A longer evolutionary history restricts novel adaptation in animals

Ariel E. Marcy
Department of Biology, Stanford University

Five hundred and twenty million years ago, the Cambrian explosion produced the largest diversity
in body plans the world has ever known. About 100 different phyla emerged by the end of this era
including all 30 extant today (Rozhnov 2010). Since then, the number of phyla has dwindled despite
an overall increase in lower taxonomic ranks, such as families (Knoll 2006). Theories for the
explosion include greater ecological opportunity during the Cambrian, but this does not explain why
no new phyla appear after the Permian when other opportunities were granted.
The fossil record suggests the animal ability to generate novel adaptations, such as those that
distinguish higher taxonomic ranks, peaks early and decreases with time and subsequent
specialization (e.g. Erwin et al. 1987). Evolutionary theory predicts the pattern of biodiversity seen
in the fossil record by modeling how early organisms generate adaptations (Kauffman 1989). When
primitive, less fit animals readily mutate their early ontogeny, the resulting morphological
characters drive divergence of high level taxonomic groups (Kauffman 1989). A recent synthesis of
developmental genetics proposes gene regulatory networks as evolutionary significant generators of
morphological change (Davidson and Erwin 2010). Mirroring the hierarchical organization of taxa,
the hierarchical design of these DNA regions allows rapid evolution at first, but each viable
modification restricts the scope of subsequent developmental changes (Davidson and Erwin 2010).
Thus as animal life evolves over time, their ability to generate viable novel adaptations decreases,
producing higher taxonomic groups first and then filling in with families, genera, and species.

The Cambrian Explosion: interpretations of the fossil record

The rapid Cambrian proliferation of high taxonomic groups intertwines with early metazoan
animals at their most unconstrained. As such, the Cambrian explosion is central in understanding

why animal diversity fills in top-down. This section will discuss whether this event actually is an
explosion, the distinction between phyla and body plan, and the pivotal role of mutation in
radiations of high taxonomic groups.
An explosion characterized by rapid diversification of the highest taxonomic groups is
persuasive evidence for decreased evolutionary constraint earlier in multicellular animal evolution
because it requires higher order differences to appear first. Proponents of the long slow
accumulation origin of phyla, however, have suggested that the explosion is an artifact of geological
preservation (e.g. Cohen 2005). Most of our knowledge comes from a few well-preserved
Lagersttten, which could give the impression of sudden phyla while small accumulations of
changes over millions of years went unpreserved. This taphonomic argument is rebuffed by the lack
of large metazoan animals in slightly earlier sites with comparable geological conditions (Knoll
2006). The diversity of well-preserved protist acritarch assemblages increased around the
Cambrian (Knoll 2006). As a reasonable marker for overall marine diversity, this supports a sudden
increase in animals (Knoll 2006).
The fossil record thus brackets the duration of the explosion the divergence of major
taxonomic groups - to ~20 million years (Fig. 1) (Conway Morris 2000). While some suggest the
half a billion years granted by the Phanerozoic Eon would not be enough for the most primitive
phyla to gradually accumulate random changes to evolve into the most complex (Rozhnov 2010).
Furthermore, within extant phyla, defining body plan characters are remarkably stable rendering
them readily identifiable over 500 million years of fossil deposits (Rozhnov 2010). Thus the fossil
record demonstrates relative unconstraint before phyla diverge but not after.

