformative process may also be an unsung force for evolution, says Frank Ryan
M
etamorphoses is the title Ovid chose for his classic collection of stories in which men and women are magically transformed into four-legged animals, birds and flowering plants. In the real world there are no such miracles, but the metamorphoses of tadpoles into frogs and caterpillars into butterflies are every bit as startling as Ovid’s poetic vision. Think about it – two separate beings with radically different body forms and life cycles developing from a single fertilised egg. This must surely be one of the strangest processes in nature. Metamorphosis has intrigued observers for millennia. Aristotle tried to make sense of it by describing the caterpillar as a continuation of embryonic life, “nothing more than a soft egg”, existing before the perfect adult butterfly is formed. Today we have a good understanding of metamorphosis in insects (see “How to make a butterfly”, page 58) and we also know that the phenomenon is far more widespread than Aristotle could have realised. As well as the familiar examples in insects and amphibians, it also features in an astonishing 15 separate phyla of marine animals, and that’s where it is most intriguing. Metamorphic transformations among marine invertebrates take a baffling variety of forms. We know about some of them, thanks to decades of painstaking research, and what we are finding is starting to shed light on the evolution of animals themselves. Life began in the oceans, and one theory suggests that metamorphosis in marine animals holds the key to the so-called Cambrian explosion, the exuberant evolutionary radiation that occurred more than half a billion years ago and gave rise to the entire animal kingdom.
56 | NewScientist | 24 September 2011
The idea is highly controversial, but is now gaining support from genetic studies. It is starting to look as though metamorphosis may have been an important and overlooked source of creativity in evolution. Back in the 1870s, Charles Darwin’s friend and protégé, Francis Maitland Balfour, suggested that if we could trace the “primary larval form” of the earliest marine animals, we would discover the common ancestor of the animal kingdom. He realised that he could not simply scour the oceans for this ancient missing link, since it would have evolved into something different long ago. So he began by systematically comparing marine larvae and adults in various groups to try to work out their evolutionary pathways.
Window on the past Balfour’s analyses revealed a problem that has bedevilled any attempt to unravel the mysteries of marine metamorphosis. Often, closely related species have very different larvae, indicating that these have not evolved from the original forms, but are secondary forms that arose at some point later in evolution. Nevertheless, the comparative study convinced Balfour that the original primary larval form was likely to be a simple sphere covered in protuberances called cilia. Animals in the phylum Cnidaria have larvae rather like this, and two members of the phylum, the jellyfish and hydra, are among the earliest animals to appear in the fossil record. His bold analysis was applauded by Darwin and others, but a few years after publishing a book on his ideas Balfour died in a climbing accident and his work was largely
forgotten. A century would pass before another biologist took up the baton. Donald Williamson began working as a planktonologist at the University of Liverpool, UK, in the 1950s. In his research at the Marine Laboratory on the Isle of Man, he was struck by the bewildering variety of forms and strange life cycles of the larvae he studied. The larva of Luidia sarsi, for example, is a semi-transparent diaphanous sprite that feeds on algae and grows to a remarkable 4 centimetres. Then something extraordinary happens. Instead of changing shape to become an adult, a cluster of cells lining the larva’s internal cavity grows, like an alien invader, and out of these a starfish is born. Floating free from its other self, the adult form settles on the ocean floor, where it survives and grows by hunting down other starfish in the dark of night. Meanwhile, the larva continues its vegetarian existence, grazing the surface waters above. Starfish are echinoderms, and Williamson was intrigued by the entire spiny-skinned phylum, which also contains sea urchins, brittle stars, sand dollars, feather stars and sea lilies. As larvae, most are bilaterally symmetrical, yet their adult forms have radial symmetry, and all are “born again” from pluripotent cells within the larva’s abdominal cavity. An equally bizarre metamorphosis typifies the sea squirts, where not only does the adult develop within the growing tadpole larva, its development is entirely separate from it. The tadpole has rudimentary features characteristic of the chordate phylum, including a notochord – a kind of primitive spine – and a simple brain, but when the time is right it heads for the ocean floor, where it sacrifices most of these chordate features >
imagequestmarine.com
mark conlin/v+w/imagequestmarine.com
The earliest ancestor of all animals may have resembled a simple jellyfish larva
24 September 2011 | NewScientist | 57
”The larval and adult forms of marine invertebrates
