Scientists Debate the Origin of
Cell Types in the First Animals
Jordana Cepelewicz
From
one came many. Some 700 million years ago, a single cell gave rise to the first
animal, a multicellular organism that would eventually spawn the incredible
complexity and diversity seen in animals today. New research is now offering
scientists a fresh perspective on what that cell looked like, and how
multicellularity could have emerged from it — a transition that marks one of
the most pivotal events in the history of life on Earth.
For well over a century, it
has been widely assumed that the ancestors from which the first animal
evolved were simple blobs of identical cells. Only later, after the animals
formed their own branch on the tree of life, did those cells start to
differentiate into various cell types with specialized functions. But now,
painstaking genomic analyses and comparisons between the most ancient animals
alive today and their closest non-animal relatives are starting to
overturn that theory.
The recent work paints a picture
of ancestral single-celled organisms that were already amazingly complex.
They possessed the plasticity and versatility to slip back and forth between
several states — to differentiate as today’s stem cells do and then
dedifferentiate back to a less specialized form. The research implies that mechanisms
of cellular differentiation predated the gradual rise
of multicellular animals.
Now, scientists are reporting the
most compelling evidence yet for the new narrative. Their work, and the debate
inspired by its publication inNature last month, also highlights how
difficult it is to pin down definitive answers to these kinds of evolutionary
questions — and how wide a net researchers have to cast in pursuit
of those answers.
Looking for Close Relatives
In the 1860s, the biologists
Henry James Clark and William Saville-Kent separately noted a striking
resemblance between the cells of two organisms. Choanoflagellates are tiny
spherical or egg-shaped cells crowned with a “collar” of fingerlike protrusions
surrounding a single flagellum that whips back and forth. These protists stir
up water currents with their flagella, sweeping their next meal (usually
bacteria) into their collars to eat. Meanwhile, sponges are simple animals made
up of many cell types, including choanocytes — collared, flagellated cells
that line the chambers inside the sponge and capture its food. Choanocytes
look and act remarkably like choanoflagellates, so much so that some scientists
posited in the 1980s and ’90s that choanoflagellates might be animals that
evolved from sponges and then simplified down to one cell.
The
structural similarities prompted experts to think that
the cells shared an ancestor, and that the single-celled
choanoflagellates might be the key to understanding how the multicellular
sponge came about. Building on this, the famed marine biologist Ernst Haeckel
put forth a theory for the evolution of animal multicellularity in 1874, which
researchers have since elaborated on: A choanoflagellate-like ancestral cell
started it all. Many such cells came together to form a colony, a hollow ball
of identical cells that, in turn, gradually differentiated into cell types and
tissues with various functions. This eventually led to the first animal, the
sponge — and the rest is history.
All the signs indicated that this
was the right way to think about animal evolution. In the 2000s, more than a
century after Haeckel proposed his theory, genomic evidence
confirmed that choanoflagellates were animals’ closest living
relatives. “Out of the many single-cell eukaryotes out there, 150 years ago
choanoflagellates had been proposed as a close relative of animals,” said Pawel
Burkhardt, a molecular biologist at the Sars International Center for
Marine Molecular Biology in Norway. “Then the first genome was sequenced, and
bam! It actually was really true.”
“Scientists, including myself, have for a long
time enjoyed this choanoflagellate-choanocyte connection,” said David
Gold, a geobiologist at the University of California, Davis, “because it
tells a clear and elegant story.”
Besides, said Douglas
Erwin, a paleobiologist at the Smithsonian Institution’s National Museum of
Natural History in Washington, D.C., “You’re going to question Haeckel? How
do you question Haeckel? It’s almost like questioning Darwin.” [[!!??!!]]
[[And in spite of all the signs confirming
the theory, and its calirity and elegance – and acceptance in the scientific
community – it is now seen to be wrong. Is the moral obvious for those contemporary
theories that are supported by all the evidence and are clear and elegant and
accepted?]]
The First Seeds of Doubt
But uncertainty about that clear
and elegant story has been growing over the past decade. The idea that animals
arose from a colony of choanoflagellate-like cells implies that cell
differentiation evolved after multicellularity did. But “the data is
demonstrating that it’s not like that,” said Iñaki Ruiz-Trillo, an evolutionary biologist at the
Institute of Evolutionary Biology in Barcelona.
The first complication came in
2008, when a group of scientists, in an effort to more
precisely map out the evolutionary relationships among animals on the
tree of life, identified comb jellies rather than sponges as the earliest
animals. [[Hmmm – what dating methods did they use first? And what methods
second? And why did they not agree?]] The finding generated controversy. “It’s still
very much a heated question,” Gold said, “but I think it forced the community
to reappraise the classic narrative.”
Subsequent
discoveries continued to fuel the debate over which animal group came first.
And some studies uncovered overlooked
differences [[Hmm – overlooked differences
– so they were there but no one paid attention….could that be happening again
today?]] between choanoflagellates
and sponge choanocytes. The cells’ shared ancestry began to look less like
a foregone conclusion.
Scientists also began to realize
that choanoflagellates and two closely related unicellular groups all have
complex life cycles that proceed through various cell states. These states
essentially act as different cell types — but rather than all existing side by
side as in a multicellular organism, they arise sequentially in a single
cell. “They have temporal cell differentiation,” Burkhardt said.
And during those life cycles, all
three of these protists spend part of their lives in a form that borders on
something like primitive multicellularity. Choanoflagellates have a colonial
form; the second protist group has amoeba-like cells that aggregate; the cells
of the third group grow to have hundreds of nuclei.
This prompted a paper
in 2009 that rejuvenated an old alternative to Haeckel’s hypothesis.
