A sign of the spines

According to the old, if inaccurate, aphorism ontogeny recapitulates phylogeny, or the development of an individual organism replays its evolutionary history. This idea was seen in the work of various scholars, from Ernst Haeckel to Sigmund Freud, but at the turn of the 20th century some paleontologists thought it could hold true stated the other way. Might the evolution of a group of organisms mimic the growth of an individual organism, from birth (emergence of a new species) to death (extinction)?

In his 1917 textbook Organic Evolution the paleontologist Richard Swan Lull considered the ontogeny of individuals and groups of organisms together. He called the latter concept the "Racial Cycle" and noted that it was primarily based upon the work of invertebrate specialists. Ammonites, the cephalopods with coiled shells so common during the Mesozoic, were a good example. The shell of an old individual would record the entire life of the animal, form simple beginnings to structural "decadence" before becoming simple again as it approached death.

According to Lull this same cycle could be applied to entire lineages. The signs of "racial old age", in particular, were hard to miss;

Just as senility may readily be recognized in the individual by certain characteristics such as the graying of the hair, loss of teeth, of upright carriage, of vigor and elasticity of step, so to the trained eye characteristics are discernible which point to racial senility.

Taking his cues from the English paleontologist Arthur Smith Woodward, Lull listed the signs of evolutionary senescence as follows;

• Relative Increase of Size.--One of the characteristics recognizable as belonging to racial senescence, although having no parallel in that of the individual, is relative increase of size far beyond that which is usual in the group to which the animal belongs. In certain recorded instances among the prehistoric animals, such an increase was followed by extinction, and in several living examples racial death is certainly threatened if not a very real probability, for ... great increase of size is accompanied by slow maturity and consequent lessening of the rate of increase, which severely handicaps the species in the struggle for existence.

• Spinescence.--Another gerontic character found occasionally in all skeleton-bearing animals is spinescence, that is, the tendency on the part of the shells of molluscs and of brachiopods, the external mail of Crustacea, and even the internal skeletons of vertebrates to produce a superfluity of dead matter. ... In general, such excrescences seem like growth-force run riot, as though with the lessening vitality incident to racial old age, it is no longer adequately controlled.

• Degeneracy.--Physical degeneracy is another phylogerontic trait, this time paralleling certain senile characteristics of the individual. Among these is loss of teeth, which is recorded several times: first, among the fishes such as the sturgeon and certain deep-sea forms like the "gulper" eel, Macropharynx, which evidently feeds upon the bottom oozes. The turtles, which are among the oldest of living reptiles, had lost their teeth by Triassic time, when they first appear in the rocks; the birds, which were toothed during the Age of Reptiles, have also been toothless since its close.

The tie between "spinescence" and senescence was the best example of this trend and had primarily been popularized by the paleontologist Charles Emerson Beecher. Collected in The Origin and Significance of Spines his work related an increase in spines, thorns, and similar structures to the rise and fall of groups of organisms.

Beecher saw the accumulation of spines as a limit to evolution. The more spinose an organism was the more stringent the limit on its evolution. It could keep on adding complexity to its ornamentation but its ability to leave descendants became hindered as it did so. This was related to the development of spines in echinoderms. There could hardly be more spiny creatures, and each spine of an adult is dead tissue moved by living tissue at its base. This means that the spine, when fully formed, can never be modified or grow into anything else. Beecher's view was that very spiny organisms followed the same sort of pattern. The more they weighed themselves down under dead tissue the more unlikely they were to be able to change their forms. [Nevermind the evolution and persistence of sea urchins over geologic time.]

The interaction between living and dead tissue was important to Beecher's hypothesis. A "young" group of organisms are more plastic or adaptable because most of their resources and energy is spend on living tissue important to the basic functioning of the organism. As ornaments made of dead tissue are added, however, more resources are expended in producing dead tissue. This hinders the development of living tissue, according to Beecher, and contributes to the decline of the group. This is why groups appeared to become extinct soon after they reached the height of spinosity, just as individual animals would grow old and die after the acme of their growth. Beecher summarized his views as follows;

So in organisms, the smooth rounded embryo or larval form progressively acquires more and more pronounced and highly differentiated characters through youth and maturity. In old age, it blossoms out with a galaxy of spines, and with further decadence produces extravagant vagaries of spines, but in extreme senility comes the second childhood, with its simple growth and the last feeble infantile exhibit of vital power.

The history of a group of animals is the same. The first species are small and unornamented. They increase in size, complexity, and diversity, until the culmination, when most of the spinose forms begin to appear. During the decline, extravagant types are apt to develop, and if the end is not then reached, the group is continued in the small and unspecialized species, which did not partake of the general tendency to spinous growth.

...

