Ontogenetic Depth as a Complexity Metric for the Cambrian Explosion

An online chat with Paul Nelson hosted by ISCID on February 5, 2003

The original full transcript is located at http://www.iscid.org/paul-nelson-chat.php
The source paper with diagrams is located at http://www.iscid.org/nelsonchat.pdf

Live Moderated Chat with Paul Nelson

Transcript from February 5, 2003 9:00-10:15 PM Eastern

ISCID Moderator
Our guest speaker today is Paul Nelson. Dr. Nelson is a philosopher of biology, specializing in evo-devo and developmental biology. He is also a fellow of the International Society for Complexity, Information and Design. Dr. Nelson received his Ph.D. from the University of Chicago Department of Philosophy. His thesis critiques aspects of macroevolutionary theory in light of recent developments in embryology and developmental biology. Entitled "On Common Descent", it will be published as volume sixteen in the University of Chicago Department of Ecology and Evolution's "Evolutionary Monographs" series (and the first in this prestigious series to critique neo-Darwinism).

ISCID Moderator
Dr. Nelson has written several articles on the philosophical aspects of evolutionary biology including one recently published in Biology and Philosophy. He edits the journal Origins & Design.

ISCID Moderator
Everyone is encouraged to take a glance at the discussion paper that Dr. Nelson put together for the chat. It can be viewed at the following URL: http://www.iscid.org/nelsonchat.pdf

ISCID Moderator
I am now going to hand the talk over to Dr. Nelson. Participants can start sending in questions.

Paul Nelson
I apologize for not making the paper available sooner (I had hoped to have it up on the ISCID page by Feb 1, but family illnesses and other matters intervened).

Paul Nelson
Sadly, I've earned a well-deserved reputation for being probably the pokiest design theorist on the planet. :-(

Paul Nelson
Anyway -- I hope tonight's discussion sparks your thinking about how best to explain the origin of animals.

Paul Nelson
Here's the format I think would work well. I'll ramble on for a while, laying out some ideas, and then will type BIG SIGH or something like that.

Paul Nelson
BIG SIGH is your clue that I've gone on long enough (doubtless more than long enough), and it's time to ask questions.

Paul Nelson
Truth in advertising note:

Paul Nelson
This ISCID informal discussion material represents work in progress that I am undertaking in collaboration with Marcus Ross, a paleontology graduate student in the Department of Geosciences, University of Rhode Island (317 Woodward Hall, 9 East Alumni Avenue, Kingston, RI, 02881-2019; E-mail: mros1106@postoffice.uri.edu).

Paul Nelson
Marcus, who is the paleontological half of the project, presented the first part of our joint work as a poster, "Ontogenetic Depth as a Complexity Metric for the Cambrian Explosion," Paper No. 187-34, at the 2002 Annual Meeting of the Geological Society of America (30 October 2002).

Paul Nelson
We will be submitting a follow-up paper on the concept of ontogenetic depth to the 62nd (2003) Annual Meeting of the Society of Developmental Biology, to be held July 30 to August 3 in Boston, MA (where, incidentally, the poster Jonathan Wells and I had planned to present at the 2002 SDB meeting in Madison will also be available as a paper for anyone who is interested).

Paul Nelson
Practical consequence of truth-in-advertising note: I may well have to punt on paleontology questions. Sorry!

Paul Nelson
Marcus and I plan to have a comprehensive paper ready to submit to SDB by the end of March. Maybe we can put a pre-print up at ISCID.

Paul Nelson
Before I get to the main course (love those food metaphors), let me give you a couple of philosophical/sociological appetizers.

Paul Nelson
The longer I work as a senior fellow at the Discovery Institute -- writing, lecturing, going to meetings (both design and regular science) -- the more I value evolutionary biologists.

Paul Nelson
"Opposition is true friendship," wrote William Blake (1757-1827). Blake loved a good paradox, and this one fits the bill.

Paul Nelson
If competition ("opposition") is good for selling computers or the political process, it's also good for science and scientific discovery.

Paul Nelson
What's the fastest way to find out what's wrong with your ideas? Run them by someone who thinks you are dead wrong.

Paul Nelson
And he or she will tell you! If they're right, you can abandon that idea. (Hurts, of course.)

Paul Nelson
If they throw their best criticisms at your ideas, however, and the ideas stumble through, still alive, you may be onto something.

Paul Nelson
I'm hoping that people (tonight) can suggest aspects of the problem of the origin of animals that I've overlooked or missed.

