The Evolutionary Transition To Mammals

The ancestors of mammals, Synapsida, diverged from basal amniotes—protothyrid captorhinomorphs—at least 300 million years ago, in the Pennsylvanian Period. As the oldest and most primitive amniotes, protothyrids were also ultimately ancestral to reptiles (including lizards, snakes, and turtles) and archosaurs (crocodilians, dinosaurs, and birds). Synapsids include two successive radiations, the Pennsylvanian-Permian Pelycosauria, and the largely Permo-Triassic Therapsida (see Carroll, 1988, for an excellent summary). Although synapsids were long classified as reptiles, it is now accepted that they shared a more recent ancestry with mammals. Therapsids arose in the Permian from sphenacodontid pelycosaurs (which include the carnivorous "sail-backed" Dimetrodon from Texas). The Cynodon-tia of the late Permian-Triassic were the most mammal-like therapsids.

Note that cladistically, mammals are, therefore, successively nested within synapsids, pelycosaurs, therapsids, and cynodonts. These names were long applied (in what is now regarded as a paraphyletic sense) only to nonmammalian Paleozoic and early Mesozoic representatives, excluding mammals (e.g., Romer, 1966; Carroll, 1988). For convenience, the names are used here in that sense, rather than modifying them with the term "nonmammalian" each time they are mentioned.

Through the Permian and Triassic, a succession of cyn-odonts progressively acquired mammal-like anatomy, including heterodont dentition, postcanine teeth with three longitudinally aligned cusps, a pair of occipital condyles, a secondary palate, differentiation in the vertebral series, confinement of ribs mainly to the thoracic region, modified limb girdles, better-defined limb joints, and less sprawling posture (Figs. 3.3, 3.4). Particularly important was progressive enlargement of the dentary at the expense of the post-dentary bones. Many of these features were already evident in the well-known Early Triassic cynodont Thrinaxodon ( Jenkins, 1971). As the dentary enlarged in some advanced cynodonts, it approached or came in contact posteriorly with the squamosal bone, creating a secondary jaw joint beside the old "reptilian" articular-quadrate joint. In Pro-bainognathus this secondary jaw joint was between the suran-gular and the squamosal (Figs. 3.4, 3.5), whereas in Diarthro-gnathus it was between the dentary and the squamosal. The bones of the "reptilian" jaw joint (articular and quadrate) were probably also involved in transmitting sound to the stapes and would eventually become the malleus and incus of the mammalian middle ear. Concomitantly the cheek teeth became more complex, and further modifications of the jaw and skull permitted reorientation of the jaw muscles. These changes led to more precise occlusion. The accumulation of these mammal-like features in cynodonts leaves little question that they were the progenitors of mammals. However, it has become increasingly clear that mammal-like specializations arose repeatedly among cyn-odonts, making the precise ancestry of Mammalia difficult to decipher.

The iterative evolution of mammalian characters in multiple lines of cynodonts led to the prevailing view during much of the twentieth century that mammals constitute a polyphyletic grade rather than a clade, a view strongly influenced by the work of George Gaylord Simpson, Everett C. Olson, and Bryan Patterson (see Luo et al., 2002). However, most authorities since about 1970 have concluded, as did Gregory (1910), that Mammalia (=Mammaliaformes of Rowe, 1988, and McKenna and Bell, 1997) is monophyletic

Sinoconodon Skeletal StructureThrinaxodon

2 cm

Fig. 3.4. Skulls of advanced cynodonts and a basal mammal: (A) cynodont Thrinaxodon; (B) cynodont Probainognathus; (C) Sinoconodon, a primitive mammal. Key: a, angular; ar, articular; d, dentary; eo, exoccipital; f, frontal; j, jugal; l, lacrimal; mx, maxilla; n, nasal; p, parietal; pm, premaxilla; po, postorbital; prf, prefrontal; q-qj, quadrate-quadratojugal; ref lam, reflected lamina; sa, surangular; sm, septomaxilla; sq, squamosal. (A, B from Hopson and Kitching, 2001; C from Crompton and Sun, 1985.)

