“Was the first craniate on the road to cognition?”
Evolution and Cognition 2003; 9(2):142-156.

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Evolution and Cognition is an international, peer-reviewed science journal, printed by the University of Vienna.  It is the journal of the Konrad Lorenz Institute for Evolution and Cognition, named for, and located in the family mansion of, the Nobel laureate who discovered animal “imprinting” and laid the foundation for an evolutionary approach to animal behavior.
Fred Heeren:
Figure 1. One of 305 Haikouella lanceolata fossil specimens from Haikou, near Kunming, China (early Cambrian period, 530 mya).
Figure 2. Anatomical interpretation of Haikouella lanceolata (gen. et sp. nov.). Abbreviations: Abv (anterior branchial vessel); An (anus); Ap (anterior projection); At (atrio); Atp (atriopore); Ba (branchial arches); Baf (banchial-arch-filamentals); Br (brain); Buc (buccall cavity): Co (copulatory organ); Cp (caudal project); Da (dorsal aorta); Df (dorsal fin); Ds (denticular structure); Eg (endostyle glands); Es (endostyle); Esp (esophagus); Hd (head); Ht (heart); It (intestine); Lb (lobated structures); Le (lateral eye); Mg (midgut); Mm (myomeres); Mo (mouth opening); Ms (myosepta); Mw (median wall); Nc (neural cord); Nt (notochord); Ph (pharyngeal cavity); T (tentaclelike structure); Va (ventral aorta); Vf (ventral fin).
page 2 of this paper
Was the First Craniate on the Road to Cognition?
A Modern Craniate’s Perspective

Fredric J. Heeren

Abstract Chinese fossil discoveries of the earliest known craniates (from the early Cambrian period) have led scientists to question whether the evolution of human-level cognition is a rare occurrence in the universe. The earliest chordate is now best represented by a well-documented metazoan called Haikouella lanceolata. Possessing a relatively large brain, this animal appears to demonstrate that the brain and endoskeleton did not evolve together, as had been assumed, but rather that the brain appeared long before full endoskeletization. The paleontologist who describes the animal further notes a “top-down” pattern in the appearances of new forms in the fossil record. Researchers find such observations relevant to the question: Was the evolution of human-level cognition in some sense inevitable, or was it an accident dependent upon historical contingencies? The new evidence for early craniates lends support to the view that human- level cognition may be part of a developmental package, but historical contingencies pose serious problems for a strictly law-like explanation.   

Key words Contingency, convergence, developmentalism, directionality, internalism, saltation, top-down evolution.

One might propose three mutually exclusive hypotheses to explain the existence of human- level cognition 2 observed on Earth:
1. Human-level cognition occurs as a fluke in the universe; on Earth it may be explained as an incidental result of highly contingent events. 3
2. Human-level cognition is a common occurrence throughout the universe; its existence on Earth may be explained as a result of highly constrained or law-like processes.
3. Human-level cognition on Earth can be explained as neither fluke nor the result of law-like processes; 4 the frequency of its occurrence in the universe may not be predictable.

An investigator who knew that hypothesis 1 or 2 was correct would be able to comment knowledgeably upon the probability of human-level cognition existing on any planet where signs of life were observed. To estimate the probability of human-level cognition on such a planet, a scientist might only need to know the length of time that the planet had sustained conditions for life. Ideally, an investigator attempting to choose between the above hypotheses should observe life at several stages on many habitable planets before claiming confidence in his selection. Of course, the best an Earthbound scientist can do at present is to search for helpful clues on the one planet where we know that life exists; and here at least Earth’s crust does provide helpful access to pertinent glimpses of past life stages. Of greatest relevance for any such researcher is the fossil record’s snapshot in which the body plan 5 first appears that would eventually house human-level cognition.

To join such an investigation, we would like to explore the following questions: When does this body plan appear relative to other body plans? Does this body plan have an assured, or at least a likely, survival to permit time for the evolution of cognition—or is the survival of its future lineage dependent upon highly contingent events? Do other body plans appear that would also seem to make good candidates for the support of human-level cognition? How predictable is the appearance of a suitable, large brain-carrying body plan? For that matter, upon what basis can we predict body plans at all, or changes in any form of life? Does evolution proceed in a bottom-up fashion where small changes accrue into large ones aided by no higher law than natural selection, or are there top-down forces at work, driving organisms more forcefully toward obligatory forms?