often look like entirely different organisms, perhaps because that is exactly what they used to be” and turns into the bottom-tethered gilded teapot that is the adult sea squirt. Of course Williamson noticed the startling mismatch between many larvae and their adults. Unaware of Balfour’s earlier work, he set about constructing a tree of life based on larval features and then compared this with the conventional tree for the corresponding adults. From this emerged his controversial “larval transfer” theory, which proposed that widely separated evolutionary lineages had occasionally come together to form hybrid species. In other words, the larval and adult forms of marine invertebrates often look like entirely different organisms because that is exactly what they used to be (Larvae and Evolution, Chapman and Hall, 1992). The theory provoked frank disbelief among many biologists. Undaunted, Williamson set out to confirm it in an extraordinary series of experiments involving improbable sexual
crosses between animals from different marine invertebrate phyla. Accepting that he could never reproduce the natural hybridisations that had taken place over the vastness of evolutionary time, Williamson merely hoped that any success in producing hybrid offspring would be enough to convince his peers to take the theory seriously. Two experiments in particular produced interesting findings. In 1990, working alone, Williamson fertilised eggs from the sea squirt Ascidia mentula with sperm from the sea urchin Echinus esculentus. Then in 2002, with Sebastian Holmes and Nic Boerboom, he did the reverse cross, using eggs from the urchin and sperm from the sea squirt. Both crosses resulted in large numbers of offspring, the majority of eggs developing into easel-shaped larvae – the “pluteus” form typical of sea urchins, rather than the tadpole larvae that are the hallmark of sea squirts. Most of these
larvae subsequently metamorphosed to a rounded adult form, which Williamson called a “spheroid”. The first cross created spheroids with a suction cup, that enabled them to attach to surfaces. Most intriguingly, the second produced spheroids that reproduced asexually through budding, the pinching off of a section of the body to create a clone. These spheroidal offspring had never been seen before, although they bore a striking resemblance to Balfour’s primary larva, which he had considered the last common ancestor of the animal kingdom. Although the findings were never published, Holmes presented them at the 38th European Marine Biological Symposium in 2003. But were the spheroids really hybrids, as Williamson believed? Unfortunately he had no facility to perform genetic or molecular analyses and without this we cannot be sure. Other, less dramatic crosses between marine invertebrates of different species, genera and occasionally families do seem to have produced hybrids, however. For example when Rudolf Raff and colleagues at Indiana University, Bloomington, crossed two species of Australian sea urchin, Heliocidaris
silvia/minden pictures/flpa
How to make a butterfly The female red admiral butterfly lays each of its eggs on a separate nettle leaf. When the larva emerges it rolls the leaf around itself, creating a tent that it devours from the inside out. Over the next 12 to 14 days, the hungry caterpillar consumes one leaf after another, moulting four times to allow it to grow without bursting out of its skin. Finally it is ready for a truly cataclysmic change. Within the cloistered sanctuary of the pupa, the larval tissues and organs melt down to a molecular soup, from which the glory of the adult butterfly emerges. The same genome that once created a simple grub now gives rise to bejewelled wings, multifaceted eyes, a feeding proboscis, jointed legs and, most important of all, the fully functional sexual parts that will produce the next generation. For millennia, people have been intrigued by how butterflies and other insects undergo their phoenix-like rebirth. A critical insight into the process came in the mid 20th century from biologist Vincent Wigglesworth. Working first at the London School of Hygiene and Tropical Medicine and then at the University of
58 | NewScientist | 24 September 2011
Cambridge, he conducted a series of rather macabre experiments using the bloodsucking bug, Rhodnius prolixus. Like the red admiral, its larvae moult four times before metamorphosing into adults. By chopping their heads off at various stages of development and then joining these to bodies from different stages to create
blood-sharing conglomerations, Wigglesworth showed that metamorphosis is controlled by hormones. His work and that of others, including Carroll Williams at Harvard University and Soichi Fukuda at Nagoya University in Japan, revealed that three separate organs are involved – a region of the brain called the pars intercerebralis, a hormonesecreting gland in the neck called the corpus allatum and the prothoracic gland in the thorax. Today we know that the whole panoply of insect metamorphoses, from the incomplete metamorphosis of dragonflies, mantises, cockroaches and locusts to the dramatic transformations of butterflies, moths, beetles, bees and house flies, is controlled by the precisely timed signals of two hormones. Ecdysone, produced by the prothoracic gland, triggers each moult, with its effects during the initial stages moderated by juvenile hormone, produced in the corpus allatum. Then, when all the larva-to-larva moults have occurred, the breaks are lifted and ecdysone alone orchestrates the spectacular final transformation to the adult.
