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ARTICLE
Where Are My Genes? Genomic
Considerations on Darwin’s Doubt
Michael Buratovich
In his book Darwin’s Doubt (Meyer 2013), Discovery Institute philosopher of science and
“intelligent design” proponent Stephen C Meyer makes some very unorthodox claims about
animal origins. Evolutionary developmental biologists have shown over two decades of
work that regardless of how animals look, most of them use a common “toolkit” of genes
for their development. Furthermore, a respectable body of evidence shows that changes in
animal body plans and body parts are driven by changes in gene regulation (Carroll 2000).
Meyer, however, breaks with this contemporary thinking and argues that the diversification of animal body plans during the Cambrian explosion, in a time period “lasting only 5
to 6 million years” (Meyer 2013:72), must have required the creation of new genes. His reasoning stems from the increased number of cell types in Cambrian animals relative to their
earlier counterparts. Increased numbers of cell types, to his thinking, means an increased
number of genes to encode the proteins that characterize those cell types. Meyer writes:
During the Cambrian period, a veritable carnival of novel biological forms arose. But
because new biological form requires new cell types, proteins and genetic information, the Cambrian explosion of animal life also generated an explosion of gene information unparalleled in the previous history of life. (Meyer 2013:163)
Meyer further claims that these new genes, which drove animal diversification, must
have encoded novel protein structures known as protein folds. His reasoning is relatively
straightforward. Protein folds, or domains as they are also called, are the “smallest unit of
structural innovation in the history of life,” and building “fundamentally new forms of life
requires structural innovation. And new protein folds represent the smallest selectable unit
of such innovation” (Meyer 2013:191).
However, according to Meyer, the generation of new protein folds runs into a probabilistic
Rock of Gibraltar, since the “probability of any given mutational trial generating (or ‘finding’) a specific functional protein among all the possible 150 amino-acid sequences is 1
change in 1077” (Meyer 2013:200). Meyer contends that these odds make it far too unlikely
that random mutation and natural selection could generate a new protein fold, and therefore, we need a new model, specifically “intelligent design,” to explain the origin of animal
life.
I will address Meyer’s mistaken probability argument elsewhere (Buratovich forthcoming),
but most of Meyer’s remaining assertions in the above paragraphs are likewise simply mistaken. The evolution of Cambrian life was not restricted to 5–6 million years but was the
culmination of millions of years of animal evolution, and animal diversification does not
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require the evolution of new genes and proteins. Don’t get me wrong; I am all for challenging current paradigms, but not when current knowledge in the field is misrepresented
in order to do so.
B u r r ow i n g i n t o t h e P r e c a m b r i a n
Period
Middle
510
Cambrian
540
580
Tommotian
First arthropod and echinoderm body fossils
Arthropod traces
First brachiopod and mollusk fossils
Small shelly fossils increasing in
diversity through time
Rich Ediacaran and Vendian fossil assemblages;
trace fossils are still small, chiefly horizontal,
first small shelly fossils
“Vendian”
570
Chengjiang fauna
Cambrian Explosion
Larger burrows (such as Treptichnus pedum),
some penetrating
550
560
Burgess Shale fauna
Atdabanian
Manykaian or
NemakitDaldynian
Neoproterozoic
Millions of years ago
530
Toyonian
Botomian
Phanerozoic
520
Fossil Events
Siberian Stages
Lower
500
Era
Meyer is correct when he says that more complex animals require greater numbers of cell
types. But Meyer wants to restrict the entirety of this explosive increase in structural complexity to the duration of the Cambrian explosion (circa 521–514 million years ago [mya]),
during which large numbers of structurally diverse animals first appeared in the fossil
record (Peng and others 2012). Thus Meyer claims that animals diversified within a time
period “lasting only 5 to 6 million years” (Meyer 2013:72). However, he largely ignores organisms discovered in the lead-up to the Cambrian explosion.
Various fossils from multicellular organisms,
including embryos, rare body fossils, and
small horizontal trace fossils
590
600
F i g u r e 1. Fossil events in the Cambrian and Precambrian.
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Geologists have subdivided the Cambrian period, which extends from 542–488 mya, into
shorter, successive stages (Figure 1). Before the stage that includes the Cambrian explosion (known as the Atdabanian stage), there were the Tommotian (529–521 mya) and
Manykaian or Nemakit-Daldynian (542–529 mya) stages. Analyzing fossil finds from each
of these stages as well as from the Precambrian makes it clear that animal diversification
was already well underway by Meyer’s 5–6-million-year window.
