Perceptive readers will find hints of worry in a journal’s one-sided presentation of the Cambrian explosion. Darwin’s Doubt? What doubt would that be? Current Biology‘s senior reviews editor, Florian Maderspacher, is too enraptured with “The Tree View of Life” to pay any attention to doubt. Waltzing through the grass, he ponders the distant relatives under his feet.

Whatever we see moving and growing around us is a member of our extended family. The mighty eagle and the ugly slug, the sequoia, the grass and the green slime on the beach — all are our relatives. And also what we don’t see — the microbes on our skin and in our guts, the bacteria that can kill us and the fungi that provide antibiotics — it’s all in the family. [Emphasis added.]

Though earlier biologists had noted the nested hierarchies in life, it was Charles Darwin who organized the leaves into a tree, he explains. Maderspacher ponders the power of that vision.

This is powerful stuff. Not only because it is so evocative of this “greatest show on Earth”, but also because there is a great deal of apparent truth in it. Trees not only reflect the hierarchies of traits naturalists used to classify the diversity of life. The bifurcations in the tree’s branches also echo the bifurcations that are a hallmark of life on all levels of biological organization. Populations split, sometimes leading to separate species, cells divide — so each multicellular organism is its own Bonsai tree of life — and most profoundly the bifurcations of the tree reflect the splitting of the DNA strand during replication. So, the tree is more than a metaphor, it mirrors real biological processes. No wonder then that to this day trees pervade biological thinking. This is probably most evident in the family tree of animals, which fascinates us not only because it’s our immediate arboreal neighbourhood, but also because it provides the framework within which we can now begin to try to understand the processes that gave rise to the staggering diversity of animal forms.

But what if it’s not true? What if the evidence shows abrupt appearance of complex life without a tree-like pattern of ancestry? Perhaps he should read two other papers in the special issue, The History of Life on Earth, more carefully. They’re updates on the problems of the Cambrian explosion.

Graham Budd

The first, Graham Budd of Uppsala University, is co-author with Maximilian Telford and Herv� Philippe in an article on “Phylogenetic Insights into Animal Evolution.” We met Graham Budd in Darwin’s Doubt denying that alleged trace fossils in the Precambrian represented animal remains (p. 85), and confirming Meyer’s denial that alleged Precambrian ancestors of bilaterians, like Vernanimalcula, represented animal ancestors (pp. 90-91). Does he have any news since these citations from 2008 and 2004?

While the Cambrian yields a continuous and diverse fossil record, the fossil record before is discontinuous (i.e. fossil finds rely on rare instances of exceptional preservation) and few taxa can be seen to cross into the Cambrian. The fossils from the Precambrian are generally problematic and no clear consensus exists about their status, even though some have been claimed to be animals or even bilaterians and members of crown-group phyla. These problems of interpreting the Precambrian record have led to wide variations in charts that attempt to plot animal phylogeny against the fossil record….

Some control exists though. For example, despite the general patchiness of the fossil record, some remarkable discoveries of microscopic fossils have been made in the Precambrian (e.g. Doushantou Formation from South China), yet none of these can be confidently assigned to bilaterians. In contrast, the emerging field of studies of microscopic organic fragments in the Cambrian reveals many such fragments that are clearly bilaterian in origin. Even if bilaterians were tiny in the Precambrian, they would be capable of being preserved in the microfossil record, suggesting that their absence is real.

Thank you for that update. Dr. Budd and his colleagues still believe in the tree view, in spite of the evidence, but they just admitted the Precambrian has no precursors of bilaterians. They should be there if they existed. “Their absence is real.” So what is more real, the tree view or the sudden emergence of most of the animal phyla?

Doug Erwin

In Darwin’s Doubt (2013) and Debating Darwin’s Doubt (2015), Douglas Erwin of the National Museum of Natural History is one of the most frequently cited Cambrian experts. The latter book cites Erwin as agreeing that the main burst of biological innovation was short, about 5 to 6 million years, not 20 or 50 million as some others have claimed. His book with James Valentine, The Cambrian Explosion (2013), is cited frequently in Debating Darwin’s Doubt. Casey Luskin reviewed it favorably in Chapter 44, noting that Erwin and Valentine admitted the brevity of the explosion and the current lack of evolutionary “uniformitarian” mechanisms to explain it.