t. burnett, k. palmer/v+W/imagequestmarine.com
Adult sea squirts seem to be less evolved than their larval forms
erythrogramma and Heliocidaris tuberculata, they produced larvae that looked distinctly different from either parent (Development, vol 126, p 1937). As these developed they underwent a series of changes, at one stage resembling starfish larvae, then sea cucumber larvae and, by day five, taking the form of the pluteus larva of the paternal species. Genetic analysis confirmed that the larvae combined features from both parents as well as following new developmental pathways. The researchers concluded that hybridisation has major potential as an evolutionary mechanism.
Evolution’s big bang In 2006 Williamson extended his ideas to propose that hybridisation, with its potential for very rapid evolutionary change, might help to explain the origins of the animal kingdom itself (Zoological Journal of the Linnean Society, vol 148, p 585). The forerunners of modern animals appear for the first time some 545 to 525 million years ago, and fossils discovered in the Burgess Shale in Canada and similar beds throughout the world show that their arrival was not presaged by a vast period of evolution. In his book, Wonderful Life, the late Stephen Jay Gould describes an extraordinary and amazingly rapid flowering of genomes at this time, during which
“virtually all of the major groups of modern animals appear with a bang”. This bang is known as the Cambrian explosion. No convincing explanation has ever been proposed for such major and rapid evolutionary change. Gould did draw attention, though, to the fact that some of the fossilised Burgess Shale animals combine a peculiar grab-bag of features that would normally be associated with several different taxonomic groups. Likewise, Simon Conway Morris at the University of Cambridge has described the Cambrian species Nectocaris pteryx as a very peculiar creature indeed, with its head resembling an arthropod but the abdomen appearing to belong to an entirely different phylum. In his 2006 paper, Williamson suggested that, as well as larval transfer, major components of animal body structure could also have been transferred by hybridisation, resulting in chimera-like appearances such as those noted by Gould and Conway Morris. Indeed, he went further and suggested that the rapid evolution of the Cambrian era may have resulted from many such hybridisations, with the astonishing implication that hybridisation contributed to a hitherto unsuspected degree to the origins of modern animal phyla and classes. While many biologists still dismiss Williamson’s ideas as overly speculative,
research published last year indicates that they may not be as wild as some have suggested. In a pioneering study of the evolutionary origins of whole phyla, Michael Syvanen and Jonathan Ducore at the University of California, Davis, compared 2000 protein sequences in representative animals from four phyla: sea squirts, fruit flies, sea urchins and humans. The analysis revealed an unexpected pattern of groupings, with the most likely implication being that the phylum including sea squirts, called the tunicates, derived from hybridisation between a primitive vertebrate and an unknown but now extinct non-vertebrate at a very early stage in the evolution of animals (Journal of Biological Systems, vol 18, p 261). It is fascinating to think that the same processes might underpin metamorphosis in marine invertebrates and be an overlooked source of creativity in evolution. Of course, Williamson’s theory remains on the fringes, but whether it is eventually accepted or refuted, he has done biology a service in highlighting the importance of metamorphosis as a clue to some of the deepest mysteries in biology. n Frank Ryan’s book, Metamorphosis: Unmasking the mystery of how life transforms, is published by Oneworld (fprbooks.com) 24 September 2011 | NewScientist | 59
M
etamorphoses is the title Ovid chose for his classic collection of stories in which men and women are magically transformed into four-legged animals, birds and flowering plants. In the real world there are no such miracles, but the metamorphoses of tadpoles into frogs and caterpillars into butterflies are every bit as startling as Ovid’s poetic vision. Think about it – two separate beings with radically different body forms and life cycles developing from a single fertilised egg. This must surely be one of the strangest processes in nature. Metamorphosis has intrigued observers for millennia. Aristotle tried to make sense of it by describing the caterpillar as a continuation of embryonic life, “nothing more than a soft egg”, existing before the perfect adult butterfly is formed. Today we have a good understanding of metamorphosis in insects (see “How to make a butterfly”, page 58) and we also know that the phenomenon is far more widespread than Aristotle could have realised. As well as the familiar examples in insects and amphibians, it also features in an astonishing 15 separate phyla of marine animals, and that’s where it is most intriguing. Metamorphic transformations among marine invertebrates take a baffling variety of forms. We know about some of them, thanks to decades of painstaking research, and what we are finding is starting to shed light on the evolution of animals themselves. Life began in the oceans, and one theory suggests that metamorphosis in marine animals holds the key to the so-called Cambrian explosion, the exuberant evolutionary radiation that occurred more than half a billion years ago and gave rise to the entire animal kingdom.