Examining these questions takes us back to the early Cambrian period, to the time, 530 million years ago, when virtually all the major animal groups, called phyla, first appear in the fossil record. In December 1999, the journal Nature announced the discovery there of what appears to be the remains of our earliest chordate ancestor (CHEN /HUANG /LI 1999a). Found in southern China’s Yunnan Province near Kunming, the stiffspined, paper clip-size animal named Haikouella lanceolata pushes back the evolution of our own phylum, Chordata , to the very start of modern metazoan life. Until its discovery, paleontologists had begun to despair of ever finding undisputed evidence that our own “advanced” phylum existed as early as the main burst of the Cambrian “explosion” of new body plans. The plentiful fossil evidence for Haikouella— 305 specimens, many in excellent condition—finally confirms what many had suspected in recent years: Our own phylum arrived on the scene along with most of the others, during the surprisingly quick radiation of new major animal groups that characterizes the early Cambrian period.

The discovery demonstrates that our chordate ancestors had to fight their way through the rough and tumble Cambrian seas, in a period when many animal groups that entered did not survive to the end. Most families—and even many whole body plans—disappeared (GOULD 1989, pp47n; WARD 2000, p184). As we detail below, many paleontologists further classify Haikouella as a craniate. Any argument for the inevitability of craniate survival could be made more confidently if this body plan had arisen after the Cambrian, since the Cambrian represents the only period in which the number of animal phyla actually decreased (Dobzhansky et al. 19 77, pp. 422–423; SOLÉ /GOODWIN 2000, pp. 249– 251). Thus, as we will see, the appearance of the craniate body plan in the early Cambrian has paradoxical implications for a heady future; it can be taken either as evidence for a head start on the pathway to intelligence, or evidence of heightened probability that this lineage would be cut off—at its head. Haikouella simultaneously creates support for two competing inferences: the evolution of cognition as a highly constrained, or as a highly contingent, process.

Current Controversies
The animal’s discovery thus raises questions at the heart of current controversies in evolution research. One of the broadest ways to characterize the competing positions is as a disagreement between externalists and internalists, i.e., those who treat external selection as virtually the sole creative force in evolution versus those who emphasize the importance of internal constraints. Related issues tend to pit developmentalists against neo-DARWINISTS , formalists against functionalists, punctuationalists against gradualists, and top-down theorists against bottomup theorists, with the first party in each pair siding with the internalists. 6

Perhaps the most profound movement in the field in recent decades has been the advancement of developmental biology (which studies the way genes control the growth of individual living organisms) as a key to evolutionary biology. Since the mid-1990s, the marriage between the two disciplines has become known as evolutionary developmental biology, or simply “evo-devo”. Evo-devo explores how changes in ontogeny (the development of individual organisms, from fertilized egg to maturity) are related to the emergence of new phenotypes over successive generations. The goal is to use knowledge of how genes control the development of embryonic structures to learn how these same genes were involved in the first appearance of such structures in past epochs. Early contributors to the field include DE BEER (1930), SCHMALHAUSEN (1949), WADDINGTON (1957), RAFF /KAUFFMAN (1983), ARTHUR (1988), and HALL (1992). Developmentalists believe that too much credit has been given to the power of natural selection.

Wallace ARTHUR finds it “strange … that mainstream neo-DARWINIAN theory has come to regard natural selection as the primary mechanism causing evolutionary change. Selection is a destructive force, which acts only to eliminate” (ARTHUR 1997, p241). Though trained as a neo-DARWINist, ARTHUR acknowledges that selection “does not create the new type in the first place”, adding: “We have come to accept a theory of evolution that explains the origin and diversification of exquisitely engineered organisms on the basis of the selective destruction of genetic/developmental variants whose initial production has been treated, for the most part, as a ‘black box’” (Ibid). When it comes to the origin of body plans, according to ARTHUR , explaining it “purely in selective terms, without reference to the underlying genetic architecture will ultimately fail. Hence the need for the new discipline of evolutionary developmental biology” (p. 291).

