Tiny sea squirts' internal
battles offer evolutionary insights
By Kristin Weidenbach
The tiny sea creatures
known as sea squirts are a bundle of paradoxes. Seen as
purple, orange or brown "flowers" in the waters
of Monterey Bay, they are actually advanced animals much
higher on the evolutionary ladder than surrounding corals
or sponges, and more like humans and other vertebrate
animals.
The squirts grow into
thumbnail-size colonies that act as a single animal
the colony has a common blood system and releases sperm
and eggs into the water via a central command. And yet
each of the "petals" of the sea squirt colony
is itself an individual animal with its own heart, mouth
and sex organs.
The sea squirt's position
on the evolutionary ladder and its unusual life cycle
makes these animals intriguing to evolutionary biologists
and immunologists like Irving Weissman, MD, professor of
pathology and developmental biology and the Karel H. and
Avice N. Beekhuis professor of cancer biology.
Weissman and his
colleagues have found that when it comes to sea squirts
you cannot trust what you see. Neighboring colonies
compete with each other for seaweed or rock real estate,
leading to fierce internal battles of natural selection.
Unless you scrutinize a colony's genes it is impossible
to know whether the sperm and eggs it harbors are truly
its own, or the squirt has become the unwitting
distributor of the reproductive cells of a domineering
neighbor.
Stanford researchers'
attempts to unravel this conundrum are yielding support
for a provocative evolutionary theory. While some people
question the entire theory of evolution, even those who
subscribe to the theory generally agree that natural
selection occurs at the level of a single individual. But
Weissman and his colleagues have shown that in certain
organisms like sea squirts that live in intimate
colonies, selection is occurring within organisms.
The researchers have found
that individual genomes the entire set of genes
carried by an organism are battling it out. The winner
of the genome struggle populates the reproductive organs
of the squirt so that any offspring are genetically
related to the genome conqueror rather than the
individual that physically releases the sperm or egg.
Such behavior would seem to represent natural selection
at its selfish extreme.
"Literally, you
cannot believe your eyes," senior author Weissman
writes in a paper describing the team's findings,
published in the August 3 issue of the Proceedings of the
National Academy of Sciences. "Because the phenotype
that is represented by the body may not represent the
genotype that is transmitted by the gonads."
Sea squirts are vulnerable
to this type of genetic sabotage because of the phase of
their life cycle that they spend as part of a colony.
When a tadpole-like sea squirt larva settles down in a
tidal pool it begins budding to produce a colony of
genetically identical squirts. Like humans and other
organisms that lead a separate existence, all the members
of this sea squirt colony carry the same genes in their
sperm or eggs and in the cells that form the body of the
animal.
Squirt problems can arise
when a tadpole from a different colony settles nearby and
begins building its own colony kingdom. Cramped in
amongst the rocks, the two different colonies can grow
close enough to touch and may merge into a super-colony
better able to withstand predators. Then the internal
power struggles begin.
Of the two colonies that
have fused, one of them is usually absorbed and by all
outward appearance, has disappeared within a few weeks.
But evidence of two genetically distinct animals often
can be found in the blood system of the remaining
super-colony. Cells from both the "winner" and
the "loser" colony can co-exist or one
population of cells may oust the other. In the most
surprising scenario, the body of the super-colony is
populated with cells from the "winner" colony
whereas the sex organs are populated with cells that had
been sequestered there from the "loser" colony.
When this super-colony releases sperm and eggs it will
carry the genes of the "loser" colony, not the
"winner."
Weissman thinks that the
warring cells are stem cells rare cells that retain
the ability to reconstitute an organ system or even the
entire body of an animal. Weissman is widely recognized
as the discoverer of human stem cells and he believes
that in these cells he has found the sea squirt version.
To prevent a single genome
from gradually dominating all the sea squirt colonies
that live in Monterey Bay, Weissman and others believe
that the animal has a genetic security system that
prevents completely dissimilar colonies from fusing at
all. Two different colonies that share none of the
fusibility and histocompatibility genes (Fu/HC) will
recoil and permanently reject each other. Some
immunologists and evolutionary biologists believe that
this acceptance or tolerance of a foreigner is the same
phenomenon that governs acceptance or rejection of an
organ transplanted from one human to another. In both
instances cells are able to recognize self and non-self.
The Fu/HC genetic security
system permits limited fusions between sibling colonies
that will enlarge a colony and make it better suited to
fend off predators. At the same time, it preserves the
genetic diversity of the entire population by preventing
the merger of genetically disparate colonies. With these
limitations, a post-fusion "winner" colony
nurturing sex cells from the "loser" will at
least be supporting a generation of progeny that is
genetically similar to itself.
On a human level it would
be as if an unwelcome visitor infiltrated your home
demanding to be fed and supported. The Fu/HC locus is
like a security guard stationed at the door ensuring that
only kin gain entry because once the intruder is in or
a neighboring squirt colony has fused with you a
battle for control will occur and ownership of the house
or the colony is up for grabs. Better that the
squatter be your sibling or cousin than an unrelated
stranger.
Weissman believes that
learning more about the sea squirts will reveal many
secrets about natural selection and evolution, and even
about the immune system of higher animals.
Co-lead authors of the
study were Douglas Stoner, PhD, a postdoctoral fellow in
Weissman's lab at the Hopkins Marine Station, and Baruch
Rinkevich, PhD, formerly a visiting researcher at the
marine station and now at the National Institute of
Oceanography in Haifa, Israel. The study was funded by
the US-Israel Binational Science Foundation, the Minerva
Center for Marine Invertebrate Immunology and
Developmental Biology and by grants from Systemix/Sandoz.
SR
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