Back in 1949, the Russian biologist Alexey Zakhvatkin had proposed that
multicellular animals evolved when temporally differentiating cells formed
colonies and began to commit to particular stages in their life cycles,
allowing a few cell types to exist at once. Ruiz-Trillo and his colleagues
provided further evidence for this so-called temporal-to-spatial transition. In
a series of studies, they showed that certain families of regulatory proteins
supposedly unique to animals, including those involved in cell differentiation,
were actually already
present in their far more ancient unicellular relatives.
Now, a team of researchers led
by Sandie
Degnan and Bernard Degnan, a married pair of marine biologists at the
University of Queensland in Australia, have provided additional support for
this view of animal evolution while also taking a swing at the traditional
theory’s foundation: the evolutionary link between the choanoflagellates
and the sponge choanocytes.
A More Flexible Ancestor
When the team started their
project, they “really just wanted to put some meat on the bones of the
[traditional] theory,” Bernard Degnan said. To do so, they examined the gene
expression in choanocytes and other kinds of sponge cells, then compared those
findings with published data on choanoflagellates and two other protists.
They expected to establish that
sponge choanocytes had gene expression profiles most like those of
choanoflagellates. Instead, they found that another type of sponge cell did.
That cell type, called an
archaeocyte, acts like a stem cell for the sponge: It can differentiate into
any other cell type the animal might need. Some of the gene expression patterns
in archaeocytes are significantly similar to those of the protists
during particular life cycle stages, according to Bernard Degnan. “They’re
expressing genes that suggest that they have an ancestral regulatory system,”
he said. “All animals are just variations on that theme that was created a long
time ago.”
Moreover, the choanocytes seemed
to be unexpectedly transient. “The choanocytes, which are supposed to be
the bedrock of all animal origins … are almost ephemeral,” he said. “They don’t
stay stably in that state, but kind of quickly dedifferentiate into these stem
cells, the archaeocytes.”
To Gold, who was not involved in
the study, this result is the strongest evidence yet that sponge choanocytes
should not necessarily be used as “some sort of proxy for the origin of
animals.”
Bernard Degnan thinks it’s
possible that choanoflagellates and sponge choanocytes arrived independently at
their collared, flagellated architecture. In the shared ancestry of
choanoflagellates and sponges there could have been something like an
archaeocyte or a pluripotent stem cell. “It transited between different cell
types, and those cell types then became stable,” he said. “And essentially
that’s what gave rise to true multicellularity.” Later, as animals got bigger
and more complex, their cells had to become more precise, specialized and fixed
in their identities, but they lost a lot of their versatility in the process.
In retrospect, this version of
multicellularity’s origin makes a lot of sense. According to some experts, we
can think of the single-celled organisms that came before animals as stem cells
of sorts: They could go on dividing forever, and they could perform a variety
of functions, including reproduction. Other early animals, such as jellyfish,
show a great deal of that seemingly ancestral plasticity as well.
“Stem cells are something people
have been working on for years” in studies of development, wound healing and
cancer, Ruiz-Trillo said. Now, it’s becoming clear that they will be
“interesting for understanding evolution as well,” for discovering how
animals came to be.
A Path Toward Reconciliation
Not everyone agrees entirely with
the Degnans’ conclusions. Drawing inferences from gene expression profiles
isn’t so straightforward. “Dig into [it], and you could interpret some data
completely differently,” Burkhardt said. Differences in gene expression don’t
necessarily preclude two cell types from sharing ancestry.
This
choanoflagellate, extracted from a colony, uses its signature collar and
flagellum to trap food — much like choanocyte cells do in sponges.
Erwin agreed. Such data, he said,
“is a snapshot [taken] at a particular point in time.” Given that
choanoflagellates and sponge choanocytes have been evolving on their own for
the past 700 million years, it makes sense that they express very different genes.
In any comparison of modern
organisms, “you are looking at animals that have a history of loss and gain,”
said Maja Adamska, an evolutionary developmental biologist at
the Australian National University who did not participate in the Degnans’
study. “You risk that you will oversimplify your findings.” [[Hmm – could some
of today’s accepted “findings” be oversimplified?]]
Other sponge species, she added,
don’t have archaeocytes at all. Instead, their choanocytes perform those stem
cell-like roles. “I suspect that if we did a comparison in [those
choanocytes],” Adamska said, “we would have found higher similarity to
choanoflagellates.”
Adamska thinks that the first
animal could very well have been a pancake of stemlike cells that often shifted
their identities. She also thinks that the gene expression comparison doesn’t
rule out the evolutionary ties between choanoflagellates and the first
multicellular animal cells. “In fact, I strongly believe that my ancestors did
have choanocytes,” she said.
The two theories about the
origins of animal multicellularity aren’t mutually exclusive. “I think there’s
a place for both choanoflagellate-like features and [temporal differentiation]
features in the last common ancestor we are trying to paint,” Adamska said. “I
don’t see the contradiction there.” She and her colleagues are now working on
profiling gene expression in sponges without archaeocytes to test this idea
further.
Hints of a combined theory are
already emerging from Burkhardt’s lab. In a preprint they posted
on biorxiv.org in May, Burkhardt and his colleagues found that the
cells in a choanoflagellate colony are not all identical: They differ in their
morphology and in the ratio of their organelles. These observations, he said,
suggest that spatial cell differentiation was already happening in the
choanoflagellate lineage, and perhaps even earlier — a possibility that blends
the new ideas (that the capacity for differentiation is ancient and the
transition to animal multicellularity was gradual) with the old (that this
could happen with choanoflagellate-like cells).
So while there’s still no
definitive answer on what exactly the first animal looked like, the picture is
getting clearer. “We are getting closer to understanding where we came from in
the depths of time,” Adamska said. “And I think that is so cool.”