Terrestrial Vertebrates

Terrestrial Vertebrates

Michel Laurin *

     =============================================== Ichthyostega  
     |
     |============================================== Acanthostega  
     |
     |============================================== Tulerpeton  
     |
     |     ========================================= Crassigyrinus  
     |     |
     |     |  ====================================== Loxommatidae  
     |     |  |
     |     |  |  =================================== Temnospondyli  
     |     |  |  |
     |     |  |  |  ================================ Whatcheeria  
     |     |  |  |  |
     |     |  |  |  |  ============================= Embolomeri  
     |     |  |  |  |  |
     |     |  |  |  |  |  ========================== Gephyrostegidae  
     |     |  |  |  |  |  |
     |     |  |  |  |  |  |  ======================= Solenodonsaurus  
<<===|     |  |  |  |  |  |  |
     |     |  |  |  |  |  |  |====================== Seymouriamorpha  
     |     |  |  |  |  |  |  |
     ======|  |  |  |  |  |  |             ========= Aistopoda  
           ===|  |  |  |  |  |          ===|
              ===|  |  |  |  |          |  ========= Adelogyrinidae  
                 ===|  |  |  |          |
                    ===|  |  |          |  ========= Nectridea  
                       ===|  |      ==A=|  |
                          ===|      |   |  |  |||||| Microsauria  
                             |      |   ===|  |
                             ====T==|      ===|  === Lysorophia  
                                    |         ===|
                                    |            === Living Amphibians  (frog, salamanders, and caecilians) 
                                    |
                                    |     ========== Amniota  (reptiles, mammals, birds, dinosaurs, etc.) 
                                    |  ===|
                                    ===|  ========== Diadectomorpha  
                                       |
                                       ============= Westlothiana

Modified from Carroll (1995) and Laurin and Reisz (in press). The position of Watcheeria follows Lombard and Bolt (1995). Temnospondyls are often thought to be early amphibians. However, notice that in this phylogeny, they are not closely related to lissamphibians.

Containing clade(s): Sarcopterygii

Introduction

Classification of Terrestrial Vertebrates

Characteristics of Terrestrial Vertebrates

Discussion of Phylogenetic Relationships

Origin of Terrestrial Vertebrates

Early Evolution of the Limbs

References

Introduction

Terrestrial vertebrates include the extant tetrapods and their extinct terrestrial relatives. All members have four muscular limbs with generally well-defined joints and digits (fingers and toes). This group includes about 21100 extant species and a probably much greater number of extinct species.

Terrestrial vertebrates have a worldwide distribution. The earliest members of this group were moderately large (1-2.5 m body length). The oldest known skeletal remains of terrestrial vertebrates are know from the Upper Devonian of East Greenland (Clack, 1994), but the presence of Lower to Middle Devonian trackways in Australia suggests that this group may have originated in the Lower Devonian, at least 400 million years ago (Warren et al., 1986).

The largest group of terrestrial vertebrates is Tetrapoda (see the section "Classification of Terrestrial Vertebrates", below). Tetrapoda means "four feet", and the group was so-named as its members primitively had four limbs, as opposed to fins. This taxon includes about 3000 extant species of amphibians (frogs, salamanders, and caecilians) and approximately 18100 extant species of amniotes (mammals, reptiles, and birds). The number of extinct species of tetrapods is of course unknown, but about half of the currently known species of tetrapods are extinct (Carroll, 1988).

Tetrapods originated no later than the Mississippian (about 350 million years ago), the period from which the oldest known relatives of amniotes and of living amphibians are known (Smithson et al., 1994; Carroll, 1995).

Tetrapods range from 9.8 mm (in the frog Psyllophryne didactyla) to 30 m (in the blue whale) in overall length. They have a worldwide distribution and inhabit all major habitats. Most are terrestrial, but several have returned to the aquatic environment in which our distant ancestors lived. Aquatic tetrapods include various salamanders (sirenids, cryptobranchids, proteids, etc.), frogs (pipids), some caecilians (typhlonectids), leatherback turtles, sea snakes, pinnipeds (seals and walruses), and whales. Some tetrapods are capable of flight (birds and bats), while others glide, such as flying squirrels, dermopterans (sometimes called "flying lemurs", even though they are not primates), and the flying dragons (Draco volans).

The page Life History of Terrestrial Vertebrates contains information on this complex topic.

