|
A peer-reviewed
electronic journal published by the Institute
for Ethics and ISSN
1541-0099 20(2)
– November 2009 |
Cellular
differentiation as a candidate “new technology” for the Cambrian Explosion
Chris Phoenix
Center for Responsible
Nanotechnology
cphoenix@gmail.com
Journal of Evolution and Technology - Vol. 20 Issue 2 – November 2009 - pgs 43 - 48
http://jetpress.org/v20/phoenix.htm
Abstract
Almost all of the modern animal phyla
appear to originate in a relatively compressed interval of time known as the
Cambrian Explosion. Although several factors have been identified that may have
enabled the Cambrian Explosion, there remains the question of the final
trigger. The development of cellular differentiation, the capacity of a
cellular lineage to become specialized permanently in response to external
signals, is proposed as the trigger. Cnidaria and eukaryotic slime molds, which
pre-date the Cambrian, have specialized cellular functions but their cells do
not appear to differentiate irreversibly. With differentiation, cellular roles
can be fixed during embryogenesis. Fixed cellular roles may have enabled more
complex and more competitive organisms, perhaps by facilitating multi-scale
structures in organs or increasing the stability and reliability of network
systems including synaptic connections. A candidate evolutionary pathway to
cellular differentiation is proposed.
Introduction
For
reasons that have remained unclear, almost all of the modern animal phyla
arrive in the fossil record during a geologically short period of about twenty
million years, starting about 540-545 million years ago (Baker, 2006;
Valentine, Jablonski, and Erwin, 1999). The Cambrian Explosion has been a
unique and troubling anomaly in the history of life.
Various
attempts have been made to explain the Cambrian Explosion. Rapid change
following a long period of quasi-stasis suggests the existence of a triggering
or enabling event, either external to organisms or incorporated in organisms.
It has been noted that the oxygen content of the atmosphere was slowly rising
(Thomas, 1997). This was likely an enabler, and has been suggested as a trigger
by Ohno (1997), but it fails to explain why the development of new body types
was so abrupt. Other proposed enablers include the development of complex
multicellular animals (metazoans) during the previous Ediacaran period, and the
disappearance of the worldwide ice sheets that preceded that period.
Around
the time of the Cambrian Explosion, the geological record indicates several
shifts in the ratio of various isotopes that are differentially concentrated by
metabolism, which implies that biological productivity changed around that
time. However, it has been unclear whether this was a result of some unknown
environmental factor that may have contributed to or triggered the Cambrian
Explosion, or whether it was simply a result of the shifting populations caused
by the Cambrian Explosion (Brasier, Corfield, Derry, Rozanov, and Zhuravlev,
1994).
In
the absence of any clear external trigger, it is reasonable to look for a
biological capability that may have triggered the explosion – a capability, newly developed, which
allowed or promoted the development of diverse and disparate life forms that
were previously not favored, or perhaps not even possible. For example, the
development of eukaryotic cells might have represented a candidate trigger;
however, there is clear fossil evidence of eukaryotes at least several hundred
million years prior to the Cambrian Explosion (
It
has been suggested that the development of eyes triggered the Cambrian
Explosion (Parker, 2003). However, if the Cambrian Explosion was triggered by
the development of a new biological capability, then we should not expect to
find that capability in animals that pre-date the Cambrian by many millions of
years, such as the Cnidarians. Modern jellyfish have Hox genes and and some
have eyes, which suggests that neither of those innovations was the trigger.
Butterfield
(2007) describes the increasing impact of coevolution during the Ediacaran and
early Cambrian periods. A new and highly advantageous biological capability
would make the animal lineage that developed it highly competitive. Instead of
coevolving with existing Ediacaran fauna, the improved animals might quickly
drive many Precambrian lineages into extinction and fill their niches with
rapidly diversifying body plans. A reasonable comparison for the rate of
disruption might be the introduction of rats and other invasive species to an
island ecosystem. It may be worth noting that animals which first appear in the
Cambrian strata are all bilaterian (even starfish have bilateral embryos),
while Precambrian fauna included radially symmetrical animals. This line of
reasoning also suggests that we may be able to identify a trigger by looking
for differences between Cambrian and Precambrian animals.