56 | NewScientist | 24 September 2011
The idea is highly controversial, but is now gaining support from genetic studies. It is starting to look as though metamorphosis may have been an important and overlooked source of creativity in evolution. Back in the 1870s, Charles Darwin’s friend and protégé, Francis Maitland Balfour, suggested that if we could trace the “primary larval form” of the earliest marine animals, we would discover the common ancestor of the animal kingdom. He realised that he could not simply scour the oceans for this ancient missing link, since it would have evolved into something different long ago. So he began by systematically comparing marine larvae and adults in various groups to try to work out their evolutionary pathways.
Window on the past Balfour’s analyses revealed a problem that has bedevilled any attempt to unravel the mysteries of marine metamorphosis. Often, closely related species have very different larvae, indicating that these have not evolved from the original forms, but are secondary forms that arose at some point later in evolution. Nevertheless, the comparative study convinced Balfour that the original primary larval form was likely to be a simple sphere covered in protuberances called cilia. Animals in the phylum Cnidaria have larvae rather like this, and two members of the phylum, the jellyfish and hydra, are among the earliest animals to appear in the fossil record. His bold analysis was applauded by Darwin and others, but a few years after publishing a book on his ideas Balfour died in a climbing accident and his work was largely
forgotten. A century would pass before another biologist took up the baton. Donald Williamson began working as a planktonologist at the University of Liverpool, UK, in the 1950s. In his research at the Marine Laboratory on the Isle of Man, he was struck by the bewildering variety of forms and strange life cycles of the larvae he studied. The larva of Luidia sarsi, for example, is a semi-transparent diaphanous sprite that feeds on algae and grows to a remarkable 4 centimetres. Then something extraordinary happens. Instead of changing shape to become an adult, a cluster of cells lining the larva’s internal cavity grows, like an alien invader, and out of these a starfish is born. Floating free from its other self, the adult form settles on the ocean floor, where it survives and grows by hunting down other starfish in the dark of night. Meanwhile, the larva continues its vegetarian existence, grazing the surface waters above. Starfish are echinoderms, and Williamson was intrigued by the entire spiny-skinned phylum, which also contains sea urchins, brittle stars, sand dollars, feather stars and sea lilies. As larvae, most are bilaterally symmetrical, yet their adult forms have radial symmetry, and all are “born again” from pluripotent cells within the larva’s abdominal cavity. An equally bizarre metamorphosis typifies the sea squirts, where not only does the adult develop within the growing tadpole larva, its development is entirely separate from it. The tadpole has rudimentary features characteristic of the chordate phylum, including a notochord – a kind of primitive spine – and a simple brain, but when the time is right it heads for the ocean floor, where it sacrifices most of these chordate features >
imagequestmarine.com
mark conlin/v+w/imagequestmarine.com
The earliest ancestor of all animals may have resembled a simple jellyfish larva
24 September 2011 | NewScientist | 57
”The larval and adult forms of marine invertebrates
often look like entirely different organisms, perhaps because that is exactly what they used to be” and turns into the bottom-tethered gilded teapot that is the adult sea squirt. Of course Williamson noticed the startling mismatch between many larvae and their adults. Unaware of Balfour’s earlier work, he set about constructing a tree of life based on larval features and then compared this with the conventional tree for the corresponding adults. From this emerged his controversial “larval transfer” theory, which proposed that widely separated evolutionary lineages had occasionally come together to form hybrid species. In other words, the larval and adult forms of marine invertebrates often look like entirely different organisms because that is exactly what they used to be (Larvae and Evolution, Chapman and Hall, 1992). The theory provoked frank disbelief among many biologists. Undaunted, Williamson set out to confirm it in an extraordinary series of experiments involving improbable sexual