Harvard zoologist Stephen Jay GOULD , who died in 2002, noted that DARWIN himself had not believed that natural selection was the exclusive means of evolutionary modification. Nevertheless, he said, certain “ultra-DARWINISTS ” were trying to “out-DARWIN DARWIN ” by claiming “that natural selection regulates everything of any importance in evolution” (GOULD 1997). For their part, neo-DARWINISTS accused G OULD of wandering too far from the reductionism 7 so necessary to science’s success. Daniel DENNETT even suggested that GOULD must have had a “hidden agenda” to sneak purpose back into biology (DENNETT 1996). The accusation was patently false; GOULD never wrote with any such intent; in fact, he went to great lengths to create new terms to replace any that smacked of teleology. “Preadaptations” became “exaptations” precisely to avoid the teleological overtones; “saltation” and “laws of form” became “facet-flipping” (GOULD 2002, pp342– 351), helping to assure that the element of chance overshadowed any Platonic connotations.

In his last monograph , GOULD wrote: “I argue that ‘internalism’ poses two separate challenges to pure DARWINIAN functionalism: saltational change arising from internal forces of mutability, and inherent directionality of variation… Most internalists … emphasize the second theme of channels and preferred directionality of variation” (2002, p445). One of the traits that made GOULD stand out from other internalists was his emphasis on chance. He seemed intent to exonerate himself from any charge of advocating teleology by assuring us that, though constraints have their important place, stochastic events have the final word. Our own existence is attributable to a “golden happenstance” in the Cambrian explosion (p. 1159), the start of an unlikely course that continued with the repeated overcoming of odds to produce humans as “an ultimate in oddball rarity” (1996–1997). If the developmental patterns of bilaterians appear to have become fixed into “limited and excellent, perhaps even optimal, designs”, it is only because they represent just one possible solution among numerous entirely plausible alternatives of strikingly different form, each yielding a subsequent history of life entirely different from the outcome actually experienced on earth” (2002, p1159). Yet all who support development’s importance to evolution (including GOULD , who used terms like “directionality” and “congealed designs”) must support the concept of directionality, however they explain it.

ARTHUR uses the term “directionality” to describe the observation of large-scale evolutionary changes preceding smaller modifications, “big ‘experiments” giving way to progressively more restricted modifications” (ARTHUR 1997, p207), i.e., the top-down concept that we will explore below. He writes: “This idea of directionality—which is absent from conventional neo-DARWINIAN theory —is important in Evolutionary Developmental Biology” (Ibid).

Against this background, we can now return to the findings about the earliest known craniate, to note the support they yield for this article’s first two hypothetical options: human-level cognition as either fluke or common occurrence. We can also compare the support they afford straightforward neo- DARWINISM versus developmentalism.

A listing of Haikouella -related supporting evidence for developmental constraints—and the ubiquity of human-level cognition in the universe —could read as follows:
1) early priority of cephalization over endoskeletization,
2) constraints/convergence/channeling, 8  
3) hierarchical phylogenies,  
4) saltation,  
5) top-down pattern in the fossil record, and  
6) the principle of mediocrity.

Supporting arguments for contingency—and the rarity of human-level cognition in the universe— would include:
1) The appearance of craniates in the early Cambrian (the one period where the number of phyla decreases) greatly increases the probability that this lineage would become extinct;
2) Non-chordate phyla can be shown to be incapable of developing human-level cognition; and
3) Human-level cognition has evolved only once on this planet.

As we recount the findings reported by Haikouella’s investigators, we will examine each of these in turn.

Settling the Matter of Chordates in the Cambrian
Before Jun-Yuan CHEN ’s discovery of Haikouella (CHEN /HUANG /LI 1999a; CHEN /HUANG /LI 1999b) (Figures 1 and 2), it was beginning to look doubtful that Cambrian chordates would ever become firmly established. Each new interpretation of the mostly poorly preserved would-be-chordate specimens was hotly disputed.

Biologists belonging to the contingency camp, as opposed to those expecting directionality, would have settled for an extremely primitive-looking chordate or half-chordate. Champions of chance expected the earliest chordate to exhibit brawn before brains; they sought the distinguishing chordate feature of muscles arranged in V-shaped blocks (called myotomes) without expecting to find much of a head at first. Even more essential for an earliest chordate candidate is the notochord, from which chordates get their name. The notochord is a stiffening, muscularized rod that runs down the middle of the back. The head was seldom mentioned except in reference to things to come, and never as an essential element for the earliest chordate. To illustrate what the earliest chordate should look like, biologists chose amphioxus, an animal that appears headless and pointy at both ends, as the most plausible living model. The name “amphioxus” literally means “both [ends] pointed”.