Paul Nelson
But there is another respect in which I value evolutionary (and evo-devo) biologists. For their own candor.

Paul Nelson
Here's an example, where I cannot name the scientist in question (yet, anyway). This is directly relevant to tonight's discussion.

Paul Nelson
This happened at the now-notorious 1999 China meeting on the origin of animal body plans.

Paul Nelson
(The meeting has become notorious because design theorists were involved in its planning, and presented papers, much to the dismay of the American and British scientists present.)

Paul Nelson
(The European and Chinese scientists didn't really seem to care -- but that's another story.)

Paul Nelson
One day, I was sitting outside the dining hall, waiting for lunch to be served.

Paul Nelson
I had with me (on top of my conference files) an overhead transparency, showing the complex regulatory sequence of an invertebrate developmental gene.

Paul Nelson
And up walked the author of that very paper (a visiting American biologist), from which I had borrowed the figure.

Paul Nelson
Of course he spotted the diagram right away. "What do you plan to do with that?" he asked me.

Paul Nelson
"I thought I might use this in my talk," I said, "as a quick illustration of the complexity of embryonic regulation."

Paul Nelson
The biologist smiled. Knowing that he was something of a critic of neo-Darwinism, I asked him what historical process he thought had assembled the complex regulatory sequence.

Paul Nelson
His answer really surprised me. "I don't know," he said, "but I do know that ordinary mutation and selection won't do it."

Paul Nelson
He went on to say that he thought our (that is, the biological community's) understanding of evolution lagged way behind its other knowledge.

Paul Nelson
And that brings me to ontogenetic depth.

Paul Nelson
Let me describe our motivating puzzle. ("Our" refers to Marcus Ross and me.)

Paul Nelson
No scientist sets out (consciously, anyway) to become the butt of jokes in the future. Thus, when we now read Ernst Haeckel's statement that a cell is a "simple little lump of albuminous combination of carbon," we smile to ourselves - perhaps saving the passage for a humorous Powerpoint interlude - but we may also add, "Well, actually, in the late 19th century - could Haeckel or anyone else have foreseen just how complicated the cell would turn out to be?" The guy got it wrong.

Paul Nelson
The deeper point, of course, is that one cannot explain the origin of something when one does not understand what that thing really is. Haeckel failed to explain the origin of cells because he profoundly misunderstood, or mischaracterized, his explanatory target.

Paul Nelson
As the historian and philosopher of science Harmke Kamminga (1986) has observed, "At the heart of the origin-of-life problem lies a fundamental question: What is it that we are trying to explain the origin of?" In 2003, we know that the ultimate target of abiogenesis research - the object whose origin we are trying to explain - is not an "albuminous combination of carbon."

Paul Nelson
Therefore any historical explanation that aims to generate "simple lumps," instead of a real cell, will miss the mark by a long distance.

Paul Nelson
The same problem of accurately characterizing the explanatory target arises later in the history of life, with the origin of the bilaterian animals. The origin of the animals has remained a puzzle in historical biology from Darwin's time to the present.

Paul Nelson
As with any scientific problem, understanding what needs to be explained stands as the first task. The motivating question can be framed as follows: What sort of biological event does the geological first appearance of forms such as arthropods (e.g., Anomalocaris) or molluscs (e.g., Scenella) represent?

Paul Nelson
As with any scientific problem, understanding what needs to be explained stands as the first task. The motivating question can be framed as follows: What sort of biological event does the geological first appearance of forms such as arthropods (e.g., Anomalocaris) or molluscs (e.g., Scenella) represent?

Paul Nelson
Various measures have been proposed to quantify complexity increases in evolution, notable among them genome size (Britten and Davidson 1969), gene number, and cell type (Valentine 1994).

Paul Nelson
But genome size is vulnerable to the so-called "C-value paradox," i.e., the lack of correlation between genome size (measured as DNA content) and apparent morphological complexity.

Paul Nelson
Gene number estimates can vary widely (see, e.g., Ewing and Green 2000 versus Liang et al. 2000, whose estimates for gene number in humans differ by a factor of 4), and cell type counts may be skewed by the use of intensively studied model taxa, possibly leading to higher counts (McShea 1996, 483).

Paul Nelson
These difficulties suggest that a more comprehensive measure, relating more of the data of interest - body plans, organ systems, cell and tissue types, etc. - may be needed.