Several hundred million years after the Cambrian explosion, the Permian extinction
eradicated 96% of species producing another large radiation in its wake (Kauffman 1989). In marine
organisms, the new genera and families proliferated at about the same rate as in the Cambrian, but
no phyla or classes emerged (Erwin et al. 1987, Rozhnov 2010). Kauffman summarized the
difference with, The Cambrian filled in from the top down; the Permian witnessed filling in of
higher taxa from the bottom up (Fig. 2). The entire Phanerozoic shows a decreasing trend in the
appearance of maximum taxonomic rank in radiations following major extinctions (Rozhnov 2010).
Since taxonomic rank roughly corresponds to degree of divergence, this result in comparison to the
Cambrian supports increasing constraints on animal morphology inherent in a longer evolutionary
history.
The most serious contradictory evidence comes from molecular data, which dates animal
divergences beginning 100 my earlier than the Cambrian explosion (Conway Morris 2000b). In an
effort to resolve the phylochronology of metazoans, Yang et al. analyzed molecular data in
arthropods, which they argue will be representative of other animal phyla (Fig. 1). Their molecular
evidence suggests the major metazoan phyla diverged in a blistering 15my time span in the great
Metazoan Radiation Event (MRE) (Yang et al. 2007). The MRE took place in the late Vendian about
100my earlier than the Cambrian explosion. This study pushes the appearance of arthropod phyla
away from the Cambrian explosion and back to the MRE, with sub-phyla divergences in this clade
occurring during the explosion (Yang et al. 2007). These data further corroborate the evolutionary
trend of highest taxonomic ranks radiating first followed by the next tier of taxonomic rank.

Figure 1. The Precambrian context and other events leading up to the explosion: Metazoan chronology
comparing early fossil record, molecular dates and palaeoenvironmental background. (A) Molecular dating
results (B) Early metazoan fossils and the geological context in South China. (1) Strongly negative d13C
anomalies (2) approximate position of arthropod-like fossils found in the Ediacara biotaSpriggina (3)
interval of first fossil bilaterians found in South China (3) molecular estimate for the origin of bilaterian
crown groups (4) approximate position of the first large, spinose acritarchs with high diversity found in
South China. Radiometric dates marked with stars. Grey boxes: time intervals of metazoan radiation
recovered by molecular data (A) and the fossil record (B), representing the great Metazoan Radiation Event
(MRE) and the Cambrian Explosion (CE), respectively (Yang et al. 2007).

But, molecular evidence cannot provide insights into the anatomical changes of organisms
(Conway Morris 2000b). Similarly, we must be careful not to equate the molecular divergence of
phyla with the instantaneous acquisition of all the body plan characters defining (Budd and Jensen
2000). Budd and Jensons phylogeny (Fig. 3) disentangles the concept of phyla from body plan.
A phyla represents the monophyletic clade arising after divergence from a sister phyla and a body
plan the set of characters defined by the crown group. As the cladogram shows, a body plan will be
a combination of primitive traits shared with the sister phylum and derived traits acquired after their
divergence.

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Figure 3. The cladistics of phyla and body plans (Conway Morris 2000a)

This framework allows the unfamiliar Vendian phyla be interpreted as a stem-group that
possess some, but not all, of the traits that define Cambrian phyla (Conway Morris 2000b, Rozhnov

2010). Molecular evidence suggests the MRE witnessed rapid divergence of clades of phyla over a
span of 15 million years (Yang et al. 2007), however, recognizable body plans, resolve afterwards
with the input of derived traits (Conway Morris 2000b). Stem echinoderms, for example, share
bilateral symmetry with their sister phyla, the chordates (Rozhnov 2010). The characteristic 5-sided
radial symmetry of crown echinoderms associated with a reorganization event of Hox genes and
represents a derived trait acquired some time after the echinoderm-chordate divergence (Rozhnov
2010). As Conway Morris stated his synthesis, the cladistic understanding of phyla and body plan
will offer evolutionary insights into the roles of pre-adaptation, morphological constraint, and cooptions of gene function (Conway Morris 2000a). How these concepts relate to decreasing
evolutionary novelty will be discussed below and in the two remaining sections, respectively.
To explain why phyla diverge and body plans assemble during the Cambrian, some
hypotheses cite ecological opportunities as the main drivers and with good reason important
events in animal evolution very often correspond to climatic signals (see Fig. 1). Animal
multicellularity occurred in a time of increased oxygen (Yang et al. 2007); the great Metazoan
Radiation Event and Cambrian explosion followed the extirpation of biomass by two ice ages and a
transient shallow water anoxia episode (Knoll 2006). Clearly, significant environmental changes
elicit correspondingly dramatic responses in organisms, but ecological upheavals have preceded
every radiation since the Cambrian without reproducing it (Kauffman 1989).

