Study reveals location of starfish’s head
If you put a hat on a starfish, where would you put it? On the center of the starfish? Or on the point of an arm and, if so, which one? The question is silly, but it gets at serious questions in the fields of zoology and developmental biology that have perplexed veteran scientists and schoolchildren in introductory biology classes alike: Where is the head on a starfish? And how does their body layout relate to ours?
Now, a new Stanford study that used genetic and molecular tools to map out the body regions of starfish – by creating a 3D atlas of their gene expression – helps answer this longstanding mystery. The “head” of a starfish, the researchers found, is not in any one place. Instead, the headlike regions are distributed with some in the center of the sea star as well as in the center of each limb of its body.
“The answer is much more complicated than we expected,” said Laurent Formery, lead author and postdoc in the labs of Christopher Lowe at the Stanford School of Humanities and Sciences and Daniel S. Rokhsar at the University of California, Berkeley. “It is just weird, and most likely the evolution of the group was even more complicated than this.”
Starfish (sea stars) belong to a group of animals called echinoderms. Echinoderms and humans are closely related, yet the life cycle and anatomy of sea stars are very different from ours.
Sea stars begin life as fertilized eggs that hatch into a free-floating larva. The larvae bob in the ocean in a plankton form for weeks to months before settling to the ocean floor to perform a magic trick of sorts – transforming from a bilateral (symmetric across the midline) body plan into an adult with a five-point star shape called a pentaradial body plan.
“This has been a zoological mystery for centuries,” said Lowe, who is also a researcher at Hopkins Marine Station and senior author of the paper that published Nov. 1 in Nature. “How can you go from a bilateral body plan to a pentaradial plan, and how can you compare any part of the starfish to our own body plan?”
Mapping stars
For puzzles such as this one, researchers often conduct comparative studies to identify similar structures in related groups of animals to glean clues about the evolutionary events that prompted the trait of interest.
“The problem with starfish is there is nothing on a starfish anatomically that you can relate to a vertebrate,” said Lowe. “There is just nothing there.”
At least, nothing on the outside of a starfish. And that is where genetic and molecular techniques come in.
During his graduate research, Formery studied early development in sea urchins – echinoderms, like sea stars, that also start their life as bilateral larvae before transforming into adults with fivefold symmetry. When Formery joined Lowe’s lab, Formery’s knowledge of echinoderm development combined with Lowe’s expertise in molecular biology techniques to help tackle the mystery of sea stars’ baffling body plan.
The team used a group of well-studied molecular markers (Hox genes are an example) that act as blueprints for an organism’s body plan by “telling” each cell which body region it belongs to.
“If you strip away the skin of an animal and look at the genes involved in defining a head from a tail, the same genes code for these body regions across all groups of animals,” said Lowe. “So we ignored the anatomy and asked: Is there a molecular axis hidden under all this weird anatomy and what is its role in a starfish forming a pentaradial body plan?”
To investigate this question, the researchers used RNA tomography, a technique that pinpoints where genes are expressed in tissue, and in situ hybridization, a technique that zeroes in on a specific RNA sequence in a cell.
“First we sectioned sea star arms into thin slices from tip to center, top to bottom, and left to right,” said Formery, noting that sea stars regenerate missing limbs. “We used RNA tomography to determine which genes were expressed in each slice and then ‘reassembled’ the slices using computer models. This gave us a 3D map of gene expression.”
“In the second method, in situ hybridization chain reaction, we stained sea star tissue and visually inspected the samples to see where a gene was expressed,” said Formery. This enabled the researchers to examine anterior-posterior (head to tail) body patterning in the outermost layer of cells called the ectoderm.
“This was made possible by the recent, big, technical improvement in in situ hybridization, known as in situ hybridization chain reaction, Formery said. “This new method provides better resolution of where the gene is expressed.”
The research revealed that sea stars have a headlike territory in the center of each “arm” and a tail-like region along the perimeter. In an unexpected twist, no part of the sea star ectoderm expresses a “trunk” genetic patterning program, suggesting that sea stars are mostly headlike.
Mining truly diverse biodiversity
Research is often centered on groups of animals that look like us, the researchers explained. But if we focus on the familiar, we are less likely to learn something new.
“There are 34 different animal phyla living on this planet and in over roughly 600 million years they have all come up with different solutions to the same fundamental biological problems,” Lowe said. “Most animals don’t have spectacular nervous systems and are out chasing prey – they are modest animals that live in burrows in the ocean. People are generally not drawn to these animals, and yet they probably represent how much of life got started.”
This study demonstrates how a comparative approach that uses genetic and molecular techniques can be used to mine biodiversity for insights into why different animals look the way they do and how their body plans evolved.
“Even in recent molecular papers there’s a question mark near echinoderms on the evolutionary tree because we don’t know much about them,” Formery said. “It was nice to show that – at least at the molecular level – we have a new piece of the puzzle that can now be put on the tree.”