Paul Nelson
Valentine (1994, 406) notes that "the ultimate measure of body-plan complexity would presumably be one that reflects the information required to specify the entire body, involving both gene number and the organization of gene expression."

Paul Nelson
We suggest that a measure of *ontogenetic depth* may bring together many (if not most) of the key biological parameters, and help investigators focus on what really needs to be explained in such events as the Cambrian Explosion.

Paul Nelson
So here is our proposal.

Paul Nelson
Consider Figure 1 [which should be available sometime this week from ISCID] which shows several of the salient biological levels employed in assessing the complexity increases exhibited by the Cambrian Explosion.

Paul Nelson
Gene number is the sum of all functional sequences in a taxon's genome (whether those loci are classical protein-coding genes or regulatory sequences).

Paul Nelson
Cell number is the total count of discrete cells, of any type, possessed by an adult organism capable of reproduction.

ISCID Moderator
Figure 1 is available now: http://www.iscid.org/nelsonchat.pdf

Paul Nelson
Cell type describes the total number of histologically differentiated cellular morphologies (e.g., gut epithelium, nerve, muscle, blood cell).

Paul Nelson
You're amazing, Mod!

Paul Nelson
Tissue type describes the organization of cell types into functional units such as sheets or epithelia, connective materials, skeletal parts, and so on.

Paul Nelson
Organ systems are the higher-level anatomical relationships responsible for major organismal functions (e.g., sensory, locomotory, digestive, reproductive).

Paul Nelson
Body plans represent the major architectural features characteristic of groups such as Arthropoda, Mollusca, Brachiopoda, and the other bilaterian phyla.

Paul Nelson
Now, it might seem that the natural way to illuminate the relationship between these levels would begin "bottom up," with the genes.

Paul Nelson
We argue, however, that for the problem of the origin of the phyla, the concept of an ontogenetic network best integrates these levels (see Figure 2).

Paul Nelson
An example of one aspect of an ontogenetic network can be seen in Figure 3, depicting the beginning of the cell lineage of the nematode Caenorhabditis elegans.

Paul Nelson
Ontogenetic networks in all animals commence with a single cell, the fertilized egg. Then an unfolding arborescence of developmental decisions begins, whose complexity and overall architecture varies by taxon.

Paul Nelson
In all animals, however, a point in the adult phenotype arrives when reproduction - the generation of gametes capable of fertilization - is possible.

Paul Nelson
This distance, from the egg to the adult capable of reproduction, is what we term ontogenetic depth (see Figure 4).

Paul Nelson
Somewhat more formally, ontogenetic depth may be defined as the distance, in terms of cell division and differentiation, between a unicellular condition and a macroscopic adult metazoan able to reproduce itself (i.e., generate gametes).

Paul Nelson
The ontogenetic depth of a handful of extant animals (from the model systems of developmental biology) is known with precision.

Paul Nelson
In the nematode Caenorhabditis elegans, for instance, a relatively small animal only 1.5 mm in length, 7 to 9 rounds of cell division lie between the fertilized egg and any cell in the adult: 959 somatic cells in the hermaphrodite (with a variable number of germ cells), and 1031 cells in the male (with its distinctive tale).

Paul Nelson
For larger metazoans, of course, such as the dipteran Drosophila melanogaster, ontogenetic depth is much greater, as total cell number, degree of cellular differentiation, and time to reproductive capability increase accordingly.

Paul Nelson
The value of ontogenetic depth as a complexity metric lies in its relationship to all the parameters listed in Figures 1 and 2.

Paul Nelson
Of course, the ontogenetic depth of any extinct organism cannot be determined with complete exactitude.

Paul Nelson
However, it should be possible, using modern analogues for fossil taxa - e.g., the extant monoplacophoran Neopilina for the extinct mollusc Scenella - to obtain good estimates on the ontogenetic depth requirements of many Cambrian forms.

Paul Nelson
This is research we are now conducting. It is likely that reasonable estimates of the ontogenetic networks, and depth, required to specify such extinct organisms as Anomalocaris or Opabinia, will require no less complexity than that of modern animals.

Paul Nelson
All right, you say. So what? What's the significance of this idea?

Paul Nelson
That's where we come to what I've been calling "the marching band problem." I first used this term at the China meeting (Nelson 1999).

Paul Nelson
I realize "marching band problem" may seem tangential (at best) to the discussion, but bear with me.

Paul Nelson
To a skeptic, the concept of ontogenetic depth may look to be little more than a roundabout way of expressing the already-familiar problem of how animals originally evolved from unicellular or colonial ancestors.