!
Figure 2. Taxa fills in top down: The evolution of biological diversity in the Phanerozoic: the upper portion
shows the change in the number of genera of marine animals in the Phanerozoic (Sepkoski, 1995), the lower
portion shows the maximum rank of new taxa, appearing at the major boundaries in the Phanerozoic
(Rozhnov, 2001). Numbers show the geological age in Ma dating back from the present.

Evolution implies an accumulation of traits, which some have extended to the acquisition of
traits such as eyes or burrowing behavior to enter new ecological roles, like macroscopic predation
or filter feeding on the seafloor (e.g. Conway Morris 2000). Conway Morris posits that the
subsequent trophic interactions will cause cascading radiations, evidenced by sudden abundance of
defensive hard shells and bustling benthic communities (Conway Morris 2000). Cohen criticizes

this theory because it assumes these traits already exist in the populations of these organisms, preprimed for predatory selective pressures (Cohen 2005). Furthermore, the ancestors of the
mineralized metazoan lineages were all free-swimming pelagic organisms, if faced with sudden
predation, active evasion or camouflage would be more likely responses than mineralization (Cohen
2005).
Instead, Cohen posits mineralization as a pre-adaptation for defense, with an original
advantage for settling in the nutrient-rich, stable, yet depauperate benthic ecosystems following the
shallow water anoxic event (Cohen 2005, Knoll et al. 2006). Knoll predicted this event would
create permissive ecologies in which novel (and not necessarily fitter) mutants generated by
surviving populations could persist and expand under low selective pressure, providing raw
materials for evolutionary innovation (Knoll et al. 2006). Cohens data supports Knolls theory as
benthic mineralization was derived from shared metazoan biochemical pathways in at least seven
different and unrelated ways by as many pelagic lineages (Cohen 2005). All three scientific groups
posited subsequent trophic or community interactions with pre-adapted mineralized benthic clades
produced the sudden appearance of high benthic diversity.
While Cambrian researchers disagree on the details of what caused the explosion, as
demonstrated above, theories of ecological opportunity and trophic interaction complement each
other. I argue, however, that the importance of pre-adaptations in producing biodiversity is
understated. In the scenario above, biochemical pathway mutations allowed multiple lineages to
adapt in a low selective pressure environment, accommodating seven different colonizations and
subsequent niche broadening of each clade (Cohen 2005). The mutations then provide fodder for
pre-adaptations, which in this case fundamentally changed the way these organisms interacted and

co-evolved with the community assemblage (Conway Morris 2000). Thus mutations producing
niche-broadening pre-adaptations represent the rate-limiting step in a process determining which
morphological novelties persist. Therefore the amount of morphological constraint organisms
inherit from their evolutionary history has a direct, and I argue, the most salient effect on the rank of
taxonomic groups appearing after extinction events. This hypothesis can be tested from a theoretical
point of view.

Morphological constraint and theoretical evolutionary frameworks

Evolutionary theorists have proposed frameworks to model the evolution of organisms
through time, focusing in particular on the fate of mutants. Building on Wrights adaptive landscape
framework (Fig. 4), they predict how early multicellular animals would explore the morphospace.
This section will outline the theoretical framework proposed to explain the pattern of diversification
around the Cambrian. As seen in the fossil record, the theories predict an increasing constraint with
time in animal abilities to produce novel adaptations and a decrease in the rate at which viable
mutations are introduced.
Wrights adaptive landscape visualizes the relationship between phenotype and fitness (Fig.
4). The shape of the landscape is determined by the epistatic interactions among genes, which create
local optima for several phenotypes in the context of a niche (Kauffman 1989). A population of
organisms is represented as point on the landscape. Populations located in valleys have relatively
low fitness but also a greater number of viable mutations available and possible adaptive walks
across the landscape. When a population is not on a local optimum, directional selection acts on the

populations, such that it hill-climbs in small steps until it maximizes fitness by conquering a local
optima.