Extensive trace fossils are found in Precambrian rocks as far back as approximately 560
million years. Trace fossils include burrows, footprints, tracks, and trails. While not preserved remains of organisms themselves, trace fossils can provide important information
about the animals that left them. Their bodies may not have been preserved, but from
these traces we can draw inferences about their morphologies and biological activities
(Droser and Gehling 2012). The organisms that left Precambrian trace fossils, for example,
were almost certainly soft-bodied, less than 1 cm long, and 1 or 2 mm in diameter—about
the same diameter as the grains of sand that compose the rocks they were encased in.
Paleontologists, therefore, have given scientific names to the burrows left by these organisms, since they were left by living creatures. This is to help codify the fossilized activities
of the creatures that lived during these geologic time periods even though their bodies
were not preserved.
The oldest Precambrian trace fossils are relatively simple and consist of surface trails or
horizontal burrows. Later in the Precambrian period, the diversity of trace fossils increases,
as does their complexity. Instead of simple, straight traces, later Precambrian trace fossils
show irregular, meandering crossing trails, meandering sinusoidal trails, irregular branching burrows, and a variety of stuffed burrows in which the burrowing organisms actively
backfilled their tunnels with sediment. Vertical burrows become common around the Precambrian/Cambrian border, as do more complex traces that become progressively larger.
These include elaborate branching burrows, spiraling traces, and spreite burrows, which
are curved layers formed by the organism tunneling back and forth through sediment,
presumably in search of food (Crimes and Droser 1992).
Burrowing requires the ability to rework underlying soils or sediments. To leave these fossil traces, the animals must have been capable of coordinated movement, which implies
that they possessed an array of muscles controlled by a relatively complex nervous system.
The nervous system must have been capable of mediating behaviors that includes the control of longitudinal and radial muscles in the body wall that work antagonistically to each
other to shorten and then elongate the animal. Additionally, because many burrows are
lined with fossil fecal pellets, these animals also almost certainly possessed well-developed
digestive systems. And finally, we can infer that these burrowing animals had a fluid-filled
body cavity to provide necessary firmness (Valentine 2004:216). All of these anatomical
features also characterize the later Cambrian fossil life for which it is so famous; the only
thing missing is the exterior exoskeleton and jointed appendages.
The appearance of the distinctive burrow network, Treptichnus pedum, identifies the advent of the Cambrian period. Treptichnus pedum shows a series of burrows with curved
branches that represent feeding probes that penetrate the overlying sediments (Valentine
2004:179). The animal that left this trace fossil is doing more than simply burrowing below
the substratum to get away from predators, as earlier creatures did. Instead, this animal is
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coming to the surface to feed, which constitutes a novel behavior in the history of burrowing life. The peculiar form of this trace leaves little doubt that it was formed by an animal
with a central digestive system and sophisticated neural system (Budd and Jensen 1998,
2000). The nervous system of this organism adumbrates the complex nervous systems of
animal with jointed appendages (for example, arthropods). T pedum appears about 10 million years before skeletonized fossils become common and about 20 million years before
the Cambrian explosion. Thus, the ancestors of major animal groups with all their interesting cell types diverged during the late Precambrian and not during the Cambrian. These
events in animal evolution set the stage for the later Cambrian explosion, and their omission by Meyer is a serious oversight.
Something old, something new
Did animal diversification require new genes? Contemporary evolutionary biology does not
view the derivation of new genes as necessary for the diversification of animal body plans.
This conclusion stems from genomic studies of simple invertebrates and a survey of the
developmental genetics of different types of animals.
Bilaterally symmetric animals (those animals whose adult bodies can be divided only
in one plane, such as worms, mollusks, arthropods, and vertebrates) share eight major,
conserved signaling pathways that are used during development: (1) Wnt/TCF, (2) TGF–β/
MADS, (3) Hedgehog/Ci, (4) Nuclear Hormone Receptor, (5) Receptor tyrosine kinase, (6)
Notch, (7) TollR/Rel, and (8) JAK/STAT (Erwin and Davidson 2002, 2009). A gene, protein,
or pathway is considered “conserved” if has undergone relatively few changes throughout
its evolutionary history; that is, there have been few (if any) extensive mutational changes
since it first arose.