Paul Nelson
We think, however, that focusing on ontogenetic depth helps to illuminate the central challenge that standard (neo-Darwinian) evolutionary theory faces when confronted with phenomena such as the geological first appearance of forms like Anomalocaris.

Paul Nelson
As noted earlier, the cells of an adult metazoan are specialized for particular functional roles (as gametes, nerves, gut epithelia, skin, skeleton or exoskeleton, sensory organs, and so on).

ISCID Moderator
Figures for the marching band problem can be found here: http://www.iscid.org/nelsonchat.pdf

Paul Nelson
"The production of [these] differentiated cell types," writes Carl Schlichting (2003), "is a hallmark of multicellular organisms." The production process itself is an ontogenetic network, commencing with the fertilized egg.

Paul Nelson
"A function [one might say *the* function] of developmental processes," notes Strathmann (2000), "is putting the right kind of cells in the right places at the right times. The criterion for 'right" is survival and reproduction."

Paul Nelson
Or what we're calling "reproductive capability." Quick (but very important) note: differences in reproductive output are the only conditions on which natural selection can act (see John Endler's 1986 monograph, Natural Selection in the Wild).

Paul Nelson
One can conceive this process of differentiation (or cellular specialization) very much on the model of an American university marching band (see Figure 5, where a 105 member marching band is depicted as orange dots, arrayed at the sideline of a football field).

Paul Nelson
Mea culpa: the discussion paper says the band has 140 members. Obviously I can't do 3rd grade multiplication! :-(

Paul Nelson
In one sense, of course, any marching band is strongly disanalogous to a developing animal.

Paul Nelson
A nematode or fruit fly commences its existence as a single cell (the fertilized egg), and will then construct its cell populations during development, whereas the marching band begins its maneuvers with all of its members already present.

Paul Nelson
But in another sense - the one that we'll focus on - the two processes share many parallels.

Paul Nelson
The band will move, through a series of intermediate maneuvers, toward its functional endpoint - say, spelling "CAL STATE" on the field (see Figure 6).

Paul Nelson
In its development, an animal also moves from the fertilized egg, through a series of intermediate "maneuvers," towards its functional endpoint, namely, an organism capable of reproduction.

Paul Nelson
The latter process, of course, is vastly more complex:

Paul Nelson
" This temporally ordered sequence of morphological heterogeneities that we call development," writes Arthur (1997), "generates adult tissue patterns that, in some taxa, can be highly complex, involving very precise and repeatable arrangements of billions, even trillions, of cells."

Paul Nelson
Now, if the band is going to spell "CAL STATE" successfully, it should be intuitively obvious that the members must have their instructions in place before they venture onto the field.

Paul Nelson
The trumpet player, for instance, standing in the front row on the sideline, who will eventually become the tip of the serif at the bottom of the letter "L" (see Figure 7), must know how to execute the series of turns and motions that will carry him to his endpoint on the field.

Paul Nelson
The same is the case with a developing organism. "Development is possible," writes Arthur (2000), "only if cells 'know' what to do in all these respects," i.e., assign their planes of division, tendencies to move, directions and rates of movement, modes of differentiation into particular cell types, and cell death (apoptosis).

Paul Nelson
" So the key question," Arthur continues, "becomes 'how do they know?', and the whole of developmental biology could be regarded as an attempt to answer this question."

Paul Nelson
If the question "How do cells know?" is to be answered by developmental biology, its sister (and far more difficult) question "How did cells learn what they know?" must be addressed by evolutionary (or historical) biology.

Paul Nelson
And here serious, and currently unanswered, questions arise.

Paul Nelson
" How cell types of multicellular organisms came to be differentiated," notes Schlichting (2003), "is still an open issue...the origins of differentiation remain unclear."

Paul Nelson
Given that the origin of animals - organisms defined by differentiated structures - is thought by most scientists to have been a problem solved, at least in outline, by Charles Darwin, this is not a minor difficulty.

Paul Nelson
Some authors have recently noted this explicitly, e.g., Davidson 2001. He writes:

Paul Nelson
"...classical Darwinian evolution could not have provided an explanation, in a mechanistically relevant way, of how the diverse forms of animal life actually arose during evolution, because it matured before molecular biology provided explanations of the developmental process."

Paul Nelson
"To be very brief, the evolutionary theory that grew up before the advent of regulatory molecular biology dealt with the problem of the origin of novel organismal structures in two ways."