The main breathing organ of most terrestrial vertebrates is the lung, but other respiratory organs exist in many groups. More detail is available on the Breathing in Terrestrial Vertebrates page.

Many terrestrial vertebrates have a tympanum for hearing high-frequence, air-borne sounds, and a lateral-line organ is found in many aquatic amphibians. For more information, see the Hearing in Terrestrial Vertebrates page.

Classification of Terrestrial Vertebrates

In the past, most terrestrial choanates were included in Tetrapoda (Gaffney, 1979). Recently, Tetrapoda was formally defined as a crown-group (Gauthier et al., 1989). A crown-group is a clade that includes the last common ancestor of two or more extant taxa, and all its descendants. In this case, Tetrapoda was defined as the clade that includes the last common ancestor of lissamphibians and amniotes, and all its descendants. According to Gauthier et al. (1989), Tetrapoda included most known fossil terrestrial vertebrates because temnospondyls were thought to be the stem-group of amphibians, whereas embolomeres, gephyrostegids, and seymouriamorphs were thought to be more closely related to amniotes than to lissamphibians. Therefore, only a few very early terrestrial vertebrates, such as Ichthyostega and Acanthostega, were excluded from Tetrapoda.

The choanate phylogeny presented here suggests that temnospondyls, embolomeres, gephyrostegids, and seymouriamorphs are not part of the crown-group. If it is accurate, these taxa are not tetrapods and the origin of the "tetrapod limb" predates the origin of Tetrapoda. Until a new classification of terrestrial vertebrates reflecting this phylogeny is published, we can simply call these taxa terrestrial vertebrates.

The node marked with an "A" on the tree is referred to by some as Amphibia; others restrict this name to descendents of the most recent common ancestor of extant amphibians (the terminal taxon Living Amphibians in this tree). The author prefers the first usage, and the definition of Amphibia as all tetrapods more closely related to extant amphibians than to amniotes has historical precedence, but the second usage has been fairly widespread and cannot be ignored. In this page, the term Amphibia always refers to node "A" and extant amphibians are referred to as lissamphibians.

The node marked with a "T" is referred to by some as Tetrapoda; others expand the use of this name to include all terrestrial vertebrates. However, in this page, Tetrapoda always refers to node "T".

Characteristics of Terrestrial Vertebrates

Terrestrial vertebrates have an extensive fossil record (Carroll, 1988). Phylogenetic studies have revealed several derived characteristics (synapomorphies) of terrestrial vertebrates:

Loss of several cranial bones.: In osteolepiforms (the group of fishes most closely related to tetrapods), the skull was rigidly linked to the shoulder girdle by several bones that disappeared early in the evolution of terrestrial vertebrates. The loss of these bones also allowed the appearance of a mobile neck that allows the head to be moved relative to the trunk. This decoupling allows the head to remain relatively stable while walking.
Loss of the opercular bones that cover the gill chamber in bony fishes.: The operculum was no longer needed in early choanates because they had lost the internal gills of their early ancestors. However, the operculum may have disappeared before the internal gills (Coates and Clack, 1991).
A reduction of the notochord and a rigid spine.: The vertebral centra of osteolepiforms are thin and surround the notochord (a rigid rod present in all chordates and that persists in man as the intervertebral disks) without constricting it greatly. In terrestrial choanates, the centra are thick and they constrict the notochord. Special articulatory surfaces (the zygapophyses) link the neural arches to each other.
A shorter notochord that does not extend into the braincase.: The notochord of osteolepiforms extended up to the vicinity of the pituitary.
Four muscular limbs with discrete digits (fingers and toes).: Osteolepiforms had fleshy fins with elements homologous to the humerus, radius, ulna, intermedium, ulnare, femur, tibia, fibula, and fibulare, but the homology of more distal limb elements is uncertain, and no digits were present.
A sacral rib connecting the axial skeleton (the spine) to the pelvic girdle (the hip).: This allows the weight of the body of tetrapods to be transmitted to the hind limb. There was no bony connection between the pelvic girdle of osteolepiforms and their axial skeleton.
The loss of dermal fin rays (the modified scales that support the fins).: This simply represents the elimination of a structure that was no longer needed and may even have been harmful on land.