Like all the other contributors to Current Biology‘s special issue, though, Erwin completely ignores Meyer. His entry, “Novelty and Innovation in the History of Life,” provides him a platform to answer Meyer’s critique — assuming he knows about it (and how could he not?). In particular, Erwin should be able in this article to answer Meyer’s primary challenge, the origin of biological information required to build new animal body plans, also the subject of our new short documentary, The Information Enigma.

Here, I begin with an overview of adaptive radiations and ecological opportunity, and provide examples of the variety of evolutionary diversifications identified from the fossil record. The limitations of the adaptive radiation model lead to the recognition of a broader array of patterns of evolutionary diversifications. Next, I turn to the historical contingency of the processes leading to some phenotypic novelties. Thus, one cannot simply assume that novel phenotypes will be available whenever ecological opportunity arises. Macroevolutionary lags and the contingent nature of novelty demand that we consider the processes generating phenotypic novelty separately from the ecological and evolutionary processes that regulate their success. Finally, I turn to the processes generating morphological novelties.

Remember, we’re looking for fossil evidence of gradually increasing complexity, or for a theory about how biological information can arise by unguided natural processes. It will not be satisfying to hear restatements of belief in the evolutionary tree view of life.

Has Erwin come across anything new since his 2013 book? Here are his mentions of the Cambrian:

• “Striking morphological novelties appeared during some of these evolutionary diversifications, from appendages and eyes in the Cambrian to feathers in the Cretaceous.”
• “In the case of the Ediacaran to Cambrian appearance and diversification of animals, many lineages were involved that had diverged tens of millions of years earlier. Morphological novelty was pervasive, but describing this as an adaptive radiation stretches the definition of the term beyond reason.”
• “Several challenges have arisen to claims that adaptive radiations are responsible for most evolutionary diversifications. For one, many events have been identified among both living and fossil clades that cannot be explained as the outcome of diversification from a single species. Examples range from the Cambrian explosion of animals, which involved many major clades but relatively few species, to the diversification of grasses.”
• “The sudden appearance of numerous bilaterian lineages in the fossil record at the base of the Cambrian is a paradigmatic example of a novelty event: the appearance of morphological novelties (individuation of new characters) and thus an increase in morphological disparity, but these novelties generally were unaccompanied by increases in taxonomic diversity or ecological abundance.”

These remarks show that he still believes the Cambrian explosion is real. Now, does he have a theory for the origin of information to build novel body plans as seen in the Cambrian animals?

Maybe we’ll find it in this subsection: “Phenotypic Novelty and Innovation.” He begins, “The focus on ecological opportunity as the driving factor in adaptive radiation led to a neglect of the mechanisms underlying the generation of novel phenotypes.” We search eagerly for the mechanism.

Surprisingly, Erwin turns to Lenski’s E. coli experiment with bacteria that adapted to digest citrate (Cit+). But wait — bacteria are not multicellular animals!

A scenario emerges for the four aspects of novelty and innovation: potentiation, novelty, adaptation and innovation (Box 2). This model is an extension and generalization of the Cit+ mutant example discussed previously. The distinction between novelty and innovations borrows from economics, where invention, the origin of a new technology, is distinguished from innovation, the spread or diffusion of such a technology so that it has an economic effect. A critical aspect of this scenario is that some environmental and ecological potentiating events may actually occur after the novelty emerges, thus creating the conditions for the macroevolutionary lags described earlier. The final stage of innovation following refinement distinguishes the ecological events associated with the success of novelties.

It’s hard to see how any evolutionist can take comfort from this proposal. What is the vera causa behind economics, invention, or technology? Clearly it is intelligence. That’s Meyer’s point. When we observe these features, we know the cause able to produce them. Erwin seems to assume that novelties arise by accident, and turn into innovations when they become economically successful. That begs the question.

Does Erwin explain it under the subsection “Evolutionary Novelty”? No; he begs the question again, merely assuming that novelties, like feathers, “arise” somehow. He adopts G.P. Wagner’s “restrictive view of novelty” that “the origin of a morphological novelty is the evolutionary process through which a novel character identity arises.” Let’s understand this: the evolution of novelty is the evolutionary process by which a novel character arises. Isn’t this what we’re trying to find out?

