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Thermal Physiology and the Origin of Terrestriality in Vertebrates

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Thermal Physiology and the Origin of Terrestriality in Vertebrates Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2005? 2005 1433 345358 Original Article ORIGIN OF TETRAPODSR. L. CARROLL ET AL. Zoological Journal of the Linnean Society, 2005, 143, 345–358. With 11 figures Thermal physiology and the origin of terrestriality in vertebrates ROBERT L. CARROLL FLS1*, JASON IRWIN2† and DAVID M. GREEN1 1Redpath Museum, McGill University, 859 Sherbrooke St. West, Montreal, Quebec, Canada, H3A 2K6 2Biology Department, Bucknell University, Lewisburg, Pennsylvania, PA 17837, USA Received January 2004; accepted for publication September 2004 The adaptive reasons for the evolutionary transition between obligatorily aquatic lobe-finned fish and facultatively terrestrial early tetrapods have long been debated. The oldest adequately known amphibians, Acanthostega and Ich- thyostega, from the final stage in the Upper Devonian (Famennian), can be clearly distinguished from the most advanced choanate sarcopterygian fish from the next older stage (Frasnian) by the presence of large pectoral and pel- vic girdles, limbs generally resembling those of later Palaeozoic land vertebrates, and the absence of bones linking the back of the skull with the shoulder girdle. Upper Devonian and most Lower Carboniferous amphibians, like their aquatic predecessors, differed significantly from modern amphibians in their much larger size, up to a metre or more in length. Animals of this size, resembling modern crocodiles and the marine iguana, could have raised their body temperatures by basking in the sun and sustained them upon re-entry into the water. It is hypothesized that the physiological advantages of thermoregulation were a major selective force that resulted in the increasing capacity for the ancestors of tetrapods to move into shallow water, and later to support their bodies against the force of gravity and increase the size and locomotor capacities of the limbs. © 2005 The Linnean Society of London, Zoological Jour- nal of the Linnean Society, 2005, 143, 345–358. ADDITIONAL KEYWORDS: Acanthostega – basking – Carboniferous – Devonian – Eusthenopteron – footprints – Ichthyostega – Panderichthys – tetrapods – thermoregulation. INTRODUCTION erable morphological gap between the typical fish fins in Eusthenopteron and the tetrapod limbs of Acan- One of the most significant events in the history of ver- thostega (Fig. 1). Based on the presence of a fish-like tebrates was the attainment of a terrestrial way of life. tail and the apparent retention of internal gills, Clack The phylogenetic sequence from choanate sarcoptery- & Coates (1995) suggested that Acanthostega and Ich- gian fish such as Eusthenopteron to primitive tetra- thyostega were primarily aquatic, and that ‘tetrapod’ pods is documented by the fossil record of the Late limbs might have evolved for aquatic locomotion. Devonian to Early Carboniferous, but the adaptive or selective advantage of the transition between life in the water and life on land has remained difficult to GIRDLES AND LIMBS explain. To investigate the initiation of terrestriality, it is nec- Numerous hypotheses to explain this transition essary to know the specific sequence of structural (Table 1) were discussed in the recent book, Gaining change. The broad outline of the phylogenetic relation- Ground (Clack, 2002a). Clack hesitated to chose ships of the best known genera involved in this among these hypotheses, citing the still incomplete sequence (Fig. 2) is generally agreed upon at present knowledge of the fossil record. There is still a consid- (Coates, 1996; Ahlberg & Johanson, 1998; Coates, Jef- fery & Ruta, 2002; Ruta, Coates & Quicke, 2003). Attention has long been focused on the hands and feet as being unique characters of tetrapods, but *Corresponding author. E-mail: [email protected] †Current address: Biology Department, Okanagan University the known Upper Devonian fossils retain distinctly College, 3333 University Way, Kelowna, BC Canada VIV 1V7 archaic characteristics relative to Carboniferous © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 143, 345–358 345 346 R. L. CARROLL ET AL. Table 1. Hypotheses to explain the origin of tetrapods, 5 more clearly resemble distal tarsals, although they based largely on Clack (2002a) are in line with a bone identified as a fibulare because of its articulation with the fibula. However, this ‘fibu- 1To get back into the water under arid conditions (Romer) lare’ articulates distally with bones resembling the 2 ‘Limbs’ initially for burrowing in the mud (Orton) metatarsals of digits 3–5, without the interposition of 3 Competition and/or predation with other aquatic forms bones resembling distal