The Panda's Thumb: More Reflections in Natural History

by Stephen Jay Gould

  Ideally, we might hold out for a simple, empirical resolution of the issue. Might we not hope to find a sequence of fossils so perfectly intermediate between a protist (single-celled ancestor) and a metazoan (multicelled descendant) that all doubt would be erased? We may effectively write off such a hope: the transition occurred in unfossilizable, soft-bodied creatures long before the inception of an adequate fossil record during the Cambrian explosion, some 600 million years ago. The first metazoan fossils do not surpass the most primitive modern metazoans in their similarity to protists. We must turn to living organisms, hoping that some still preserve appropriate marks of ancestry.

  There is no mystery to the method of genealogical reconstruction. It is based on the analysis of similarities between postulated relatives. “Similarity,” unfortunately, is no simple concept. It arises for two fundamentally different reasons. The construction of evolutionary trees requires that the two be rigorously separated, for one indicates genealogy while the other simply misleads us. Two organisms may maintain the same feature because both inherited it from a common ancestor. These are homologous similarities, and they indicate “propinquity of descent,” to use Darwin’s words. Forelimbs of people, porpoises, bats and horses provide the classic example of homology in most textbooks. They look different, and do different things, but are built of the same bones. No engineer, starting from scratch each time, would have built such disparate structures from the same parts. Therefore, the parts existed before the particular set of structures now housing them: they were, in short, inherited from a common ancestor.

  Two organisms may also share a feature in common as a result of separate but similar evolutionary change in independent lineages. These are analogous similarities; they are the bugbear of genealogists because they confound our naive expectation that things looking alike should be closely related. The wings of birds, bats and butterflies adorn most texts as a standard example of analogy. No common ancestor of any pair had wings.

  Our difficulties in identifying the trunks and limbs of life’s tree do not record muddled thinking about methods. All major naturalists, from Haeckel on (and even before) stated their procedure correctly: separate homologous from analogous similarity, discard analogies, and build genealogy from homology alone. Haeckel’s law was a procedure, unfortunately incorrect, for the recognition of homology. The goal is, and has been, clear enough.

  In a broad sense, we know how to identify homology. Analogy has its limits. It may build striking external, functional similarity in two unrelated lineages, but it does not modify thousands of complex and independent parts in the same way. At a certain level of precision, similarities must be homologous. Unfortunately, we rarely have enough information to be confident that this required level has been attained. When we compare primitive metazoans with different protists as potential relatives, we often work with only a few features held in common for any contrast—too few to be sure about homology. Moreover, small genetic changes often have profound effects upon external, adult form. Therefore, a similarity that looks too uncanny and complex to arise more than once may actually record a simple and repeatable change. Most importantly, we aren’t even comparing the right organisms, but only pale reflections of them. The transition from protist to metazoan occurred more than 600 million years ago. All true ancestors and original descendants disappeared eons ago. We can only hope that their essential, identifying features have been retained in some modern forms. Yet, if retained, they have surely been modified and overlain with a plethora of specialized adaptations. How can we separate original structure from later modification from new adaptation? No one has ever found an unfailing guide.

  Only two scenarios have been favored for the origin of metazoans from protists: in the first (amalgamation) a group of protistan cells came together, began to live as a colony, evolved a division of labor and function among cells and regions, and finally formed an integrated structure; in the second (division), cellular partitions formed within a single protistan cell. (A third potential scenario, repeated failure of daughter cells to separate following cell division, has few takers these days.)

  At the very outset of our inquiry, we come up against the problem of homology. What about multicellularity itself? Did it arise only once? Have we explained its occurrence in all animals once we decide how it arose in the most primitive? Or did it evolve several times? In other words, is the multicellularity of various animal lineages homologous or analogous?

  The metazoan group usually regarded as most primitive, the sponges, clearly arose by the first scenario of amalgamation. In fact, modern sponges are little more than loosely knit federations of flagellated protists. In some species, cells can even be disaggregated by passing the sponge through a fine silk cloth. The cells then move independently, reaggregate into small clumps, differentiate and regenerate an entire new sponge in its original form. If all animals arose from sponges, then multicellularity is homologous throughout our kingdom, and it arose by amalgamation.

  But most biologists regard sponges as an evolutionary dead end without subsequent descendants. Multicellularity is, after all, a prime candidate for frequent, independent evolution. It displays the two primary features of analogous similarity: it is reasonably simple to accomplish, and it is both highly adaptive and the only potential path to the benefits it confers. Single cells, ostrich eggs notwithstanding, cannot become very large. The earth’s physical environment contains scores of habitats available only to creatures beyond the size limit of a single cell. (Consider only the stability that arises from being large enough to enter a realm where gravity overshadows the forces that act upon surfaces. Since the surface/volume ratio declines with growth, increasing size is the surest path to this realm.)