Figure 4. The adaptive landscape

!
Kauffman extends this idea in his concept of rugged adaptive landscapes, which have a
multitude of peaks near and far away from any given point (Kauffman 1989). If the earliest
multicellular animals begin in a valley, he hypothesized two ways to navigate the landscape via
mutations (Kauffman 1989). The first is through the traditional gradual climbs, in which small point
mutations in protein-coding DNA create small substitutions in amino acid chains (Kauffman 1989).
This slow route of evolutionary change does not modify mutants much from original population
i.e. move them far from their original adaptive valley (Kauffman 1989). Furthermore, mathematical
models predict a doubling in time to the next improvement uphill, further decreasing the rate of
evolution (Kauffman 1989). As the fossil record demonstrates, slow accumulations of change
cannot explain radiation events like the Cambrian explosion.
The second option, however, moves organisms across the landscape in long-jumps, via
mutations affecting early ontogeny (Kauffman 1989). The resulting novel mutants land in an

unoccupied niche not adjacent to the original population in valley called hopeful monsters their
likelihood of increasing fitness is at first, much higher than their hill-climbing relatives (Kauffman
1989). Within one generation, the hopeful monster may become reproductively isolated from its
parental population in this fast, yet risky venture of modifying early developmental features
(Kauffman 1989).
When Kauffmans framework is applied in time, it predicts three rough time scales for a
theoretical metazoan radiation (Kauffman 1989), which I argue is supported by fossil and molecular
evidence (Fig. 5).
1) Fitter long jump mutants out-compete less fit hill-climbing relatives. In this stage, longjumping hopeful monsters find success much quicker than the ponderous hill-climbers.
Furthermore, Kauffman suggests the long-jump process can be iterative, allowing the organisms to
skip across the rugged landscape, populating a wide range of peaks (Kauffman 1989). These
conditions, where novel changes occur rapidly and phyla are founded (Kauffman 1989), correspond
to the emergence of phyla in MRE discussed in Yang et al. 2007. I suggest iterative long-jumping
underpins the successive input of derived characters accumulating into the cladistic definition of a
body plan. For example, the derived reorganization event of Hox genes conferring 5-sided radial
symmetry to echinoderms (Rozhnov 2010) fits the long-jump mutation requirement of affecting
early development.
2) The rate of finding fitter long-jump mutants decreases rapidly and eventually becomes
slower than hill-climbing mutants. Now nearby local optima are conquered and classes and orders
fill in around phyla (Kauffman 1989). These correspond to the taxonomic ranks that appeared in
arthropods in the Cambrian explosion (Yang et al 2007). The seven convergent mineralization

pathways provide examples of mutations effecting later stages of ontogeny (Cohen 2005) and thus
more local hill-climbing. Their most recent common ancestor would likely include the hopeful
monster that acquired the shared biochemical pathways (Cohen 2005).
3) Local optima are reached, and biodiversity reaches a stasis. Long-jumps are not favored,
so higher level taxa are not formed during these events (Kauffman 1989). Lower taxa can diverge as
slow environmental changes shift local optima, prompting small short bursts of mole-hill-climbing.
The signature of this in the fossil record is not as clear. The Paleozoic following the Ordovician
radiation is known for an unprecedented stasis in biodiversity but major and rapid climatic events
also occur during this time (L. Hadly, pers. comm.).

1) MRE

Figure 5. Navigating the rugged adaptive

landscape of the fossil record
Histogram displays of the distributions of
times of appearance of animal phyla, classes,
and orders in the marine fossil record. The
width of each histogram bar is 10 MY. Solid
bars indicate taxa with durably skeletonized
representatives and open bars indicate taxa
with exclusively soft-bodied or lightly
sclerotized members. Note that all
distributions are skewed with modes over the
early Paleozoic (Erwin et al. 1987).