Formery, Lowe, and Rokhsar are also researchers at the Chan Zuckerberg BioHub. Rokhsar is also a researcher at the Okinawa Institute of Science and Technology. Additional Stanford co-authors are Ian Kohnle, Judith Malnick, and Kevin Uhlinger of Hopkins Marine Station. Additional authors are from Pacific Biosciences in Menlo Park, California, and Columbia Equine Hospital in Gresham, Oregon.
This research was funded by NASA, the National Science Foundation, and the Chan Zuckerberg BioHub.
JOURNAL
Nature
ARTICLE TITLE
Molecular evidence of anteroposterior patterning in adult echinoderms
ARTICLE PUBLICATION DATE
1-Nov-2023
Starfish body is a head, say scientists
New research sheds light on evolution of mysterious star-shaped body
Peer-Reviewed PublicationIMAGE:
MICRO-CT SCAN OF SEA STAR SHOWING THE SKELETON (GREY), DIGESTIVE SYSTEM (YELLOW), NERVOUS SYSTEM (BLUE), MUSCLES (RED) AND WATER VASCULAR SYSTEM (PURPLE).
view moreCREDIT: UNIVERSITY OF SOUTHAMPTON
The bodies of starfish and other echinoderms are more like heads, according to new research involving the University of Southampton.
The research, published today [1 November] in Nature, helps to answer the mystery of how these creatures evolved their distinctive star-shaped body, which has long puzzled scientists.
Echinoderms are a group of animals that includes starfish (or sea stars), sea urchins, and sand dollars. They have a unique ‘fivefold symmetric’ body plan, which means that their body parts are arranged in five equal sections. This is very different from their bilateral ancestors, which have a left- and right-hand side which mirror one another, as in humans and many other animals.
“How the different body parts of the echinoderms relate to those we see in other animal groups has been a mystery to scientists for as long as we’ve been studying them,” says Dr Jeff Thompson, a co-author on the study from the University of Southampton. “In their bilateral relatives, the body is divided into a head, trunk, and tail. But just looking at a starfish, it's impossible to see how these sections relate to the bodies of bilateral animals.”
In the new study, led by Laurent Formery and Professor Chris Lowe at Stanford University, scientists compared the molecular markers of a sea star to other deuterostomes - a wider animal group that includes echinoderms and bilateral animals, like vertebrates. They share a common ancestor, so by comparing their development, the scientists could learn more about how echinoderms evolved their unique body plan.
Researchers used a variety of high-tech molecular and genomic techniques to understand where different genes were expressed during the development and growth of sea stars. The team at Southampton used micro-CT scanning to understand the shape and structure of the animal in unprecedented detail.
Then, researchers at Stanford, in collaboration with Professor Dan Rokhsar at UC Berkeley and Pacific BioSciences, used ‘RNA tomography’ and ‘in situ hybridization’ to create a three-dimensional map of gene expression in the sea star and find out where specific genes are being expressed during development. Specifically, they mapped the expression of genes which control the development of the ectoderm, which includes the nervous system and the skin. This is known to mark the anterior-posterior (front-to-back) patterning in the bodies of other deuterostomes.
They found this patterning was correlated with the midline-to-lateral axis of the sea star arms – with the midline of the arm representing the front and the outmost lateral parts more like the back. In deuterostomes, there is a distinct set of genes expressed in the ectoderm of the trunk. But in the sea star, many of these genes are not expressed in the ectoderm at all.
Dr Thompson explains: “When we compared the expression of genes in a starfish to other groups of animals, like vertebrates, it appeared that a crucial part of the body plan was missing. The genes that are typically involved in the patterning of the trunk of the animal weren’t expressed in the ectoderm. It seems the whole echinoderm body plan is roughly equivalent to the head in other groups of animals.”
This suggests that sea stars and other echinoderms may have evolved their five-section body plan by losing the trunk region of their bilateral ancestors. This would have allowed the echinoderms to move and feed differently than bilaterally symmetrical animals.
“Our research tells us the echinoderm body plan evolved in a more complex way than previously thought and there is still much to learn about these intriguing creatures,” says Dr Thompson. “As someone who has studied them for the last ten years, these findings have radically changed how I think about this group of animals.”
Molecular evidence of anteroposterior patterning in adult echinoderms is published in Nature and is available online.
This research was supported by the Leverhulme Trust, NASA, NSF and the Chan Zuckerberg BioHub.
Ends
Micro-CT scan of sea star Micro-CT scan of sea star showing the skeleton (grey), digestive system (yellow), nervous system (blue), muscles (red) and water vascular system (purple).
Micro-CT scan of sea star Micro-CT scan of sea star showing the skeleton (grey), digestive system (yellow), nervous system (blue), muscles (red) and water vascular system (purple).
