Bionieuws, March 29, 2014
New insights on early animal evolution
Willy van Strien
Comb jellies, placozoans, sponges, cnidarians - biologists strongly disagree on which one
of them have been the first animal group on earth. A new paper identifies the comb
jellies as the most basal clade on the phylogenetic tree - but as yet, the study doesn’t
convince everybody.
The comb jelly Mnemiopsis leidyi (Vidar A, Wikimedia Commons)
A long time ago, a multicellular animal lived on earth that would become the ancestor of the
animal kingdom. How did extant animals evolve from that common ancestor? Biologists
disagree. Last year in Science (December 13, 2013), Joseph Ryan (National Institutes of
Health, Bethesda, USA) and colleagues surprisingly reported that the comb jellies have been
the first group to split off, followed by the sponges.
This idea had already been suggested before, but it had been quickly rejected. People argued
that sponges are more different from to us than comb jellies, and so must be older. They
added that the comb jellies must be related to the cnidarians (jellyfish, sea anemones and
hydras), with which they share their gelatinous body, nervous system and muscle cells. But
Ryan tells: “We did several analyses, and all results indicate that the comb jellies are the
oldest animal group.”
Implications
He is not the first who tried to unravel the origin of the oldest four clades of the animals
(Metazoa): the sponges (Porifera), placozoans (Placozoa), cnidarians (Cnidaria) and comb
jellies (Ctenophora). These four groups predate the bilaterally symmetrical animals
(Bilateria), to which all other species belong.
And that is all biologists know for sure.
They compared proteins, DNA, RNA and whole genomes, and produced different scenarios
for early animal evolution. There still is no agreement, in spite of increasingly extensive
studies analysing more and more genetic information of more and more species. And that is
no surprise: early animal evolution took place 700 to 900 million years ago in a relatively
short time, which makes it difficult to find traces of the history in the genetic code.
Now the team of Ryan is the first to sequence the genome of a comb jelly, Mnemiopsis leidyi.
It is a small genome, and less than half of it corresponds to the genome of other Metazoa.
The researchers then conducted phylogenetic analyses. They compared a set of genes from 58
animal species as well as the complete genome of 13 species with each other and with
different taxa outside the Metazoa. They concluded that the comb jellies appeared first, then
the sponges, then the placozoans and finally the cnidarians and bilaterians.
That revives an old, controversial hypothesis that has major implications. For if comb jellies
are older than sponges and placozoans, they must have developed their nervous system and
muscle cells independently of the cnidarians and the bilaterians. Alternatively, the common
Metazoan ancestor must have possessed a simple nervous system and muscle cells, which
were subsequently lost in sponges and placozoans. Both possibilities seem unlikely at first
sight.
Loss
Nevertheless, some parts of both scenarios appear to be true. Ryan investigated what genes
are present or absent in the animal groups. Comb jellies share some genes involved in cell
communication with other animals. They share many genes related to the nervous system
with cnidarians and bilaterians; but they miss most genes that play a role in muscle
development in cnidarians as well as in bilaterians. Sponges and placozoans have an
unexpected genetic complexity, in spite of their simple appearance (see below), and comb
jellies share a common set of neural genes with sponges.
So, the Metazoan ancestor probably had cell communication and a simple nervous system.
“And a form of light perception”, Ryan suspects. “In Mnemiopsis leidyi we found two genes
for light-sensitive proteins (opsins).” Sponges and placozoans lost that nervous system, but
retained genetic traces of it.
Muscle cells must have developed independently in comb jellies, cnidarians and bilaterians.
This makes sense, for in bilaterians, muscle cells derive from the mesoderm, the third
embryonic germ layer that the four older animal groups lack.
Ryan: “This picture is consistent with the idea of comb jellies as oldest animal group. Or they
would have lost many genes that they originally shared with cnidarians and bilaterians. That
seems unlikely.”
Unconvinced
But after so many conflicting results from molecular phylogenetic analyses, biologists now
are cautious. Prof. Dr Gert Wörheide (Ludwig Maximilian University of Munich), together
with others, showed last year how sensitive such research is for the selection of genes, species
and outgroups included in the analyses (Integrative and Comparative Biology, March 2013;
Molecular Phylogenetics and Evolution, April 2013). Similar analyses can yield completely
different evolutionary trees – and all with high statistical reliability.