Maybe developmental gene regulatory networks (dGRNs) can explain it:

This restrictive definition of novelty links the appearance of novel characters to the structure of developmental gene regulatory networks. Specifically, it proposes that small networks of transcription factors within larger gene regulatory networks are responsible for these novel characters. Such recursively wired subnetworks of developmentally significant genes have been identified for characters ranging from feathers to heart formation. They have been described as character homology identity networks, or CHiNs and kernels (Figure 3). CHiNs were first identified in the formation of patterns associated with new cell types, while kernels are associated with regional patterning mechanisms in developing embryos. Each concept reflects the significance of structured, hierarchical developmental gene regulatory networks in underpinning novel morphological structures. During development, character identity involves these recursively wired regulatory subnets. Positional information determines where the characters form, while the downstream components of the network are responsible for localized cell differentiation. The focus on novel individuated structures is particularly helpful as these can, in principle, be recognized in the fossil record. Novel individuated structures also feature in major evolutionary transitions, critical events in the history of life including the origin of eukaryotes, multicellularity and social systems.

More question-begging. Where do the “new cell types” come from? Did they just “arise” too? Where did “structured, hierarchical… networks” come from? Where did “positional information” come from? And where is the evidence in the fossil evidence that “in principle” can be recognized? The very things we are looking for are the very things he fails to provide.

Meyer addressed the “developmental gene regulatory network” theory of novelty in detail in Debating Darwin’s Doubt, since it was the centerpiece of Charles Marshall’s critical review. Meyer showed how it assumes the very thing it needs to prove: that genetic information can arise by unguided processes. It’s hard to imagine Erwin being unaware of this interchange, but he writes as if he thought of this himself and nobody ever challenged it.

Maybe Erwin can explain the origin of biological information in the subsection, “Innovation and Morphological Disparity.” The disparity of animal body plans is a key feature of the Cambrian explosion. Here, sadly, he only makes his problem worse:

A recent analysis of disparity in 98 metazoan clades through the Phanerozoic found a preponderance of clades with maximal disparity early in their history. Thus, whether or not taxonomic diversification slows down most studies of disparity reveal a pattern in which the early evolution of a clade defines the morphological boundaries of a group which are then filled in by subsequent diversification. This pattern is inconsistent with that expected of a classic adaptive radiation in which diversity and disparity should be coupled, at least during the early phase of the radiation.

What this admits is that disparity is a worse problem than evolutionists had realized: it’s ubiquitous, not just in the Cambrian.

We see from his conclusion that he knows neo-Darwinism has a serious problem. If he had answers, he wouldn’t be calling on fellow evolutionists to get together and solve it.

Does evolutionary biology need a new research program in evolutionary novelty distinct from the existing work on adaptation and speciation? Some evolutionary biologists view morphological novelty as built upon the variation existing within a species. Others, particularly many evolutionary developmental biologists, view novelty as based on evolutionary changes distinct from standing variation. Considerable experimental work will be required to test the hypothesis that evolutionary novelties are underpinned by the origin of particular gene regulatory network structures. I suspect that novel individuated morphological structures will be identified that are not associated with such gene network structures, which will draw attention to the developmental mechanisms that ensure their evolutionary stability. Turning from novelty to innovation, there is great opportunity for carefully documenting the environmental and ecological circumstances under which innovations arise, how closely they are linked to morphological novelty, and whether there are particular conditions that foster increased innovation.

Erwin just danced around Meyer’s challenge by speculating that gene regulatory networks, or unspecified developmental mechanisms, or the environment can create the high levels of information necessary to build new animal body plans. If he had anything better than idle speculations or promissory notes since Meyer’s books came out, or if he had better fossils to muffle the explosion, this was a prime opportunity to share them.

The strength of a theory can be gauged by how well it stands up to attacks and how well it incorporates new evidence. If Current Biology‘s “History of Life on Earth” issue represents the best evolutionary thought on the Cambrian explosion to date, by the world’s most knowledgeable experts, with access to the best fossil evidence, Meyer’s thesis is doing pretty well. His critics would do well to stop ignoring the challenge and address its claims directly.