Such conserved entities—be they genes, proteins, or pathways—have detectable similarities—in nucleic acid sequences, amino acid sequences, or pathway components, respectively—among different organisms. The varied deployment of the eight conserved pathways
during development among bilaterally symmetric animals establishes the peculiar forms of
these animal groups. Thus, animals achieve their final disparate forms not by using new
genes (or completely different genes) that encode novel proteins with brand-new protein
folds, but through the differential expression of a common set of evolutionarily conserved
genes that encode components of signal transduction pathways. This strongly suggests that
the evolution of animal diversity was driven not by the creation of new genes, but by the
increasingly creative use of already existing genes.
But while all animals use versions of the same signaling pathways, it might be argued that
they arose all at once during the Cambrian explosion, thus maintaining Meyer’s argument.
However, when we examine the genomes of extant organisms closely related to animals
as well as structurally simple animals whose ancestors originated in the Precambrian and
earlier, it is clear that the majority of the body plan signaling pathways were in place well
before more complex animals arose (Table 1).
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Organism
Type
TGF–β /
MADS
Hedgehog/
Ci
NHR
RTK
Notch
TollR/
Rel
JAK/
STAT
Conserved Signaling Pathways in the Sequenced Genomes of Various Organisms
Wnt/TCF
Ta b l e 1.
Capaspora
owczarzaki
Filasterean (singlecelled)
–
–
–
–
+
~
–
~
Monosiga
brevicollis
Choanoflagellate
(singlecelled)
~
–
~
–
+
~
~
~
Trichoplax
adhaerens
Placozoan
(small, flat
animal)
+
+
–
+
+
~
~
~
Amphimedon
queenslandia
Sponge
+
+
~
+
+
+
+
~
Oscarella
carmella
Sponge
+
+
+
+
+
+
+
+
Hydra
Cnidarian
magnipapillata
+
+
+
+
+
+
+
–
Nematostella
vectensis
+
+
+
+
+
+
+
~
Cnidarian
+ the genome encodes all the components of this signaling pathway
– the genome shows no convincing evidence that it contains the components of
this signaling pathway
~ the genome either encodes some but not all of the components of this signaling
pathway, or encodes incomplete components of this signaling pathway
Looking at the two unicellular organisms in the table, Capsaspora owczarzaki and Monosiga brevicollis, we can see that at least one of the signaling pathways conserved among animal groups has its genesis in closely related single-celled organisms (King and others 2008;
Manning and others 2008; Suga and others 2013). Capsaspora owczarzaki is a filasterean,
a group closely related to choanoflagellates (Shalchian-Tabrizi and others 2008; Torruella
and others 2012). Monosiga brevicollis is a choanoflagellate that looks like the feeding cells
of sponges and is the closest living relative of animals (Lang and others 2002; Steenkamp
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and others 2006). The genomes of both of these single-celled organisms encode the components of the RTK (receptor tyrosine kinase) pathway, which is used by such important
signaling molecules as insulin, epidermal growth factor, and other growth factors (Schlessinger 2014). In addition, the genome of C owczarzaki encodes transcription factors that act
downstream of some signaling pathways in metazoans, such as CSL (Notch–Delta pathway)
and STAT (JAK–STAT pathway), whereas their upstream-acting proteins are missing (Suga
and others 2013). The genome of M brevicollis contains transcription factors that are used
in the Wnt signaling pathway, a Hedgehog-like gene, all the domains of the Notch protein
in separate genes, a Toll-interacting protein (Tollip) that regulates Toll-like receptors, a
JAK-like kinase and a STAT-like gene. The genome of M brevicollis also encodes a host of
cell adhesion molecules and extracellular matrix molecules that are important in the development and structure of multicellular animals (King and others 2008). Thus, the seeds of
those components integral for multicellularity are found in the genomes of those unicellular organisms that are most closely related to modern animals. This strongly suggests that
such molecules were available long before the Cambrian period.
