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evolution

When snakes had paws

Polemics over serpents shows how organisms can acquire or lose apparently essential characteristics

MARK WIDHALM / FIED MUSEUMFossil of Haasiophis terrasanctus: hind paw (highlighted on the side) ancestor in common with today’s boa constrictor and rattlesnake MARK WIDHALM / FIED MUSEUM

Admired and feared, mysterious and seductive, serpents are a challenge to herpetologists (specialists in reptiles) and paleontologists, who just can’t find the answer to an old question: what, after all, is the origin of these animals? The debate is heated. In 1997, Michael Caldwell, a Canadian, and Michael Lee, an Australian, believed they had unveiled the mystery. In an article published that year in Nature, they analyzed two fossils of snakes with hind paws, which lived 95 million years ago and were found in Israel. The conclusion: they were species that originated in a marine environment and were a possible link between mosasaurs – large lizards that inhabited the seas in the days of the dinosaurs – and serpents, a group of snakes made up of about 3,000 species.

Brazilian Hussam Zaher pooh-poohed the idea as soon as he read the work. A researcher at the Zoology Museum of the University of São Paulo (USP), he threw a bucket of cold water on the idea that the species being studied, Pachyrhachis problematicus, could be the common ancestor of all snakes and came from the sea. His studies, which were transformed into eleven articles, including one published in Science in 2000, maintain that Pachyrhachis is not the long awaited missing link. It is, rather, an animal close to a group of today’s snakes, the macrostomates, like the rattlesnake (Crotalus durissus), the boa constrictor (Boa constrictor) and the python (Python reticulatus).

“This controversy helped to refine the morphological knowledge about serpents, and showed that the evolution of this group of animals is far more complex than one imagined, although the question about the origin of the serpents remains without an answer”, Zaher warrants. The debate on the origin of snakes, fueled by means of scientific articles with painstakingly constructed arguments, leads specialists at one time to applaud an idea, and at another to balk at conclusions that used to seem well founded. In a wider manner, he recalls that the evolutionary process of species in general does not havea predetermined direction, nor does it necessarily lead to more advanced organisms – characteristics like paws, apparently essential, may arise and, later on, simply disappear.

The front paws of snakes had already disappeared, millions of years previously, by mechanisms different from those that led to the elimination of the hind paws. According to studies published in 2000 by English researchers, the front members went away radically, without leaving any trace, due to a group of regulatory genes being disabled. The disappearance of the hind paws, on the other hand, is due to the loss of a structure in the embryo called the ectodermic apical crest. The hind paws waste away and disappear unless they are used, as if the organism had decided no longer to channel its energy into that part of the body, which had proved to be unnecessary – in a process similar to the one seen with cave fish, which almost all have atrophied eyes or even none at all.

According to Zaher, in the Cretaceous period, between 144 and 65 million years ago, all serpents had hind paws that gradually disappeared as the lineages evolved up to today, and not just at once, from an ancestor that still showed a vestige of paws. To be sure, these paws were not used for movement or support, as they were too small. One hypothesis is that they could have fulfilled some kind of function during the sexual act.

The story of Pachyrhachis, the first snake with paws, began at the end of the 60’s, when the fossil was discovered at Ein Yabrud, an archeological site near to Jerusalem, in Israel. Some 95 million years old, the intriguing serpent with paws was initially studied by a Jewish paleontologist of Austrian origin called George Haas, one of the great names in herpetology of those days.

For a moment, at the end of the 70’s, Haas had in his hands two fossils of snakes with paws. The first had a cranium, but the tail was missing. The second showed the opposite characteristics: the tail, from which the hind paws came, had been preserved, but the cranium was no longer very visible. Although the two animals showed great similarity and were very close to serpents, Haas preferred not to risk it and described two different species: the one that had paws was classified as Ophiomorphus colberti and associated with a marine lizard of the dolichosaur lineage. The other, a snake, was given the name of Pachyrhachis problematicus – a clear allusion to the questions it left unanswered.

The fossils spent over 20 years in a drawer at the Hebrew University of Jerusalem, until Caldwell and Lee, now in the 90’s, rescued the subject. “Those animals were supposedly the ancestors of snakes, but no one had yet studied them with proper methods, as it ought to have been done”, says Lee, from Adelaide University, in Australia. The two paleontologists did not need long to conclude that Haas, who died in 1981, had been too cautious. The two fossils described actually belonged to a single species – Pachyrhachis. “We then had just one animal”, explains Zaher. “It was a snake with paws”. That was were agreement ended.