These characters did not appear simultaneously and suddenly. The oldest known terrestrial vertebrates, such as Ichthyostega and Acanthostega, possess intermediate conditions for some of these characters and lack others. For instance, Ichthyostega retained a subopercular, a bone that was part of the opercular complex that covered the gill chamber of osteolepiforms. Acanthostega retained an anocleithrum, which is one of the elements that linked the shoulder girdle to the skull in osteolepiforms (Coates and Clack, 1991). The notochord of Ichthyostega extended deeply into the braincase, and most of its caudal vertebrae lacked zygapophyses (Jarvik, 1952). The connection between the sacral rib and the pelvic girdle of Acanthostega was still poorly defined. Finally, both Ichthyostega and Acanthostega retain lepidotrichia in the tail, indicating that these taxa still had a caudal fin.

The previous list includes only skeletal characters because all the earliest groups of terrestrial vertebrates are extinct, and soft anatomical characters can only be studied in extant taxa. The following characters are found in tetrapods, but not in other extant vertebrates:

A layer of dead, horny cells that reduces evaporative water loss.: This layer is present in amniotes and in most lissamphibians.
A well-developed muscular tongue with glands.: However, some lissamphibians have only a primary tongue, like fishes. A primary tongue is simply a fleshy fold on the floor of the mouth that lacks intrinsic muscles and with limited mobility.
A parathyroid gland involved in controlling the level of calcium in the blood.
A Harderian gland located anterior to the eye.: This gland secretes an oily liquid that lubricates the eye.
A vomeronasal (Jacobson's) organ.: This olfactory organ is located in the palate and is probably used to smell the food in the mouth.
The loss of the internal gills.: The external gills present in many aquatic and larval lissamphibians are new structures and are not homologous with the internal gills of fishes.

It is difficult to determine exactly when these characters appeared because they are not preserved in fossils, except for indirect clues about the internal gills, and the closest known relatives of tetrapods are extinct. However, these characters are not found in lungfishes (the closest extant relatives of tetrapods). Acanthostega, a Devonian terrestrial choanate, still had internal gills (Coates and Clack, 1991), but no other terrestrial choanate is known to have had them. Therefore, internal gills were probably lost early in the evolution of terrestrial vertebrates, in the Devonian or the Mississippian (about 360 million years ago), and no tetrapod ever had internal gills.

Discussion of Phylogenetic Relationships

The phylogeny of terrestrial vertebrates is controversial. All systematists agree that extant amphibians form a monophyletic group (Lissamphibia) that is closely related to amniotes, but the origin of lissamphibians and amniotes is controversial. Laurin and Reisz (in press) suggest that lepospondyls are the stem-group of amphibians, and that diadectomorphs are more closely related to amniotes than to lissamphibians. Consequently, many groups of Paleozoic terrestrial vertebrates, such as temnospondyls and seymouriamorphs, are not closely related to amniotes or to lissamphibians:

     ====================== Ichthyostega
     |
     |  =================== Temnospondyli
     |  |
     |  |  ================ Loxommatidae
     |  |  |
     |  |  |  ============= Embolomeri
     |  |  |  |
=====|  |  |  |  ========== Seymouriamorpha
     ===|  |  |  |
        ===|  |  |     ==== Lissamphibia (frogs, salamanders, and caecilians)
           ===|  |  ===|
              ===|  |  |||| Lepospondyli
                 ===|
                    |  ==== Diadectomorpha
                    ===|
                       ==== Amniota (mammals, reptiles, and birds)

However, most previous studies have suggested that lissamphibians are derived from temnospondyls, and that diadectomorphs, seymouriamorphs, and embolomeres are more closely related to amniotes than to lissamphibians (Bolt, 1969; Gaffney, 1979; Gauthier et al., 1988, 1989; Milner, 1988, 1993; Panchen and Smithson, 1988; Trueb and Cloutier, 1991; Lombard and Sumida, 1992). Lepospondyls have often been viewed as a prarphyletic group that included early relatives of temnospondyls and lissamphibians. Therefore, most known terrestrial vertebrates were viewed as related to either lissamphibians or amniotes. Only Ichthyostega and other Devonian taxa (Acanthostega, Tulerpeton) were not believed to be on one of these two main evolutionary lineages:

     =================== Ichthyostega
     |
     |        ========== Lissamphibia (frogs, salamanders, and caecilians)
     |     ===|
     |  ===|  |||||||||| Temnospondyli
     |  |  |
     |  |  ||||||||||||| Lepospondyli
     |  |
=====|  |  ============= Loxommatidae
     ===|  |
        |  |  ========== Embolomeri
        |  |  |
        ===|  |  ======= Seymouriamorpha
           ===|  |
              ===|  ==== Diadectomorpha
                 ===|
                    ==== Amniota (mammals, reptiles, and birds)

Additional discussion and more detailed phylogenies can be found on the Phylogeny of Terrestrial Vertebrates page.