From the study of the ontogenies of spinose forms, it has already been ascertained that they were simple and inornate during their young stages; and from the phylogenies of the same and similar forms, it was likewise learned that they were all derived from non-spinose ancestors. It has also been shown that spines represent an extreme of superficial differentiation which may become fixed in ontogeny, and the further conclusion, that spinosity represents a limit to morphological and physiological variation, has been reached. Finally, it is evident that, after attaining the limit of spine differentiation, spinose organisms leave no descendants, and also that out of spinose types no new types are developed.

This idea appeared to work for marine invertebrates, but what about vertebrates? As Lull's listing shows other characteristics thought to mark "old phylogenetic age" were added to fit vertebrates into this scheme. Large size, toothlessness, or the adoption of an eel-like body shape could be just as effective as spinosity in making organisms seemingly inadaptable. What is strange, however, is that some groups said to contain "gerontic" characteristics were relatively successful. (By this I mean the group persisted over many millions of years, was marked by a diverse number of species, and may have living descendants.) Even though toothlessness is rated a "degenerate" character, for example, turtles and birds survived in great numbers to the modern day and had been toothless for many millions of years. If toothlessness was a sign of evolutionary senility and decline then turtles and birds showed no sign of it.

Even the dinosaurs, clearly suffering from these traits indicative of evolutionary old age, did not precisely fit the hypothesis. The reason for their dominance over the Mesozoic world while exhibiting so many aberrant traits was as puzzling to Lull as their extinction;

In several instances among prehistoric forms extinctions have come with startling suddenness so far as our records show, and in each instance without known competitors which could possibly have worsted the race in an interracial strife. As the representatives of these forms often showed in one way or another certain of the phylogerontic characteristics which have been mentioned, the inference is that they died a natural death. Instances are the dinosaurs, of which the first to be rendered extinct were the gigantic Sauropoda, Brontosaurus [=Apatosaurus] and its kind, who died out long, long before the final extinction of the dinosaurs as a whole; and when the race had well-nigh run its course, we see some forms gigantic, others spinescent, others toothless, and the marvel is, not that they died, but that they survived so long, for the years of dinosaurian dominance exceeded in number the warriors of 1915.

The biologist Horatio Hackett Newman expanded on Lull's framework in his 1920 textbook Vertebrate Zoology. Newman proposed that a "young" group of organisms was marked by being small, highly active, and unencumbered by armor or ornamentation. An old one, on the other hand;

is characterized by sluggish behavior, by herbivorous habits or feeding habits involving little exertion, by structures on the whole specialized or degenerate, often by giant size or bulky build, and by accumulations of inert materials such as armor, spines, heavy bones or flesh. These and other characters are now very generally recognized as criteria of racial senescence.

What could cause this aging of lineages? Newman did not argue that senescent groups had become "degenerate" through overspecialization but through internal mechanisms that became more apparent as groups aged. It was well known that malfunctions of endocrine glands in the body could cause individuals to improperly develop, so perhaps something similar was happening to the "degenerate races";

It is not unlikely that racial senescence, like individual senescence, may be the result of a progressive deterioration of the germinal determiners of these important balance-wheels of organic growth. It is also not unlikely that most of the changes in bodily proportion, which constitute a vast preponderance of specific and racial differences, are largely due to relative racial atrophy or hypertrophy of these growth-regulating glands. The giant races may be those in which thyroid abnormality has unloosed the restraints to growth, and size has reached the limit of mechanical possibility. Similarly racial thyroid or hypophysis atrophy may account for degenerate types.

"Racial senescence" was clearly a messy concept. Examples were cherry-picked from all over the fossil record, and even then many of them appeared to conflict the evolutionary lesson they were supposed to teach. It was also unclear whether it should be understood as overspecialization or by some kind of internal force (with natural selection acting as the grim reaper in either case).

Perhaps the concept of evolutionary senescence was attractive because it appeared to be useful in identifying patterns of evolution and extinction in the fossil record. As a summary of the "Decline and Senescence of Groups" in the 1911 edition of the Encyclopedia Britannica noted "Periods of gradual evolution and of efflorescence may be followed by stationary or senescent conditions." Why should this be so? Why did fossil groups seem to undergo quick periods of evolution but then undergo little change or fail to generate further disparity in form? Evolutionary senescence appeared to be as good an explanation as any, even if its mechanism was impossible to know for certain.

Much like orthogenesis the idea of "racial senescence" was abandoned by the middle of the 20th century. Even so, questions of pattern, extinction, and persistence in the fossil record remained. It was not until the 1970's that these puzzles began to be solved when paleontology and paleobiology were revitalized by researchers like Stephen Jay Gould, Niles Eldredge, Jack Sepkoski, David Raup, Thomas Schopf, and others. (See David Sepkoski's wonderful new paper on this subject, freely available here [pdf]). This was the revolution that brought paleontology back to the "high table" of evolutionary study, and I am certainly glad to see the developing synthesis between it and other biological disciplines (like evo devo and molecular biology).