crosses between animals from different marine invertebrate phyla. Accepting that he could never reproduce the natural hybridisations that had taken place over the vastness of evolutionary time, Williamson merely hoped that any success in producing hybrid offspring would be enough to convince his peers to take the theory seriously. Two experiments in particular produced interesting findings. In 1990, working alone, Williamson fertilised eggs from the sea squirt Ascidia mentula with sperm from the sea urchin Echinus esculentus. Then in 2002, with Sebastian Holmes and Nic Boerboom, he did the reverse cross, using eggs from the urchin and sperm from the sea squirt. Both crosses resulted in large numbers of offspring, the majority of eggs developing into easel-shaped larvae – the “pluteus” form typical of sea urchins, rather than the tadpole larvae that are the hallmark of sea squirts. Most of these
larvae subsequently metamorphosed to a rounded adult form, which Williamson called a “spheroid”. The first cross created spheroids with a suction cup, that enabled them to attach to surfaces. Most intriguingly, the second produced spheroids that reproduced asexually through budding, the pinching off of a section of the body to create a clone. These spheroidal offspring had never been seen before, although they bore a striking resemblance to Balfour’s primary larva, which he had considered the last common ancestor of the animal kingdom. Although the findings were never published, Holmes presented them at the 38th European Marine Biological Symposium in 2003. But were the spheroids really hybrids, as Williamson believed? Unfortunately he had no facility to perform genetic or molecular analyses and without this we cannot be sure. Other, less dramatic crosses between marine invertebrates of different species, genera and occasionally families do seem to have produced hybrids, however. For example when Rudolf Raff and colleagues at Indiana University, Bloomington, crossed two species of Australian sea urchin, Heliocidaris
silvia/minden pictures/flpa
How to make a butterfly The female red admiral butterfly lays each of its eggs on a separate nettle leaf. When the larva emerges it rolls the leaf around itself, creating a tent that it devours from the inside out. Over the next 12 to 14 days, the hungry caterpillar consumes one leaf after another, moulting four times to allow it to grow without bursting out of its skin. Finally it is ready for a truly cataclysmic change. Within the cloistered sanctuary of the pupa, the larval tissues and organs melt down to a molecular soup, from which the glory of the adult butterfly emerges. The same genome that once created a simple grub now gives rise to bejewelled wings, multifaceted eyes, a feeding proboscis, jointed legs and, most important of all, the fully functional sexual parts that will produce the next generation. For millennia, people have been intrigued by how butterflies and other insects undergo their phoenix-like rebirth. A critical insight into the process came in the mid 20th century from biologist Vincent Wigglesworth. Working first at the London School of Hygiene and Tropical Medicine and then at the University of
58 | NewScientist | 24 September 2011
Cambridge, he conducted a series of rather macabre experiments using the bloodsucking bug, Rhodnius prolixus. Like the red admiral, its larvae moult four times before metamorphosing into adults. By chopping their heads off at various stages of development and then joining these to bodies from different stages to create
blood-sharing conglomerations, Wigglesworth showed that metamorphosis is controlled by hormones. His work and that of others, including Carroll Williams at Harvard University and Soichi Fukuda at Nagoya University in Japan, revealed that three separate organs are involved – a region of the brain called the pars intercerebralis, a hormonesecreting gland in the neck called the corpus allatum and the prothoracic gland in the thorax. Today we know that the whole panoply of insect metamorphoses, from the incomplete metamorphosis of dragonflies, mantises, cockroaches and locusts to the dramatic transformations of butterflies, moths, beetles, bees and house flies, is controlled by the precisely timed signals of two hormones. Ecdysone, produced by the prothoracic gland, triggers each moult, with its effects during the initial stages moderated by juvenile hormone, produced in the corpus allatum. Then, when all the larva-to-larva moults have occurred, the breaks are lifted and ecdysone alone orchestrates the spectacular final transformation to the adult.