Paul Nelson
"The first has been to treat the mechanisms generating novel morphological structures as a black box. New forms were considered to arise 'because' the environment changed."

Paul Nelson
"But while changes in Precambrian or Ordovician weather, continental shifts, or temperature may have contributed crucial selective forces, they do not generate heads or appendicular forms; only genes do that."

Paul Nelson
[Side comment from Paul: Or, we might say, genes *plus* (the three-dimensional localization of their protein products, et cetera - nucleic acid alone an organism never made).]

Paul Nelson
Davidson goes on to argue that "stepwise, adaptive changes in protein sequence...is probably largely irrelevant to the evolution of any salient features of animal morphology," but we will focus on a more general difficulty, involving the process of natural selection itself, and its (probable) impotence for constructing ontogenetic networks.

Paul Nelson
Suppose we interrupt a marching band midway through its maneuvers, at some stage before "CAL STATE" appears on the field.

Paul Nelson
Suppose, furthermore, that we cause this interruption at a marching band competition where "success" is defined (at least in part) by actually reaching the endpoint where the name of the band's home institution is spelled.

Paul Nelson
It should again be intuitively obvious that the functional reason for the band's intermediate maneuvers is not the maneuvers themselves, but rather the distant endpoint that those maneuvers enable or bring about.

Paul Nelson
Now look again at Figure 3, showing the early cell lineage of C. elegans. One cannot interrupt this canonical cell division pattern and obtain a viable organism.

Paul Nelson
Viability, and, in particular, reproductive capability - the only outcome "visible" to natural selection - lie in the distance, after several rounds of cell division and differentiation.

Paul Nelson
How then did natural selection construct the ontogenetic network of C. elegans?

Paul Nelson
Figure 8 represents this problem in schematic form, using a very shallow network to make the point.

Paul Nelson
Reproductive capability arises only in the square on the right, when its five cells are in place.

Paul Nelson
But the cells must be put there by a specific developmental process. What constructed that process?

Paul Nelson
OK. BIG SIGH.

Paul Nelson
Oops -- before the Q & A, here are the references:

Paul Nelson
Arthur, Wallace. 1997. The Origin of Animal Body Plans: A Study in Evolutionary Developmental Biology. Cambridge: Cambridge University Press.

Paul Nelson
Britten, Roy and Eric Davidson. 1969. Gene Regulation for Higher Cells: A Theory. Science 165:349-357.

Paul Nelson
Davidson, Eric. 2001. Genomic Regulatory Systems: Development and Evolution. New York: Academic Press.

Paul Nelson
Ewing, Brent and Phil Green. 2000. Analysis of expressed sequence tags indicates 35,000 human genes. Nature Genetics 25:232-234.

Paul Nelson
Kamminga, Harmke. Protoplasm and the Gene. In A.G. Cairns-Smith and H. Hartman, eds., Clay Minerals and the Origin of Life. Cambridge: Cambridge University Press, pp. 1-10.

Paul Nelson
Liang, Feng et al. 2000. Gene Index analysis of the human genome estimates approximately 120,000 genes. Nature Genetics 25:239-240.

Paul Nelson
McShea, Daniel. 1996. Metazoan Complexity and Evolution: Is There a Trend? Evolution 50:477-492.

Paul Nelson
Nelson, Paul. 1999. Generative Entrenchment and Body Plans. Lecture presented at the International Symposium on the Origins of Animal Body Plans and Their Fossil Records, eds. J.Y. Chen, P.K. Chien, D.J. Bottjer, G.X. Li, and F. Gao, Early Life Research Center, Kunming, People's Republic of China, 21-25 June.

Paul Nelson
Schlichting, Carl D. 2003. Origins of differentiation via phenotypic plasticity. Evolution and Development 5:98-105.

Paul Nelson
Schnabel, Ralf. 1997. Why does a nematode have an invariant cell lineage? Seminars in Cell & Developmental Biology 8:341-349.

Paul Nelson
Strathmann, Richard. 2000. Functional design in the evolution of embryos and larvae. Seminars in Cell and Developmental Biology 11:395-402.

Paul Nelson
Valentine, James W. 1994. The Cambrian Explosion. In S. Bengston, ed., Early Life on Earth (New York: Columbia University Press), Nobel Symposium No. 84; pp. 401-411.

The full chat transcript including Q&A is located at http://www.iscid.org/paul-nelson-chat.php