  Not only has multicellularity evolved separately in the three great higher kingdoms of life (plants, animals, and fungi), but it probably arose several times in each kingdom. Most biologists agree that all origins within plants and fungi occurred by amalgamation—these organisms are the descendants of protistan colonies. Sponges also arose by amalgamation. May we then close the issue and state that multicellularity, although analogous both across and within kingdoms, evolved in the same basic way each time? Modern protists include colonial forms that display both regular arrangement of cells and incipient differentiation. Remem ber the Volvox colonies of high school biology labs? (Actually, I must confess that I don’t. I attended a public high school in New York just before Sputnik went up. We had no lab at all, though it arrived in a flash just as I left.) Some volvoxes form colonies with a definite number of cells arranged in a regular manner. The cells may differ in size, and reproductive function may be confined to those at one end. Is it such a big step to a sponge?

  Only among animals may we make a good case for another scenario. Did some animals, ourselves included, arise by division? This question cannot be answered until we resolve one of the oldest riddles in zoology: the status of the phylum Cnidaria (corals and their allies, but also including the beautiful, translucent Ctenophora, or comb-jellies). Almost everyone agrees that the Cnidaria arose by amalgamation. The dilemma resides in their relationship with other animal phyla. Almost all possible schemes have their supporters: cnidarians as descendants of sponges and ancestors of nothing else; cnidarians as a separate branch of the animal kingdom without descendants; cnidarians as the ancestors of all “higher” animal phyla (the classical view of the nineteenth century); cnidarians as degenerate descendants of a higher phylum. If either of the last two schemes can ever be established, then our issue is settled—all animals arose by amalgamation, probably twice (sponges and everything else). But if the “higher” animal phyla are not closely related to cnidarians, if they represent a third, separate evolution of multicellularity in the animal kingdom, then the scenario of division must be seriously considered.

  Supporters of a separate origin for the higher animals generally cite the Platyhelminthes (flatworms) as a potentially ancestral stock. Earl Hanson, a biologist at Wesleyan
University, has been a leading crusader, both for a platyhelminth origin of higher animals and for the scenario of division. If his iconoclastic view prevails, then the higher animals, including humans of course, are probably the only multicellular products of division rather than amalgamation.

  Hanson has pursued his case by studying the similarities between a group of protists known as ciliates (including the familiar Paramecium), and the “simplest” of flatworms, the Acoela (named for their failure to develop a body cavity). Many ciliates maintain large numbers of nuclei within their single cell. If cellular partitions arose between the nuclei, would the resulting creature be enough like an acoelous flatworm to justify a claim for homology?

  Hanson documents an extensive set of similarities between the multinucleate ciliates and the acoeles. Acoeles are tiny marine flatworms. Some can swim, and a few live in water up to 250 meters in depth; but most crawl along the sea bottom in shallow water, living under rocks or in sand and mud. They are similar in size to the multinucleate ciliates. (It is not true that all metazoans are larger than all protists. The ciliates range in length from 1/100 to 3 millimeters, while some acoeles are less than 1 millimeter in length.) The internal similarities of ciliates and acoeles reside primarily in their shared simplicity; for acoeles, unlike conventional metazoans, lack both a body cavity and the organs associated with it. They have no permanent digestive, excretory, or respiratory system. Like the ciliate protists, they form temporary food vacuoles and perform digestion within them. Both ciliates and acoeles divide their bodies roughly into inner and outer layers. Ciliates maintain an ectoplasm (outer layer) and endoplasm (inner layer), and concentrate their nuclei in the endoplasm. Acoeles devote an inner region to digestion and reproduction, and an outer region to locomotion, protection, and capture of food.

  The two groups also display some outstanding differences. Acoeles build a nerve net and reproductive organs that can become quite complex. Some have penises, for example, and impregnate each other hypodermically by penetrating through the body wall. They undergo embryonic development after fertilization. Ciliates, by contrast, have no organized nervous system. They divide by fission and have no embryology, although they do indulge in sex via a process called conjugation. (In conjugation, two ciliates come together and exchange genetic material. They then separate and each divides later to form two daughters. Sex and reproduction, combined in nearly all metazoa, are separate processes in ciliates.) Most prominently, of course, acoeles are cellularized, ciliates are not.

  These differences should not debar a hypothesis of close genealogical relationship. After all, as I argued previously, contemporary ciliates and acoeles are more than half a billion years beyond their potential common ancestor. Neither represents a transitional form in the origin of multicellularity. The debate centers instead on the similarities, and on the oldest and most basic issue of all: are the similarities homologous or analogous?

  Hanson argues for homology, claiming that acoele simplicity is an ancestral condition within the platyhelminths—and that similarities between ciliates and acoeles, largely a result of this simplicity, do record genealogical connection. His detractors reply that the simplicity of acoeles is a secondary result of their “regressive” evolution from more complex platyhelminths, a consequence of pronounced reduction in body size within acoeles. Larger turbellarians (the platyhelminth group including acoeles) have intestines and excretory organs. If acoele simplicity is a derived condition within the turbellarians, then it cannot reflect direct inheritance from a ciliate stock.