Origin of Terrestrial Vertebrates

Several scenarios have been proposed to explain why vertebrates ventured onto dry land. A theory found in most popular books is that the arid climate that was once thought to have prevailed in the Devonian had forced our sarcopterygian ancestors to crawl out of seasonally drying ponds to reach larger, deeper bodies of water (Romer, 1933). However, a problem with this scenario is that the Devonian is no longer viewed as having been seasonally dry. Furthermore, recent studies on functional morphology of fishes suggest that the limbs may have evolved to allow our early ancestors to walk at the bottom of shallow ponds or swamps (Edwards, 1989). Discovery of fairly complete specimens of the Devonian choanate Acanthostega (Coates and Clack, 1990) confirms that its limbs were poorly suited to walk on dry land (Zimmer, 1995). The inferred presence of internal gills in Acanthostega also confirms that this animal was still mainly aquatic (Coates and Clack, 1991). The transition from the aquatic to the terrestrial environment appears to have taken longer than previously thought.

Early Evolution of the Limbs

The presence of five fingers and toes has generally been believed to be primitive for tetrapods and to have been the highest number of digits that our early ancestors had. Five digits were probably present in the earliest tetrapods, but not in the earliest terrestrial vertebrates. Recent discoveries have demonstrated that the earliest terrestrial vertebrates had more digits; Acanthostega had eight fingers, Ichthyostega had seven toes, and Tulerpeton had six fingers (Lebedev, 1986; Gould, 1991). These "extra" digits were quickly lost, however, because no post-Devonian terrestrial vertebrate is known to have had more than five digits.

References

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          from the Lower Permian of Oklahoma. Science 166: 888-891.
Carroll, R. L.  1988. Vertebrate Paleontology and Evolution. 
          New York: W. H. Freeman and Company.
Carroll, R. L. 1995. Problems of the phylogenetic analysis of 
          Paleozoic choanates. Bulletin du Muséum national d'Histoire 
          naturelle de Paris 4ème série 17: 389-445.
Clack, J. A. 1994. Earliest known tetrapod braincase and the 
          evolution of the stapes and fenestra ovalis. Nature 
          369: 392-394.
Coates, M. I. & J. A. Clack. 1990. Polydactyly in the earliest 
          known tetrapod limbs. Nature 347: 66-69.
Coates, M. I. & J. A. Clack. 1991. Fish-like gills and breathing 
          in the earliest known tetrapod. Nature 352: 234-236.
Edwards, J. 1989. Two perspectives on the evolution of the tetrapod 
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Gaffney, E. S. 1979. Tetrapod monophyly: a phylogenetic analysis. 
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Gould, S. J. Eight (or fewer) little piggies.  Natural History, 
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Jarvik, E. 1952. On the fish-like tail in the ichthyostegid stegocephalians 
          with descriptions of a new stegocephalian and a new 
          crossopterygian from the Upper Devonian of East Greenland. 
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Laurin, M. & R. R. Reisz. In press. A new perspective on tetrapod 
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Milner, A. R. 1993. The Paleozoic relatives of lissamphibians. 
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          Reptiles, Birds:  1-32. Oxford: Clarendon Press.
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Smithson, T. R., R. L. Carroll, A. L. Panchen, & S. M. Andrews. 
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Zimmer, C., Coming onto the land. Discover,  June 1995, 118-127.

About this page

I wish to thank Mr. John Hutchinson, Ms. Patricia Lai, and Mr. Matthew Marlowe who edited this page. I am indebted to Dr. David Maddison who provided invaluable help in formatting this page, in linking it with other pages on the Tree of Life, and whose numerous suggestions improved the presentation of this page.

Michel Laurin
E-mail: michell@ucmp1.Berkeley.EDU.
Museum of Paleontology, University of California, Berkeley, CA 94720

Title Illustration

Terrestrial Vertebrates

Table of Contents

Introduction

Classification of Terrestrial Vertebrates

Characteristics of Terrestrial Vertebrates

Discussion of Phylogenetic Relationships

Origin of Terrestrial Vertebrates

Early Evolution of the Limbs

References

About this page

Title Illustration