2) CE

3) stasis?

Numbers added by author to indicate

Kauffmans rough time scales with trends in
taxonomic rank appearances/ stasis.

!
Overall the fossil record can be interpreted as following at least the first two stages of
Kauffmans theory, which predicts the taxonomic rank of metazoans in the MRE and the Cambrian
explosion. The theory accounts for the high level of taxonomic rank diversification unique to the

Precambrian/Cambrian radiation by reasonably assuming the low adaptive fitness of emerging

metazoans. In 1989, Kauffman positioned his theory as sufficient stand-alone alternative to
ecological opportunity and increasing robustness of developmental gene in explain the top-down
filling in pattern of diversity. I have already addressed how this theory may complement and inform
mechanisms invoking ecological opportunity. Recent work in evolutionary development suggests
the same genetic process underlies long-jumps and developmental robustness (Davidson and Erwin
2010).

A genetic mechanism
Canalization refers to the reduction in sensitivity of a phenotype to its underlying factors that
determine its expression, resulting in robustness of the phenotype despite mutation of those factors
(Loewe 2009). While Kauffman insists navigating the rugged adaptive terrain is sufficient to
explain taxonomic patterns in the Paleozoic, he also seems to imply the mutations responsible for
long-jumps also promote canalization. For example, Early stages would lock in because they adapt
on more rugged landscapes than late stages (Kauffman 1989).
A recent paper on gene regulatory networks suggests that this interpretation could be correct
for mutations affecting gene regulatory networks (GNR) (Davidson and Erwin 2010). They note
that gain-of-function mutations are overwhelmingly dominant and in GNRs would produce rapid
evolutionary change, even in large populations (Davidson and Erwin 2010). Furthermore, the
hierarchical design of gene regulatory networks conserves upstream feedback loops that force later
mutations downstream, such that these subsequent mutations have smaller effects on developmental
outcomes (Davidson and Erwin 2010). The diversity of these genes across animal lineages suggests

metazoans acquired these sophisticated patterning genes early in their history (Erwin 2009). At the
very least, this does not preclude mutations of GNRs as the genetic mechanism producing
morphological constraints and the hierarchical taxonomic patterns of the MRE, Cambrian
explosion, and beyond. The hierarchical gene regulatory networks certainly suggests an elegant
mechanism for the top-down appearance of hierarchical taxonomical rankings (Erwin 2009). More
work, however, is needed to determine the relative contribution of such genes to evolutionary trends
(Erwin 2009).

Conclusion and future directions

Fossil and molecular evidence, as well as adaptive landscape theories predict fast, high taxonomic
level changes happening earlier in animal evolution. This is a direct result of increasing
morphological constraint inherent in adaptation and at the genetic and developmental level. Fossil
evidence and evolutionary theory support the cladistic understanding of phyla as well as emphasize
the significance of pre-adaptation, morphological constraint, and co-options of gene function to the
metazoan trajectory. The intersection of morphology, community interactions and mutation is
another promising avenue of inquiry, and one with the potential to unite opposing views in
Cambrian literature.
A new field called Evolutionary Systems Biology (EvoSysBio) will investigate mechanisms
of evolution through modeling seven levels organismal biology of adaptive landscape from
genetics to ecological interactions (Loewe 2009). As demonstrated in the preceding discussion
inputs on taxonomic diversity depends on a number of inputs that span these levels. Given
Kauffmans elucidating 1989 model on the Precambrian/Cambrian radiation, I foresee sophisticated

adaptive landscape models resolving more finely the dynamics of evolution and diversity during
such events in deep time. The relative stasis of biodiversity in the Paleozoic despite environmental
upheaval comes to mind. Surprisingly, this review had a relatively short-sighted view of
evolutionary history. If I may a suggestion to the direction of this budding field, train these
theoretical models on unusual events in the fossil record, but when comparing across time consider
evolutionary history a salient character of the organisms.

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