tarsals. If the bones proximal (McNamera, Shelden) to digits 2–4 are distal tarsals, the phalangeal counts 4To escape oxygen-depleted water of these digits are 3, 3, 3. The more lateral digits are 5Feeding on terrestrial or semiterrestrial food sources incomplete distally. The tarsus of Ichthyostega appears 6 Increase in body temperature (Clack) nearly completely ossified, but there remains the ques- a. Increase in rate of digestion tion of homology in the area of the distal tarsals and b. Speed development metatarsals. In Tulerpeton, the 5th digit of the manus 7 Spawning on land 8 Limbs evolved originally for amplexus in the water appears to correspond with that of some Carboniferous (Martin, 2002) labyrinthodonts in having a phalangeal count of 4, a discrete metacarpal, and being separated from the ulnare by a squarish distal carpal. In contrast, the bone that has the appearance of the metacarpal of the 4th digit articulates directly with the ulnare, without the amphibians (Fig. 3). The autopodia (the bones distal to intervention of a typical, squarish distal carpal. In the the ulna and radius in the forelimb and the tibia and foot, there appear to be typical distal tarsals proximal fibula in the hind limb) of Acanthostega, Ichthyostega to most if not all metatarsals, but with no more than and Tulerpeton (Coates et al., 2002) are comparable two rows of tarsals medially. with those of later tetrapods in the presence of the The structure of the autopod, especially in Acan- mesopodium (the carpals and tarsals), metapodium thostega, suggests that the movements across the (metacarpals and metatarsals) and digits, but the wrist and ankle joints were significantly different number and arrangement of these bones are more from those of later tetrapods. Clack (2002a) illustrated variable and distinctly more primitive than those of Acanthostega in association with the reputed foot- well-known Carboniferous and Permian tetrapods, prints of a Devonian tetrapod, suggesting lateral ori- suggesting a period of ‘experimentation’, during which entation of the digits, as might be appropriate for the more effective joints of the wrist and ankle of later aquatic locomotion (Fig. 4). tetrapods had not yet evolved (Carroll & Holmes, It is only later, in the Lower Carboniferous (Tour- 2005). naisian) Horton Bluff Formation in Nova Scotia that In Acanthostega, the ulna extends well beyond the typical footprints with forward-facing digits have been radius, precluding an effective wrist joint, and most of documented (Matthew, 1905; Sarjeant & Mossman, the carpus remains unossified. The number of digits 1978). In a more recently collected trackway (Fig. 5), varies from eight in both the hand and the foot of Acan- the stride and pace are comparable with those of thostega, to seven in the foot of Ichthyostega (no fossil Upper Carboniferous and Permian amphibians. Other is yet known that shows the full structure of the manus; trackways represent animals walking in shallow Clack, Blom & Ahlberg, 2003), and six in Tulerpeton water, and record the movement of the digits in an (Lebedev & Coates, 1995). As emphasized by Coates anterior to posterior direction. Many newly discovered et al. (2002), the feet of Acanthostega and Tulerpeton footprints and trackways from the Horton Bluff For- appear to have evolved more rapidly than the hands. mation are now under study at Redpath Museum, Acanthostega is notable in ossifying only one element McGill University. of the carpus (the intermedium). The ossification of the Clack (2002b) emphasized the asymmetrical shape tarsus is also limited. Coates et al. (2002) state that of the metatarsals in the Tournaisian whatcheerid there appear to be fewer than the three rows of carpals Pederpes that indicates forwardly directed digits, as in and tarsals common to later Palaeozoic tetrapods, but later tetrapods. By the Viséan and Namurian A, a rel- the number is difficult to specify because of the problem atively consistent pattern of three rows of carpals and of establishing the homology of the elements between tarsals had been established, as exemplified by the the proximal row of carpals and the digits. In the hand putative stem amniote Westlothiana (Smithson et al., of Acanthostega, the proximal elements of the digits are 1994), the colosteid Greererpeton (Godfrey, 1989) and elongate bones that might be identified as metacarpals, the temnospondyl Balanerpeton (in which the number indicating a phalangeal count of 4, 4, 4, 4, 5, 5, 5, 4. Or of digits in the manus is reduced to four) (Milner & (as indicated by Coates, 1996) they may be distal car- Sequeira, 1994) (Fig. 3F–I). pals, giving a count of 3, 3, 3, 3, 4, 4, 4, 3. In the foot, Although the fossil record is still very inadequately the more squarish bones proximal to digits 2, 3, 4 and known and marked by large
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