He suspects that the previous finding of comb jellies as the oldest animal group had been an
artifact, and he is not convinced that it is different now. As yet, he holds to the classic idea
that sponges were the first animal group to split off, and that comb jellies appeared later, but
that their exact position cannot be resolved with confidence at present.
Also Prof. Dr Nico van Straalen (Free University of Amsterdam) is not convinced: “There are
many similarities between comb jellies and cnidarians and it is difficult to assume that they all
are convergences.”
But Ryan contends that comb jellies and cnidarians, despite their superficial similarities, are
in fact very different: “In contrast to cnidarians, comb jellies have eight rows of combs with
cilia for locomotion. They have colloblasts that secrete a sticky substance to catch prey, and
lack the stinging cells that cnidarians have. Their nervous system is unique. And their
development is different: they go through a cydippide larva stage, while cnidarians have a
planula larva.”
Van Straalen and Wörheide also mention a technical flaw. Ryan and colleagues used two
methods to construct evolutionary trees: a maximum-likelihood method and a Bayesian
method. The maximum-likelihood method did indicate the comb jellies as the oldest animal
group, but the Bayesian calculations failed to confirm this. “But the maximum-likelihood
method they used should not be used for the kind of data they analyzed, as we have clearly
demonstrated in 2011 (PLoS Biology)”, Wörheide says. Van Straalen states: “Both methods
should give more or less the same results. If they don’t, there were probably too many
assumptions incorporated in the analysis.”
Ryan explains that the Bayesian methods applied in the study did not achieve results: after
runs of more than two hundred days, there was still no outcome. “But now we have a new
program to run Bayesian analyses. We used it and the comb jellies emerged as the oldest
group of animals.”
Sponges hide their complexity
It is for sure that sponges are an old animal group with a long evolutionary history. Despite
their simple appearance – a pitcher with holes, water channels, central cavity and water exit
opening – they have a surprisingly complex genome, as Ana Riesgo (University of Barcelona)
and colleagues recently reported in Molecular Biology and Evolution (online at February 4).
They analyzed the transcriptome (all of the RNA) of eight sponges species and found, among
others, genes that in other animals are involved in cell communication, nervous system and
innate immune responses. “But the thing is that we do not see in sponges the structures in
which these molecules are involved in other metazoans”, Riesgo mails. “And more
importantly, sponges have those genes and they are using them, because all our study was
conducted on expressed genes. In most cases we do not know what function these genes have
in sponges.”
So, sponges are likely of complex origin and lost features such as a nervous system, of which
they still carry genetic traces. Or they are not as simple as they look. “Sponge larvae are quite
complex, they have a front and back and are responsive to light,” Riesgo says. “But some
species are also complex in the adult stage, they are more than a shapeless mass with lots of
holes.”
A team of researchers in which Riesgo participated showed that sponges have a sensory
system (BMC Evolutionary Biology, online at January 13); the team describes the system in
the freshwater sponge Ephydatia muelleri. When stimulated, many sponges ‘sneeze’. The
entire body expands and then retracts in a coordinated manner, propelling water through the
exit opening, the osculum. The researchers discovered that cells lining the osculum have cilia
of a sensory type. In other animals, such cilia perceive movement, taste, smell, light or
temperature. The sponges’ cilia, the researchers think, are sensors that turn on the sneeze
reflex when needed.
The findings of sponge complexity are compatible with the evolutionary tree of Ryan, in
which the complex looking comb jellies are older than sponges. But whether either sponges or
comb jellies are the oldest animal group, the Metazoan ancestor must have been rather
complex too. And that makes sense: as a multicellular animal, it must at least have had some
kind of cell communication and allorecognition.
The enigmatic Trichoplax
It is difficult to place Placozoa in the animal tree of life. In some trees, these animals appear
as the oldest group of animals, but in other trees their place is next to the bilaterians. The
entire clade of Placozoa is represented by only one known species, Trichoplax adhaerens,
which lives in tropical and subtropical coastal waters. This tiny creature consists of a few
thousand cells of only four different types. It has no structure whatsoever, not even a mouth
opening. It eats protozoans by crawling on top of them, after which their lower cells digest the
prey.
This animal, like sponges, has a genome that is more complex than suspected, with, among
other, genes that in other animals are involved in cell communication. Biologists from Utrecht
University last year showed that these genes are expressed (Nature Communications 2013).
According to Ryan, the Placozoa split off after comb jellies and sponges .
References
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