Caldwell and Lee went back to the theses of the American paleontologist Edward Drinker Cope, who lived in the 19th century. For him, serpents had originated in the marine environment – and they were heirs of the mosasaurs. The place where the Pachyrhachis fossils were found made this possibility very feasible. The presence of hind paws was the last piece in the jigsaw puzzle. This was the picture that led the two paleontologists to assert, in an article in Nature in April 1997, that the missing link between snakes and marine lizards had been found. “Pachyrhachis offers additional evidence on the affinities there are between the mosasaurs and serpents, bringing new information to light on the characteristics of primitive ophidians”, says Caldwell, who is today with the University of Alberta, in Canada.

“As soon as I read the work, I noticed a series of inconsistencies”, Zaher countered. In the first place, says he, some of the characteristics of the cranium of these animals were not taken into consideration, which – in his view – are decisive. These included the presence of dentition in the palate, one of the bones in the roof of the mouth, and of a supratemporal bone that goes to the back of the cranium. In addition, the analysis had left out a primitive species that was fundamental for understanding the evolution of these animals: Dinilysia patagonica, an extinct snake from the Upper Cretaceous in Argentina. Finally, Caldwell and Lee had summed up all the current diversity of snakes into just two groups, the Scolecophidia and Alethinophidia, leaving aside the macrostomates, which occupy a higher place in the serpents’ evolutionary line – and with which, as would be seen, Pachyrhachis shows significant likenesses.

The criticisms became more pressing when Zaher knew of a third fossil of a snake with paws that was said to have been discovered together with the Pachyrhachis, also in Ein Yabrud. It was only two years later, in 1999, that Zaher was authorized by the Hebrew University of Jerusalem to study the animal. In those days, he was already working with Olivier Rieppel, a fossil curator at the Field Museum, in Chicago, United States, who brought an accurate copy of the new snake with paws to USP in December 1999. Rieppel and Zaher thoroughly analyzed the fossil, based on modern concepts of comparative anatomy and evolutionary biology. “It is the cranium that holds the key to the understanding of the problem”, explains the researcher from USP.

This line of thinking showed that they were dealing with a new species: the specialized dentition in the roof of the mouth and in the mandible, added to the absence of a symphysis, the firm place of union between the two jaw bones, which guarantees the mandible greater mobility, meant an important evolutionary novelty in the history of the group, and gives serpents greater skill in catching medium and large sized prey. According to Zaher, these are characteristic of the macrostomates, serpents like the rattlesnake, the boa constrictor and the python, which have developed the ability to prey on whole animals, far larger than the diameter of their mouths. A retrospective analysis confirmed it: these elements can also be clearly seen in the Pachyrhachis.

So as to leave no doubts, Zaher makes comparisons with more distant serpents: in the Scolecophidia, the most primitive group of snakes known to date, the representatives of which look outwardly like worms, the reality is the opposite. With them, the movements of their snouts are limited, the mandible is short, and there are no teeth in the roof of the mouth. They are animals adapted to microphagy – preying on small creatures like ants and termites.

In the March 2000 issue of Science, Zaher and Rieppel described the new species of snake with paws, called Haasiophis terrasanctus in honor to Haas and to the region where it was found. In the article, they are categorical: “Pachyrhachis and Haasiophis are derived serpents, close in evolutionary terms to the macrostomates, and there is no way they can be associated with the moment in history in which these animals originated”. Caldwell rebuts this: “They admit that they described only the bones of the cranium, ignoring other parts of the fossil. This is an extremely limited procedure”.

While the debate is running, Zaher is expanding the collection of the current and fossil groups of snakes, which now has hundreds of specimens. This is where the search is based for the relations of kinship between the families and for evolutionary episodes, like the decline of the paws. For him, the search for the missing link, which would reveal the story of the origin of the serpents, has still not finished. “My intuition says that the strongest candidate for playing this role is a fossilized animal”, he comments. “With time, the scientific evidence will say if I am right”.

The Project
The fauna of the microvertebrated tetrapods of the Upper Cretaceous in the regions of Marília and Presidente Prudente (SP): biodiversity, philogeny and taphonomy; Modality Regular research project benefit line; Coordinator Hussam El Dine Zaher – Institute of Biosciences/USP; Investiment R$ 124,270.00

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