Decoding the Cambrian Radiation
On the Origin of Phyla. James W. Valentine. xxiv + 614 pp.
University of Chicago Press, 2004. $55.
The recent surge in interest in the origins of multicellular animals
(metazoans) is fueled by new evidence from three major sources:
molecular sequencing, the study of evolutionary development and the
discovery of exceptionally preserved fossils of Precambrian and
Cambrian age, particularly from China. Genetic sequences provide a
means of analyzing how the major animal groups are related and of
estimating their time of origin (using the molecular clock)—a
means that is independent of morphological data and the record of
evolutionary events the fossils reveal. The study of developmental
processes in an evolutionary framework ("evo-devo")
provides the link between genetics and morphology. These new
approaches have prompted molecular biologists to join forces with
paleontologists to focus on the sequence of events leading to the
origin of body plans before and during the Cambrian Period (543 to
500 million years ago).
Few if any authors can embrace these fields with the experience and
authority of James W. Valentine, professor emeritus of integrative
biology at the University of California, Berkeley, who has been
publishing novel and provocative ideas on the origin and nature of
phyla for more than 30 years. His most recent book, On the
Origin of Phyla, is an homage to the greatest biologist who
ever lived by one of the greatest living paleobiologists.
The concept of a phylum is not straightforward. A phylum has been
characterized as a group of species that share a unique body plan or
organization that reveals no evidence of relationship to other
phyla. This definition may be relatively easy to apply to living
animals but often proves problematic for extinct ones. Phyla
originated hundreds of millions of years ago, and extinction has
weeded out intermediate forms, leaving significant differences
between the living phyla. There is no difficulty, for example, in
distinguishing between an arthropod (say, a spider), an echinoderm
(a starfish, for example) and a chordate (such as your department
chairperson). Fossils, however, particularly those of the Paleozoic
Era (from 543 to 251 million years ago), may be more difficult to
deal with. Their morphology may be unfamiliar, and there is the
problem that information on the soft tissues has usually been lost
through decay and is not preserved.
On the Origin of Phyla is essentially about the Cambrian
radiation, the event that gave rise to most of the major animal
groups. The book's particular strength is its integration of data
from paleontology and biology.
Stephen Jay Gould's major treatment of the Cambrian radiation,
Wonderful Life (1989), was based mainly on the famous
fossils of the Burgess Shale. Gould considered many of the Burgess
Shale animals to represent extinct phyla or body plans, and he
argued that their large number was a measure of the impact of the
Cambrian explosion. Just 15 years later, Valentine's book
demonstrates that there has been a sea change in the focus on phyla,
from considering them as a measure of separation to exploring
relationships between them—something that is impossible to do,
almost by definition, on the basis of morphological data, but has
become a realistic goal in the age of molecular sequencing. Fossils,
however, remain central—if we want to understand the early
evolution of phyla, we need the evidence provided by fossils from
the Neoproterozoic Era (from 1 billion to 543 million years ago) and
the Cambrian Period.
A simple question exposes a problem in dealing with the origin of
phyla. The earliest members of a lineage have yet to acquire the
diagnostic features of the defining body plan. To which phylum do
they belong? Cladistics (a method of analyzing relationships among
taxa based on homologous characters) allows an emphasis to be placed
on the living members of a phylum: The "crown group" (the
last common ancestor of all living members of the phylum
and all the descendants of that ancestor) can be distinguished from
the "stem group" (the rest of the clade, a series of
extinct organisms lying "below" the crown group).
Molecular data are available to determine crown-group relationships,
but of course no such data will ever exist for the stem—which
is a pity, because, as Valentine points out, "stem taxa should
provide more evidence of the ancestral features of a phylum than do
the crown taxa." Stem taxa can be assigned to a phylum once
they evolve the diagnostic characters, and we can date the
appearance of phyla based on fossils.
On the Origin of Phyla is divided into three parts, the
first two of which provide a basis for the shorter third section.
Part One, "Evidence of the Origins of Metazoan Phyla,"
discusses the nature of a phylum and the history of the concept,
which originated as a strategy for classifying organisms. A
discussion of body plans explains how their development is
controlled by the genome, and this account leads naturally to a
description of methods, both morphological and molecular, for
determining connections between different phyla. Of course, the
relationships of fossil taxa can be analyzed only on the basis of
morphology. For living phyla, molecular data provide an independent
key to their relationships, and the morphological and molecular data
can be combined. The fossil record and the molecular clock also
provide evidence of timing, but they date different phenomena: The
molecular clock records the splitting of lineages, whereas fossils
date the appearance of body plans. Neither method is particularly
precise, but with more new discoveries the two have become better reconciled.