Cellular
differentiation
Cells
in modern animals are, for the most part, differentiated: locked irrevocably
into particular roles, and incapable of producing tissue types outside these
roles. Cases of dedifferentiation have been observed in the animal kingdom,
notably in the regeneration process of salamanders (Echeverri, Clarke, and
Tanaka, 2001), but these are notable exceptions to the rule. The mechanisms of
cellular differentiation are a topic of ongoing research. Specialization, in
which cells exhibit variable behavior and somatic roles in response to chemical
control signals, must be distinguished from differentiation, in which cells
become near-irreversibly locked into a particular functional role.
Examples
of specialization without differentiation can be found in descendants of
Precambrian animals. For example, the polyps of modern jellyfish include highly
specialized cells, but jellyfish can reproduce by polyp defection,
demonstrating that the descendants of polyp cells are capable of taking on all
necessary roles for a complete animal. Thus, jellyfish cells would be
considered as specialized, but not differentiated. Hox and parahox genes, which
organize cellular behavior into structures as complex as eyes, appear to
pre-date the Cambrian, since they have been found in Cnidarians (Finnerty and
Martindale, 1999); however, the existence of Hox genes is a separate question
from the permanent pattern of expression of Hox or other genes in
differentiated cells. It should be emphasized that in these examples, the
specialized cells retain full flexibility. Indeed, the ability to lock in
patterns of cellular function via differentiation could have evolved only after
specialized patterns of cellular function were established.
It
is useful to explore how cellular differentiation could have evolved
incrementally from pre-existing mechanisms. Methylation is discussed here to
provide an example of a plausible mechanism, and not as the definitive answer;
histone acetylation is another means of altering gene expression. Recent
research on human stem cells has found distinct patterns of methylation that
change as the cells differentiate (Bibikova et al, 2006), and studies of mouse
embryonic stem cells vs. differentiated cells show patterns of difference in
histone methylation (Bernstein et al, 2006). This implies that differentiation
may be implemented, at least in part, by epigenetic modification. Thus,
comparable changes in epigenetic patterns during embryogenesis are predicted in
all animals that emerged in the Cambrian, but not in the Cnidarians.
Random
epigenetic DNA methylation occurs in bacteria, where it is used to control gene
expression over multiple generations, as a sort of genetic “tuning knob” or
meta-evolutionary strategy (Caporale, 2003). Random changes to methylation
patterns can alter gene expression patterns, allowing genes to be turned off
without degrading their sequence; presumably this is useful in allowing
bacterial populations to adjust to cyclical conditions with long time scales.
In
contrast to the random epigenetic changes in bacteria, whatever modifications
are involved in the differentiation process happen at a specific time, in
response to specific signals (for example, signaling molecules during
embryogenesis), and with specific results. The development of a single
mechanism capable of inducing epigenetic change at particular points in the
genome, and at a particular point in time, in response to specific signals,
would have been enough to implement near-irreversible differentiation. For
example, a mechanism to create epigenetic changes on command might have evolved
from a mechanism that preserves epigenetic patterns during DNA copying.
Consequences and
implications
A
specialized but non-differentiated cell would take on whatever role was called
for by the signals it was receiving. The regenerative properties of Hydra show
how easily specialized cells can switch roles. Technau and Scholz (2003) note
that the endodermal and ectodermal cells in Cnidarians can adopt different
fates, at least in the polyp form. A high degree of behavioral flexibility
implies that an organism made of such cells would need to maintain constant
chemical gradients, at some energy cost, in order to preserve its structure.
Intricate organ structures would require sharp-edged gradients, costing even
more energy.