2 cm

Fig. 3.4. Skulls of advanced cynodonts and a basal mammal: (A) cynodont Thrinaxodon; (B) cynodont Probainognathus; (C) Sinoconodon, a primitive mammal. Key: a, angular; ar, articular; d, dentary; eo, exoccipital; f, frontal; j, jugal; l, lacrimal; mx, maxilla; n, nasal; p, parietal; pm, premaxilla; po, postorbital; prf, prefrontal; q-qj, quadrate-quadratojugal; ref lam, reflected lamina; sa, surangular; sm, septomaxilla; sq, squamosal. (A, B from Hopson and Kitching, 2001; C from Crompton and Sun, 1985.)

(e.g., Hopson and Crompton, 1969; Crompton and Jenkins, 1973, 1979; Rougier et al., 1996a; Luo et al., 2002; Kielan-Jaworowska et al., 2004). But as late as the 1990s some distinguished researchers still hinted at the possibility that Mammalia as it is widely conceived could be polyphyletic (Lillegraven and Krusat, 1991; Kielan-Jaworowska, 1992).

Some advanced cynodonts, called gomphodonts, evolved broad, complex teeth—somewhat reminiscent of some mammalian teeth—in association with a herbivorous diet. Despite this apparent approach toward a mammalian dentition, gomphodonts were not particularly closely related to mammals. Most early mammals were very small and had sharp teeth indicative of an insectivorous habit, making it much more likely that they descended from carnivorous/ insectivorous cynodonts. Furthermore, some experts now are persuaded that the two families of gomphodonts (Tra-versodontidae and Diademodontidae) achieved their her-bivorously adapted dentitions in parallel.

Many authorities accept that the late Triassic-early Jurassic Tritheledontidae (also called ictidosaurs), including Diarthrognathus and Pachygenelus (Fig. 3.6), are the cynodonts most closely related to mammals (e.g., Hopson and Barghusen, 1986; Shubin et al., 1991; Crompton and Luo, 1993; Luo, 1994; Hopson and Kitching, 2001; Kielan-Jaworowska et al., 2004). Although this hypothesis was initially based primarily on the dentition, a recent comprehensive analysis including cranial and postcranial skeletal characters as well as the dentition also supports this interpretation (Luo et al., 2002). Tritheledonts were small cyn-odonts, some with skulls only a few centimeters long. The teeth of some types, such as Pachygenelus, are similar in size and morphology to those of morganucodontids (basal mammals; see Chapter 4) and, like the latter, have prismatic enamel (Gow, 1980). However, the dental formula and details of the dental anatomy and enamel microstructure suggest that known tritheledonts cannot be directly ancestral to mammals. According to Bonaparte and Barberena (2001), postcranial and dental features suggest that the cynodonts Therioherpeton and Prozostrodon, both from the Upper Trias-sic of Brazil, are also closely related to mammals, although not as closely as tritheledonts.

Alternatively, Tritylodontidae, once considered mammals because of dental and general cranial resemblances to multituberculates, have also been championed as the sister-group of mammals (Fig. 3.7). Although some authorities (e.g., Sues, 1985) have argued that they are more closely related to gomphodont cynodonts, numerous synapomor-phies seem to support a close alliance between tritylodonts and mammals (Kemp, 1983; Wible, 1991; Rowe, 1993; Martinez et al., 1996). These include such features as cheek teeth with multiple roots, absence of prefrontal and postorbital bones, a partially floored cavum epiptericum (the fossa for the trigeminal nerve ganglion), postdentary bones that are similar to the auditory ossicles of primitive mammals, and many other cranial characters (e.g., Sues, 1986), as well as an odontoid process (dens) on the axis vertebra, details of shoulder and pelvic structure, and the presence of an as-tragalar canal. As in tritheledonts and basal mammals, the postdentary jaw bones are reduced relative to their state in other cynodonts. However, tritylodonts have a primitive quadrate-articular jaw joint and enlarged incisors separated by diastemata from the complex cheek teeth—a specialized, rodentlike pattern. These features exclude known forms from direct mammalian ancestry and raise the possibility that some of the mammalian traits of tritylodonts arose independently.