A chapter on the nature of the fossil record is important for
readers less familiar with the evidence of paleontology. Incomplete
information is a particular problem during the early stages of the
diversification of metazoan phyla. The most controversial evidence
is provided by the extraordinary organisms of the Ediacaran Period
(600 to 543 million years ago) of the late Neoproterozoic Era.
Valentine discusses them with the metazoan phyla, as
"prebilaterians" (organisms coming before those with
bilateral symmetry) and earliest crown bilaterians, whereas others
argue that at least some of them are not metazoans at all. Valentine
believes that the Ediacaran animals likely lie between the sponges
and crown diploblasts and suggests that the remarkable fractal
morphology displayed by some Ediacaran organisms might reflect
development controlled by Hox-type gene clusters.
But the preservation of the Ediacaran fauna with their intriguing
soft parts is the exception. Before grazing invertebrates were
widespread, microbial mats could colonize the sediment surface,
creating conditions that favored very early mineralization of the
adjacent sediment, preserving the morphology of soft tissues like a
death mask. These conditions disappeared with the Cambrian
radiation, so it is not surprising that a number of the small
soft-bodied phyla living now are unknown as fossils. As Valentine
notes, "there is nothing in the fossil record to disprove the
hypothesis that all phyla had appeared by the end of the Cambrian
or, for that matter, the end of the Early Cambrian."
Valentine styles Part Two, "The Metazoan Phyla," as
"the march through the phyla." He deals with the
prebilaterians, sponges, cnidaria and ctenophores and then with the
nature of the earliest crown bilaterians. The treatment is ordered
based on the molecular Tree of Life, dividing the protostomes into
Ecdysozoa and Lophotrochozoa, and completing the section with the
Deuterostomes. This is a comprehensive, up-to-date survey, reviewing
each phylum under four major headings: body plan, development,
fossil record and relationships to other phyla. Here, as elsewhere
in the book, the illustrations are collected from a huge variety of
original sources. The styles were selected to ensure some
compatibility, but the figures have not been redrawn. Although the
content of the book is distinctive, the design is not, but this
survey of phyla was not written primarily with undergraduates in mind!
Valentine's unique voice is particularly evident in Part Three,
"Evolution of the Phyla." Here he treats patterns of
diversity through the Phanerozoic (the 543-million-year span for
which evidence of life in the fossil record is abundant),
distinguishing between taxonomic diversity and the evolution of
morphology. He argues that bilaterian body plans originated and
radiated on the seabed rather than floating or swimming in water and
that we should seek the fossil evidence among bottom-dwelling forms.
The lack of a good record of soft-bodied animals in the
Neoproterozoic (Ediacaran examples notwithstanding), prior to the
widespread evolution of mineralized tissues ("hard parts"
to paleontologists), limits our ability to reconstruct both the
prelude to and the main events of the Cambrian explosion. Valentine
emphasizes that evolution proceeds from the top down, with body
plans appearing early, to be followed by diversification within
these themes. This, of course, is why the Neoproterozoic and
Cambrian record is so important.
On the Origin of Phyla concludes with a discussion of why a
resolution of metazoan relationships is so difficult. "For
nearly every facet of early metazoan history there is an array of
hypotheses that cannot be definitively falsified by the available
data," Valentine says. The solution then lies in more
research—more fossil discoveries, a better understanding of
the evolutionary development of the major groups, more molecular
sequences. But, as he points out, there are some gaps in the
database that can never be filled. The earliest members of the phyla
(stem representatives) became extinct long ago, and thus there is no
hope we'll ever have their genetic sequences to ponder. Yet
phosphatized embryos from the Neoproterozoic, like those from the
Doushantuo Formation of Guizhou, China, which are dated at about 570
million years ago, offer the possibility of a glimpse into
Precambrian embryology, one that could complement evidence on the
evolutionary development of living organisms.
In the absence of direct evidence of the sequence of changes that
gave rise to individual phyla, our best bet, as Valentine observes,
is to unravel those "first principles of genome evolution that
constrain the evolutionary routes between the developmental systems
that can actually be studied"—that is, those within
living taxa. The problem is one of a complexity of processes
compounded by gaps in the evidence: "in place of Darwin's
tangled bank, we find a Cambrian seafloor."
But progress has been astonishing, and much remains to be tackled. As
Valentine emphasizes, "at least in interpreting the past we are far
better off than in forecasting the future." On the Origin of Phyla
is a remarkable achievement, a timely synthesis of the current state of
this exciting field, which provides a marker against which future
progress will be measured.