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ScienceWeek
EVOLUTION: ON THE EVOLUTION OF INTERNAL NOSTRILS (CHOANAE)
The following points are made by Philippe Janvier (Nature 2004 432:23):
1) The structures known as "choanae" may seem obscure, but we all have them: they are the "internal nostrils" that form the passage between our nasal cavity and throat that we use for breathing when our mouth is closed. They have also been the subject of much argument among those studying comparative vertebrate anatomy --in particular, the question of how choanae originated in the tetrapods, or land vertebrates, a group that consists of amphibians, reptiles, birds and mammals.
2) This unique feature of the tetrapod palate was first regarded as an adaptation to breathing air. Now, however, we know that choanae occurred first in extinct fish relatives of the tetrapods at least 380 million years ago -- that is, 30 million years before tetrapods developed limbs and took to the land. So choanae may not have been initially involved in breathing. But did they arise as a novelty within the ancient fish relatives of tetrapods, or were they derived from a pre-existing structure in other fishes? This is a debate that has lasted for about a century, but it is practically settled by new data presented by Zhu and Ahlberg(1). The subject of their studies is Kenichthys, a 395-million-year-old fossil fish from China.
3) Most living jawed fishes have two external nostrils on each side of the snout: an anterior one allowing entry of water into the nasal cavity, and a posterior one for its exit. In contrast, tetrapods have only one pair of external nostrils, but their nasal cavity communicates with the mouth cavity by means of the choanae. A single group of living fish, lungfishes, seemed to bridge this gap between fish and tetrapods, as they have "internal nostrils" in their palate that superficially resemble the choanae. Early evolutionary anatomists thus considered that lungfishes constituted ideal intermediate forms, and were evidence for the piscine origin of tetrapods. Embryological studies then showed that these "internal nostrils" in fact corresponded to the posterior nostrils of other fishes, but they were also taken to be homologous with -- that is, the same as --the tetrapod choanae. The choanae were thus regarded as posterior nostrils that had migrated into the palate in the common ancestor of lungfishes and tetrapods.
4) Early in the twentieth century, however, that view was shaken by work on certain lobe-finned fishes from the Palaeozoic era (385-280 million years ago). These fishes, later referred to as "osteolepiforms" and including such examples as Osteolepis and Eusthenopteron(2), proved to have a single external nostril on either side of the snout, and choana-like openings in the palate. They became preferred as "ancestors" to tetrapods because of their close overall resemblance to them and their antiquity, and it soon became received wisdom that the tetrapods had originated from osteolepiforms. The lungfish "internal nostrils" became increasingly regarded as having merely paralleled the tetrapod choanae in evolution, because of major differences in their relationships to the surrounding nerves, bones and sensory-line canals(3). This was later confirmed by the discovery of Diabolepis, a primitive, 400-million-year-old lungfish, which retains two pairs of external nostrils (and thus lacks "internal nostrils")(4).
5) Several theories have been proposed for the origin of the choanae of tetrapods and of their fossil osteolepiform relatives. The two main possibilities are that choanae are derived from the posterior external nostrils, but independently of development of the "internal nostrils" of lungfishes, or that they are a novelty, and the posterior external nostrils have either disappeared or became the tear ducts. Debate on the matter rumbled on for decades. Rosen et al(5) even revived the theory that lungfishes have true choanae, and claimed that osteolepiforms provide no evidence for choanae, thereby creating a controversy that has had far-reaching consequences for the use of fossil data in reconstructions of evolutionary history.
6) The work of Zhu and Ahlberg(1) clearly provides the first factual basis for the theory that tetrapod choanae actually are the posterior nostrils, as are the internal nostrils of lungfishes. In a way, the new analysis reconciles the Rosen et al(5) provocative theory and the classical interpretation of the fish members of the tetrapodomorphs -- internal nostrils of lungfishes and tetrapod choanae are homologous, but their position in the palate is not.
References (abridged):
1. Zhu, M. & Ahlberg, P. E. Nature 432, 94-97 (2004)
2. Ahlberg, P. E. & Johanson, Z. Nature 395, 792-794 (1998)
3. Jarvik, E. Zool. Bidrag Uppsala 21, 235-675 (1942)
4. Chang, M. M. Bull. Mus. Natl Hist. Nat. 17, 235-268 (1995)
5. Rosen, D. E., Forey, P. L., Gardiner, B. G. & Patterson, C. Bull. Am. Mus. Nat. Hist. 167, 157-276 (1981)
Nature http://www.nature.com/nature
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PALEONTOLOGY: ON THE FISH-TETRAPOD TRANSITION
The following points are made by Jennifer A. Clack (Science 2004 304:57):
1) How did animals get from fins to fingers, from an animal that swims in water to one that walks on land? This key evolutionary innovation was apparently first made during the Devonian period, approximately 370 to 360 million years ago, and it can be succinctly described as the "fish-tetrapod transition". In recent years, the fossil evidence for this event has increased almost exponentially in quality and quantity, stimulating fresh ideas and changing perspectives (1).
2) Shubin et al (2) revealed how even fragmentary finds can be used to draw inferences about the nature and sequence of changes that must have taken place during the evolution of terrestrial locomotion by tetrapods. Shubin et al (2) describe a humerus bone from the Devonian period that they discovered in Pennsylvania. The morphology of this limb bone proclaims it to be not only from a tetrapod, but from one predicted to be of a completely new and unusual form. From this humerus, the researchers infer some of the anatomical and functional changes that took place in the tetrapod lineage during the Devonian period, and these changes in turn suggest some possible routes by which terrestriality was attained.