Cellular
slime molds and jellyfish demonstrate that diverse, intricate, collective, and
cooperative cellular behavior can be maintained by signaling (
By
contrast, given a capacity for true differentiation, a cell could stay in its
assigned role indefinitely without energy being expended to “remind it” of its
proper function. When cells can be made to differentiate irreversibly via
external chemical signals, the mechanisms of embryogenesis can be applied at
multiple size scales to produce structures of almost unlimited complexity. A
brief expenditure of signaling energy, sufficient to establish sharp gradients
and intricate patterns for as little as a few minutes, would be sufficient to
create permanent and reliable structures within the organism. This could allow
the development of more intricate and large-scale structures and networks, such
as vascular systems. In particular, preserving reliable function of individual
neurons would enable long-term synaptic learning. Either the development of
more advanced organs or the development of synaptic learning would presumably
have given a substantial advantage to the organism.
If
cellular differentiation is so advantageous, why did it not evolve earlier?
This dovetails with the question of why the Cambrian Explosion was delayed by
many millions of years. A possible answer can be found in the fact that the
descendants of a differentiated cell will all be differentiated, and thus
limited. Therefore, the organism would no longer be able to reproduce by
repurposing any convenient clump of cells, because any differentiated cells in
that clump would need special handling. This implies that, in order to make use
of differentiated cells system-wide, the organism might need to modify its
reproductive pattern; differentiation might not be very useful until the
reproductive adaptations appeared, and might even be selected against. A viable
combination of differentiation and appropriate reproductive apparatus might
take quite a while to evolve. Differentiation might also be difficult to evolve
because an imprecise molecular mechanism, one that caused many epigenetic
changes rather than targeting specific points in the genome, could easily have
unreliable or damaging impacts.
The
differentiation conjecture requires that all post-Cambrian animals descended
from a single organism, presumably bilaterally symmetrical. (Although, as
previously mentioned, starfish appear to be radially symmetrical, their embryos
are bilateral.) This would imply that recognizable ancestors of modern animals
will not be found among the Ediacarans. This parallels the arguments of
Seilacher (e.g. Seilacher, Grazhdankin, and Legouta, 2003) that most of the
Ediacaran fauna are not the ancestors of any modern animals.
Although
it is always risky to look for confirmation of a new hypothesis in previously
available data, it may be worth noting that the features of Ediacaran animals – flat bodies, apparent lack of organs,
only simple patterns of spatial organization, and appearance of being “‘quilted’
together (certainly not segmented in any metameric way)” (Gould, 2002) – might result from the constraints
implied by dynamic and unstable assignment of cellular function. The “quilting”
might result from poorly controlled growth or specialization of cells.
Conversely, the Tommotian organisms – the first to appear in the Cambrian Explosion
– may have had more
sharply defined internal structures, and perhaps may also have had internal
transport structures that provided nutrient transport through three-dimensional
volumes (Gould, 1989).
Conclusion
The
Cambrian Explosion, and the fossil record surrounding it in time, have raised
many difficult questions about evolution. An understanding of why the Cambrian
Explosion happened when it did, and why it was so rapid once it began, would
begin to answer major questions about the mechanisms of evolution and the
origins of complex animal life.
The
abruptness of the Cambrian Explosion –
the rapid production of nearly all modern animal forms –
is indirectly answered by the differentiation conjecture. The development of
finely ramified organs, perhaps in conjunction with synaptic learning, would
represent a significant broadening of the evolutionary space; in addition,
Cambrian animals would have been able to outcompete Ediacaran animals, driving
many of them extinct and opening still more niches. The development of motile
target-seeking predation, which apparently was rare or non-existent in
Ediacaran times, would have fueled an arms race, which has been recognized by
Gould and Butterfield, among others, as a driver of rapid evolution.
Although
environmental factors surely set the stage for the Cambrian Explosion, cellular
differentiation, as a capability developed by a particular lineage of organisms
which then diversified rapidly, is a strong candidate for the final trigger.
Acknowledgments
The
author wishes to thank Joao Pedro de Magalhaes, Rebecca Mancy, and Jonathan Vos
Post for helpful comments on an earlier version of this paper.
Based
on a paper presented at the BIL conference, March 1,
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