Hahn et al. (1994) proposed that the Upper Triassic Dro-matheriidae (in which they included the South American Therioherpeton and several other genera whose phylo-genetic positions previously were ambiguous) were even closer to mammals, suggesting that these animals occupied a transitional zone between cynodonts and mammals. Like trithelodonts, tritylodonts, and mammals, dromatheriids (where known) lack prefrontal and postorbital bones in the skull. The teeth have a single row of laterally compressed

Fig. 3.5. Skull of Probainognathus, showing enlarged dentary (d) approaching the squamosal (sq) and bringing the surangular (sa) into contact with the squamosal. A quadrate (q)-articular (a) jaw joint was also present. (From Romer, 1970.)

Jaw Joint Carnivorous

Fig. 3.5. Skull of Probainognathus, showing enlarged dentary (d) approaching the squamosal (sq) and bringing the surangular (sa) into contact with the squamosal. A quadrate (q)-articular (a) jaw joint was also present. (From Romer, 1970.)

cusps (typically three principal cusps), recalling those of tritheledonts and morganucodontids (Fig. 3.8). Premolar and molar morphologies can be distinguished, but the teeth lack cingula, and their roots are incompletely divided. Most of the genera are represented only by isolated teeth; hence their precise phylogenetic position (and even whether they are closely related to each other) is in dispute (e.g., Sues, 2001). Nonetheless, the current consensus is that they are not particularly closely related to mammals.

Bonaparte et al. (2003) recently described two new genera of small, advanced cynodonts (Brasilodon and Brasili-therium) from the Late Triassic of Brazil that may be closer to the ancestry of mammals than any other forms yet found. Both are known from skulls, which lack the prefrontal and postorbital bones, and Brasilitherium has morganucodontid-like lower teeth. Their phylogenetic analysis placed these genera closer to Morganucodon than are either tritheledonts or tritylodonts.

Kemp (2005) recently provided an excellent summary of the evidence for a relationship between various cynodonts and mammals. He postulated that the choice (and probable lack of independence) of anatomical characters used in various phylogenetic analyses may explain why a consensus on the sister-group of mammals has eluded researchers.

Prozostrodon

Fig. 3.6. Lower jaws of advanced cynodonts: (A) Thrinaxodon; (B) Prozostrodon; (C) Diarthrognathus; (D) Pachygenelus. Key: ANG, angular; ang., angle of dentary; ART, articular; CO, coronoid; D, dentary; FPB, fossa for postdentary bones; m. for., mandibular foramen; PA, prearticular; PAP, prearticular process; RPC, replacing postcanine; SPL, splenial; SUR, surangular. (A from Crompton and Parker, 1978; B from Bonaparte and Barberena, 2001; C from Crompton, 1963; D from Crompton and Luo, 1993.)

Fig. 3.6. Lower jaws of advanced cynodonts: (A) Thrinaxodon; (B) Prozostrodon; (C) Diarthrognathus; (D) Pachygenelus. Key: ANG, angular; ang., angle of dentary; ART, articular; CO, coronoid; D, dentary; FPB, fossa for postdentary bones; m. for., mandibular foramen; PA, prearticular; PAP, prearticular process; RPC, replacing postcanine; SPL, splenial; SUR, surangular. (A from Crompton and Parker, 1978; B from Bonaparte and Barberena, 2001; C from Crompton, 1963; D from Crompton and Luo, 1993.)

Fig. 3.8. Dromatheriid lower teeth: (A) Pseudotriconodon; (B) Dromatherium; (C) Microconodon; (D) Tricuspes; (E) Therioherpeton; (F) Meurthodon; (G) Tricuspes (lower and upper teeth). Letters in A-F designate cusps. Scale applies to G. (From Hahn et al., 1994.)

Therioherpeton Fossil

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