Micro-CT scan of sea star showing the skeleton (grey), digestive system (yellow), nervous system (blue), muscles (red) and water vascular system (purple). Credit: University of Southampton
Micro-CT scan of sea star showing the skeleton (grey), digestive system (yellow), nervous system (blue), muscles (red) and water vascular system (purple). Credit: University of Southampton
CREDIT
University of Southampton
University of Southampton
Notes for editors
- Molecular evidence of anteroposterior patterning in adult echinoderms is published in Nature. An advanced copy of the paper is available upon request.
- Video and various stills available here: https://safesend.soton.ac.uk/pickup?claimID=mxmvqtmoa28Hv84n&claimPasscode=ejTaKz87vmBP4NNu
Caption: Micro-CT scan of sea star showing the skeleton (grey), digestive system (yellow), nervous system (blue), muscles (red) and water vascular system (purple). Credit: University of Southampton
Additional information
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JOURNAL
Nature
ARTICLE TITLE
'Molecular evidence of anteroposterior patterning in adult echinoderms
ARTICLE PUBLICATION DATE
1-Nov-2023
Long presumed to have no heads at all, sea stars may be nothing but
Collaboration led by CZ Biohub SF Investigators unveils a new understanding of the sea star body plan
IMAGE:
THE UNUSUAL FIVE-AXIS SYMMETRY OF SEA STARS (PATIRIA MINIATA) HAS LONG CONFOUNDED OUR UNDERSTANDING OF ANIMAL EVOLUTION.
view moreCREDIT: LAURENT FORMERY
For centuries, naturalists have puzzled over what might constitute the head of a sea star, commonly called a “starfish.” When looking at a worm, or a fish, it’s clear which end is the head and which is the tail. But with their five identical arms — any of which can take the lead in propelling sea stars across the seabed — it’s been anybody’s guess how to determine the front end of the organism from the back. This unusual body plan has led many to conclude that sea stars perhaps don’t have a head at all.
But now, labs at Stanford University and UC Berkeley, each led by Chan Zuckerberg Biohub San Francisco Investigators, have published a study finding that the truth is closer to the absolute reverse. In short, while the team detected gene signatures associated with head development just about everywhere in juvenile sea stars, expression of genes that code for an animal’s torso and tail sections were largely missing.
In another surprising finding, molecular signatures typically associated with the front-most portion of the head were localized to the middle of each of the sea star’s arms, with these signatures becoming progressively more posterior moving out towards the arms’ edges.
The research, published Nov. 1 in Nature, suggests that, far from being headless, over evolutionary time sea stars lost their bodies to become only heads.
“It’s as if the sea star is completely missing a trunk, and is best described as just a head crawling along the seafloor,” said Laurent Formery, a Biohub-funded postdoctoral scholar and lead author of the new study. “It’s not at all what scientists have assumed about these animals.”
Two of the study’s three co–senior authors, marine and developmental biologist Christopher Lowe of Stanford University and UC Berkeley’s Daniel Rokhsar, an expert on the molecular evolution of animal species, have been collaborating for a decade, and were members of a team funded by CZ Biohub SF’s Intercampus Research Awards. Lowe cited the award, which has supported a joint postdoctoral scholar position between both labs for Formery, as an important catalyst in the new discovery.
“The work we proposed to do together was very ambitious and the kind of thing that generally does not play very well with traditional funding mechanisms,” Lowe said. “The Biohub’s willingness to take risks and provide support for a joint position between our labs has been critical for the success of this project.”
Gene expression patchwork
By staining genetic material with fluorescent labels, researchers can examine how key genes behave across the sea star body.
CREDIT
Laurent Formery
A star-shaped puzzle
Almost all animals, including humans, are bilaterally symmetrical, meaning they can be split into two mirrored halves along a single axis extending from their head to their tail. In 1995 the Nobel Prize in Physiology or Medicine was awarded to three scientists who had used fruit flies to demonstrate that the bilateral, head-to-tail body plan seen in most animals arises from the action of a series of molecular switches, coded by genes, expressed in defined head and trunk regions.
Researchers have since confirmed that this same genetic programming is shared by the vast majority of animal species, including vertebrates like humans and fish, and in many invertebrates such as insects and worms.
But the body plan of sea stars has long confounded scientists’ understanding of animal evolution. Instead of displaying bilateral symmetry, adult sea stars — and related echinoderms such as sea urchins and sea cucumbers — have a five-fold axis of symmetry without a clear head or tail. And no one has been able to determine how genetic programming drives this unusual five-fold symmetry.
Some scientists have proposed that in sea stars, the head-to-tail axis might extend from the animal’s armored back to its underbelly, which is carpeted in so-called tube feet. Others have suggested each of the sea star’s five arms corresponds to a copy of a conventional head-to-tail axis.