3) The lobe-finned relatives of early tetrapods had complex internal skeletons and a suite of muscles in their paired fins, features eventually exploited to produce weight-bearing limbs. Among the immediate relatives of tetrapods, the most proximal three elements of their limbs can be readily identified as related to the humerus, radius, and ulna of the forelimb, and the femur, tibia, and fibula of the hindlimb. The humeri of Devonian tetrapod-like fish such as Eusthenopteron and Panderichthys bear particular resemblance to those of early tetrapods, and several key features are common to them all. However, fins and limbs are conspicuously different with respect to orientation, range of movement, and function. The new humerus found by Shubin et al (2) provides some clues as to the timing and sequence in which these differences arose, although it poses yet more intriguing questions.
4) The new humerus, like those of other Devonian tetrapods and their close relative Panderichthys, is flattened dorsoventrally, and the shoulder joint appears to have had a greatly restricted range of movement. However, in Panderichthys, as in other fish, the fin and shoulder joint face posteriorly, whereas in tetrapods they are reoriented to face laterally. As a result of this reorientation, the attitude of the limb to the body is essentially horizontal rather than vertical; the operational space in which the limb acts is level with the shoulder joint rather than posterior to it; and the direction in which its muscles pull is approximately at right angles to the body rather than at an acute angle to it. Shubin et al (2) suggest that features such as the orientation of a ridge on the ventral side of this new humerus show that some of these changes had already taken place. The net result was probably a limb that was effective in the dorsoventral plane and could prop up the relatively large plated head of an early tetrapod, but whose front-to-rear movement, necessary for walking, was very limited.
References (abridged):
1. J. A. Clack, Gaining Ground: The Origin and Early Evolution of Tetrapods (Indiana Univ. Press, Bloomington, IN, 2002)
2. N. H. Shubin, E. B. Daeschler, M. I. Coates, Science 304, 90 (2004)
3. E. Jarvik, Fossils Strata 40, 1 (1996)
4. J. A. Clack, H. Blom, P. E. Ahlberg, J. Vertebr. Paleontol. 23, 41A (2003)
5. J. E. Jeffery, Biol. J. Linn. Soc. 74, 217 (2001)
Science http://www.sciencemag.org
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ON EARLY LAND VERTEBRATES
The following points are made by Robert Carroll (Nature 2002 418:35):
1) The transition between fish and land vertebrates was a turning point in the history of life. Early stages in the evolution from aquatic lobe-finned fish to tetrapods -- animals with limbs capable of locomotion on land -- are seen in many fossils from the Upper Devonian(1), just before 363 million years ago. In contrast, few remains are known from the next 30 million years, when the ancestors of the major tetrapod lineages differentiated from one another, an interval that falls in the early part of the Carboniferous period. So striking is the hiatus that Coates and Clack(2) coined the term "Romer's Gap" for it, in reference to the long search of Alfred Sherwood Romer (1894-1973) for fossils dating to that time. It is fitting that Clack (3) should be the first to recognize a well-preserved specimen of a new amphibian species from Romer's Gap. The fossil, Pederpes finneyae, comes from 350-million-year-old deposits at Dumbarton, Scotland.
2) Although the full length of the tail of Pederpes is not known, the animal was probably nearly a meter in length. It was a short-limbed, large-skulled predator, resembling an especially ungainly crocodile. But it almost certainly reproduced in the water, somewhat like modern aquatic salamanders. Grooves in the skull for lateral-line canals � a characteristic of fish � suggest that it lived partly in the water. The foot structure, however, indicates it could walk on land. Pederpes is advanced over its Devonian antecedents in having only five toes on the foot, yet has a relict of a tiny finger on the forelimb reminiscent of the supernumerary digits of the best-known amphibians -- Ichthyostega and Acanthostega -- from the Upper Devonian.
3) Discovery of a nearly complete skeleton in the middle of Romer's Gap should help in establishing the pattern of evolutionary change among early tetrapods. It might also provide context for understanding the interrelationships of all later land vertebrates. Clack demonstrates that Pederpes and other members of the Whatcheeriidae -- the family to which it is assigned -- occupied an intermediate grade between the primarily aquatic Upper Devonian amphibians and later tetrapods. In particular, the feet show major advances towards effective locomotion on land. On the other hand, whatcheeriids have no skeletal features that indicate specific affinities to either of the major groups of "conservative" amphibians, the temnospondyls or anthracosaurs, that dominated the later Carboniferous.(4,5)
References (abridged):
1. Clack, J. A. in Amphibian Biology (eds Heatwole, H. & Carroll, R. L.) 979-1029 (Surrey Beatty, Chipping Norton, Australia, 2000)
2. Coates, M. I. & Clack, J. A. in Studies on Early Vertebrates (eds Arsenault, M., Leli�vre, H. & Janvier, P.) 373-388 (Bulletin du Museum National d'Histoire Naturelle, Paris, 1995)
3. Clack, J. A. Nature 418, 72-76 (2002)
4. Carroll, R. L. in Amphibian Biology (eds Heatwole, H. & Carroll, R. L.) 1198-1269 (Surrey Beatty, Chipping Norton, Australia, 2000)
5. Anderson, J. S. Systematic Biol. 50, 170-193 (2001)
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