As we move from unicellular organisms to multicellular organisms, we encounter different
cell types assembled into tissues. Animals are referred to as “simple” if they have relatively
few cell types, and “more complex” if they possess more cell types. Sponges, for example,
are regarded as simple animals because they possess neither a nervous nor a digestive
system, and they are universally regarded as the most primitive—or basal—of all fossil
and living animals (Richter and King 2013). The earliest undisputed sponge fossil, Paleophragmodictya reticulata, dates to approximately 600 million years ago, which is tens of
millions of years before the appearance of the first Precambrian trace fossils (Martin and
others 2000). Note, however, that the genome of the sponge Amphimedon queenslandia
contains at least some of the genes for all eight of the highly conserved signaling pathways
used in animal development (Srivastava and others 2010). The genome of the sponge Oscarella carmella contains all the core components of these conserved signaling pathways
(Nichols and others 2006).
Cnidarians have bodies composed of an inner and outer layer of cells, with a jellylike layer
called the mesoglea sandwiched in between. Cnidarians have digestive and nervous systems and stinging cells known as cnidocytes, from which the group gets its name. Modern
cnidarians include the corals, sea anemones, jellies, and Hydra, the genomes of which
contain all but one of the most conserved signaling pathways (Putnam and others 2007;
Chapman and others 2010).
Many organisms whose genomes lack particular signaling pathways contain what appear
to be the beginnings of them. For example, Trichoplax, a tiny (1-mm-wide) flattened creature is composed of only four cell types. No extant animal has a simpler structure. Its
genome, however, contains components of the Notch, JAK/STAT, and TollR pathways (Srivastava and others 2008). The genome of the sponge Amphimedon contains partial elements
of the Hedgehog and JAK/STAT pathways (Srivastava and others 2010). Interestingly, the
sponge genome also contains over 30 different families of genes that encode proteins of
the “post-synaptic density (PSD).” Neurons, the cells in the nervous system responsible
for the production and propagation of nerve impulses, have arrays of cell-surface proteins
that orchestrate the transmission of nerve impulses from one neuron to another, across a
space known as a synapse. The PSD properly organizes this machinery in the membranes
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of neurons so that it functions properly (Gao and others 2013). Thus even though sponges
have no neurons, they synthesize an almost complete set of PSD proteins. These PSDspecific genes are expressed in the free-swimming larvae of the sponge, in “flask cells,”
which seem to serve as chemical sensors (Sakarya and others 2007). This is an example of
“cooptation” or “exaptation” where features (or genes) of an organism used for a particular
purpose are coopted for a new use (Gould 2002:1229–1246). Organisms that possess nervous systems have exapted the PSD proteins used by sponges to detect chemicals to make
synaptic connections between neurons. Likewise, even though the genome of the starlet
sea anemone Nematostella vetensis lacks a complete JAK/STAT signaling pathway, it does
encode the Stat5 gene, which is one of the components of this signaling pathway (Putnam
and others 2007).
A brief survey of cnidarian genomes shows that genes encoding at least some of the components of the most conserved signaling pathways are present in almost all surveyed species. These modern cnidarian species either inherited these signaling pathway genes from
a common ancestor or evolved them independently. However, if modern cnidarians independently evolved these genes, then the genes that encode the components of these signaling pathway should not display the striking similarities between them that they clearly
show (Putnam and others 2007; Chapman and others 2010). Thus modern cnidarian species inherited these genes from a common ancestor rather than evolved them separately.
Since cnidarians are almost certainly represented in the Ediacaran fauna (Scrutton 1979),
which predated the Cambrian period by tens of millions of years, even very ancient genomes were quite complex and contained most of the genes necessary to build today’s
most sophisticated multicellular creatures. The genes for these signaling pathways were
already in place long before the Cambrian period, and the creation of new genes was not
a driving force behind the Cambrian explosion.
Conclusion
Meyer’s entire thesis largely collapses because the genes that he asserts had to be created
in such a short period of time to drive Cambrian explosion were in fact in place millions
of years prior to this famous burst of diversity. This is the one of the main reasons the central hypothesis of his book Darwin’s Doubt has been rejected by mainstream evolutionary
biologists.
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About th e author
Michael Buratovich is Professor of Biochemistry at Spring Arbor University, and is also the associate editor for cell and molecular biology for Reports of the National Center for Science Education.
A u t h o r ’ s a d d r e ss
Michael Buratovich
Spring Arbor University
106 E Main Street
Spring Arbor MI 49283
[email protected]
Copyright 2015 by Michael Buratovich; licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License. http://creativecommons.org/licenses/by-nc-nd/3.0/
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