  Unfortunately, the similarities that Hanson cites are of the sort that always produce unresolvable wrangling about homology vs. analogy. They are neither precise, nor numerous enough to guarantee homology. Many are based upon the absence of complexity in acoeles, and evolutionary loss is easy and repeatable, whereas separate development of precise and intricate structures may be unlikely. Moreover, acoele simplicity is a predictable result of their small body size—it may represent a functional convergence upon ciliate design by a group that secondarily entered their range of body size, not a connection by descent. Again, we invoke the principle of surfaces and volumes. Many physiological functions, including breathing, digestion, and excretion, must proceed through surfaces and serve the entire body’s volume. Large animals have such a low ratio of external surface to internal volume that they must evolve internal organs to provide more surface. (Functionally, lungs are little more than bags of surface for exchange of gases, while intestines are sheets of surface for the passage of digested food.) But small animals maintain such a high ratio of external surface to internal volume that they often can breathe, feed, and excrete through the external surface alone. The smallest representatives of many phyla more complex than platyhelminths also lose internal organs. Caecum, for example, the smallest snail, has lost its internal respiratory system entirely and takes in oxygen through its external surface.

  Other similarities, cited by Hanson, may be homologous, but so widespread among other creatures that they merely illustrate the broader affinity of all protists with all metazoans, not any specific pathway of descent. Meaningful homologies must be confined to characters that are both shared by descent and derived. (Derived characters evolve uniquely in the common ancestor of two groups that share them; they are marks of genealogy. A shared primitive character, on the other hand, cannot specify descent. The presence of DNA in both ciliates and acoeles tells us nothing about their affinity because all protists and metazoans have DNA.) Thus, Hanson mentions “complete ciliation” as a “permanent character significantly held in common by ciliates and acoeles.” But cilia, although homologous, are a shared primitive character; many other groups, including cnidarians, have them. The completeness of ciliation, on the other hand, represents an “easy” evolutionary event that may only be analogous in ciliates and acoeles. The external surface sets a limit to the maximal number of cilia that may be affixed. Small animals, with high surface/volume ratios, may indulge in ciliary locomotion; large animals cannot insert enough cilia on their relatively declining surface to propel their mass. The complete ciliation of acoeles may reflect a secondary, adaptive response to their small size. The tiny snail Caecum also moves by cilia; all its larger relatives use muscular contraction for locomotion.

  Hanson is, of course, well aware that he cannot prove his intriguing hypothesis with the classical evidence of morphology and function. “The best we can say,” he concludes, “is that many suggestive similarities are present [between ciliates and acoeles], but no rigorously definable homologies.” Is there another method that might resolve the issue, or are we permanently condemned to unresolvable wrangling? Homology might be established with confidence if we could generate a new set of characters sufficiently numerous, comparable, and complex—for analogy cannot be the explanation of detailed, part-by-part similarity in thousands of independent items. The laws of mathematical probability will not allow it.

  Fortunately, we now have a potential source of such information—the DNA sequence of comparable proteins. All protists and metazoans share many homologous proteins. Each protein is built of a long chain of amino acids; each amino acid is coded by a sequence of three nucleotides in DNA. Thus, the DNA code for each protein may contain hundreds of thousands of nucleotides in a definite order.

  Evolution proceeds by substitution of nucleotides. After two groups split from a common ancestor, their nucleotide sequences begin to accumulate changes. The number of changes seems to be at least roughly proportional to the amount of time since the split. Thus, overall similarity in nucleotide sequence for homologous proteins may measure the extent of genealogical separation. A nucleotide sequence is a homologizer’s dream—for it represents thousands of potentially independent characters. Each nucleotide position is a site of possible change.

  Techniques are just now becoming available for the routine sequencing of nucleotides. Within ten years, I believe, we will be able to take homologous proteins from all the ciliate and
metazoan groups at issue, sequence them, measure the similarities between each pair of organisms and obtain greater insight (perhaps even resolution) for this old genealogical mystery. If acoeles are most similar to protist groups that might achieve multicellularity by evolving cell membranes within their bodies, then Hanson will be vindicated. But if they are closest to protists that can reach multicellularity by integration within a colony, then the classical view will prevail, and all metazoa will emerge as the products of amalgamation.

  The study of genealogy has been unfairly eclipsed in our century by the analysis of adaptation, but it cannot lose its power to fascinate. Simply consider what Hanson’s scenario implies about our relationship with other multicellular organisms. Few zoologists doubt that all higher animals achieved their multicellular status by whatever method the flatworms followed. If acoeles evolved by the cellularization of a ciliate, then our multicellular body is the homolog of a single protistan cell. If sponges, cnidarians, plants and fungi arose by amalgamation, then their bodies are the homologs of a protistan colony. Since each ciliate cell is the homolog of an individual cell in any protistan colony, we must conclude—and I do mean this literally—that the entire human body is the homolog of a single cell in a sponge, coral, or plant.