t. burnett, k. palmer/v+W/imagequestmarine.com
Adult sea squirts seem to be less evolved than their larval forms
erythrogramma and Heliocidaris tuberculata, they produced larvae that looked distinctly different from either parent (Development, vol 126, p 1937). As these developed they underwent a series of changes, at one stage resembling starfish larvae, then sea cucumber larvae and, by day five, taking the form of the pluteus larva of the paternal species. Genetic analysis confirmed that the larvae combined features from both parents as well as following new developmental pathways. The researchers concluded that hybridisation has major potential as an evolutionary mechanism.
Evolution’s big bang In 2006 Williamson extended his ideas to propose that hybridisation, with its potential for very rapid evolutionary change, might help to explain the origins of the animal kingdom itself (Zoological Journal of the Linnean Society, vol 148, p 585). The forerunners of modern animals appear for the first time some 545 to 525 million years ago, and fossils discovered in the Burgess Shale in Canada and similar beds throughout the world show that their arrival was not presaged by a vast period of evolution. In his book, Wonderful Life, the late Stephen Jay Gould describes an extraordinary and amazingly rapid flowering of genomes at this time, during which
“virtually all of the major groups of modern animals appear with a bang”. This bang is known as the Cambrian explosion. No convincing explanation has ever been proposed for such major and rapid evolutionary change. Gould did draw attention, though, to the fact that some of the fossilised Burgess Shale animals combine a peculiar grab-bag of features that would normally be associated with several different taxonomic groups. Likewise, Simon Conway Morris at the University of Cambridge has described the Cambrian species Nectocaris pteryx as a very peculiar creature indeed, with its head resembling an arthropod but the abdomen appearing to belong to an entirely different phylum. In his 2006 paper, Williamson suggested that, as well as larval transfer, major components of animal body structure could also have been transferred by hybridisation, resulting in chimera-like appearances such as those noted by Gould and Conway Morris. Indeed, he went further and suggested that the rapid evolution of the Cambrian era may have resulted from many such hybridisations, with the astonishing implication that hybridisation contributed to a hitherto unsuspected degree to the origins of modern animal phyla and classes. While many biologists still dismiss Williamson’s ideas as overly speculative,
research published last year indicates that they may not be as wild as some have suggested. In a pioneering study of the evolutionary origins of whole phyla, Michael Syvanen and Jonathan Ducore at the University of California, Davis, compared 2000 protein sequences in representative animals from four phyla: sea squirts, fruit flies, sea urchins and humans. The analysis revealed an unexpected pattern of groupings, with the most likely implication being that the phylum including sea squirts, called the tunicates, derived from hybridisation between a primitive vertebrate and an unknown but now extinct non-vertebrate at a very early stage in the evolution of animals (Journal of Biological Systems, vol 18, p 261). It is fascinating to think that the same processes might underpin metamorphosis in marine invertebrates and be an overlooked source of creativity in evolution. Of course, Williamson’s theory remains on the fringes, but whether it is eventually accepted or refuted, he has done biology a service in highlighting the importance of metamorphosis as a clue to some of the deepest mysteries in biology. n Frank Ryan’s book, Metamorphosis: Unmasking the mystery of how life transforms, is published by Oneworld (fprbooks.com) 24 September 2011 | NewScientist | 59