Efforts to definitively confirm such hypotheses have faced challenges, however, largely because methods for detecting gene expression, developed primarily in a small number of model organisms like mice and flies, don’t work well in the tissue of young sea stars. For years, Lowe and his colleagues had itched to bring genetic information to bear on the question by mapping genetic activity across developing sea stars. But without the complex genetic tool kits developed over decades of research that exist for typical model organisms, such a comprehensive analysis was daunting.
Game-changing technology
Lowe encountered a solution for this problem at one of the regular San Francisco meetings of Biohub Investigators, where another researcher suggested he contact PacBio, a Silicon Valley–based company that builds genome-sequencing devices. Over the previous five years, PacBio had been perfecting a technique for sequencing massive quantities of genetic material using postage stamp–sized chips jam-packed with millions of individual chemical reactors, each primed to simultaneously read long stretches of DNA captured within.
Unlike traditional sequencing, which requires chopping genetic material into small pieces to ensure accuracy, PacBio’s approach, called HiFi sequencing, can pull highly accurate data from intact, gene-sized DNA strands, making the process much faster and cheaper. It was exactly what Lowe and his team needed to establish a process for studying sea star genetics from the ground up.
“The kind of sequencing that would have taken months can now be done in a matter of hours, and it’s hundreds of times cheaper than just five years ago,” said David Rank, also a co–senior author of the new study and a former PacBio Scientific Fellow. “These advances meant we could start essentially from scratch in an organism that’s not typically studied in the lab and put together the kind of detailed study that would have been impossible 10 years ago.”
This technology allowed the researchers to sequence the genomes of the sea stars and employ an approach called spatial transcriptomics, through which they could pinpoint which sea star genes are active at precise locations in the organism. To search for patterns that would indicate a head-to-tail axis, the researchers examined gene expression differences in three different directions across the body: from the sea star’s center to its arm tips, from its top to its underbelly, and from one side edge of its arms to the other. Then, to get a closer look at how certain key genes were behaving, they labeled them one by one with fluorescent dyes to create a detailed map of their distribution in the sea star body.
The researchers found that neither of the prominent hypotheses of sea star body plan structure was correct. Instead, they saw that gene expression corresponding to the forebrain in humans and other bilaterally symmetrical animals was located along the midline of sea stars’ arms, with genetic expression corresponding to that of the human midbrain towards the arms’ outer edges. While the genes marking different subregions of the head in humans and other bilaterians were expressed in the sea star, only one of the genes typically associated with the trunk in animals was expressed, at the very edges of the sea stars’ arms.
“These results suggest that the echinoderms, and sea stars in particular, have the most dramatic example of decoupling of the head and the trunk regions that we are aware of today,” said Formery, adding that some bizarre-looking sea star ancestors preserved in the fossil record do appear to have had a trunk. “It just opens a ton of new questions that we can now start to explore.”
Laurent Formery, a CZ Biohub SF-supported postdoctoral scholar, is fascinated with the nervous system of the sea stars. Discovering that these creatures are “mostly head” has only increased his determination to learn more.
CREDIT
Laurent Formery/Evident Image of the Year Award
A door to new discoveries
Questions that the team hopes to address next involve whether the genetic patterning seen in sea stars also shows up in sea urchins and sea cucumbers. For his part, Formery also wants to look into what the sea star can teach us about the evolution of the nervous system, which, he said, no one quite understands in echinoderms.
Learning more about the sea star and its relatives will not only help solve key mysteries of animal evolution, but could also inspire innovations in medicine, the researchers said. Sea stars walk by moving water through thousands of tube feet and digest their prey by extruding their stomachs outside of their bodies. It only stands to reason that these unusual creatures have also evolved completely unexpected strategies for staying healthy — which, if we took the time to understand them, could expand our approaches to combating human disease.
“It’s certainly harder to work in organisms that are less frequently studied,” Rokhsar said. “But if we take the opportunity to explore unusual animals that are operating in unusual ways, that means we are broadening our perspective of biology, which is eventually going to help us solve both ecological and biomedical problems.”
# # #
About the Chan Zuckerberg Biohub San Francisco
CZ Biohub San Francisco, part of the Chan Zuckerberg Biohub Network, is a nonprofit biomedical research center founded in 2016. CZ Biohub SF’s researchers, engineers, and data scientists, in collaboration with colleagues at our partner universities — Stanford University; the University of California, Berkeley; and the University of California, San Francisco — seek to understand the fundamental mechanisms underlying disease and develop new technologies that will lead to actionable diagnostics and effective therapies. Learn more at czbiohub.org/sf.
JOURNAL
Nature
SUBJECT OF RESEARCH
Animal tissue samples
ARTICLE TITLE
Molecular evidence of anteroposterior patterning in adult echinoderms
ARTICLE PUBLICATION DATE
1-Nov-2023
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