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The Evolution of Growth Patterns in Mammalian Versus Nonmammalian Cynodonts

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The Evolution of Growth Patterns in Mammalian Versus Nonmammalian Cynodonts Paleobiology, 42(3), 2016, pp. 439–464 DOI: 10.1017/pab.2015.51 The evolution of growth patterns in mammalian versus nonmammalian cynodonts Rachel N. O’Meara and Robert J. Asher Abstract.—One of the major evolutionary transitions of the mammaliaform lineage was the origin of a typically mammalian pattern of growth. This is characterized by rapid juvenile growth followed by abrupt cessation of growth at adult size and may be linked with other important mammaliaform apomorphies of dental replacement and morphology. Investigation of growth patterns in the tritylodontid cynodont Oligokyphus and the basal mammaliaform Morganucodon provides insight into this crucial transition. We collected mandibular depth measurements from large samples of Morganucodon and Oligokyphus and constructed distributions of mandibular depth versus frequency for each species. These were compared with distributions from species from three different growth classes of extant amniote: testudines + crocodilians, mammals + birds, and lepidosaurs. Discriminant function analysis was used to differentiate between known growth classes by using different combinations of three measures of mandibular depth distribution shape (skew, kurtosis, and coefficient of variation) as proxies for different juvenile and adult growth patterns. Classification of the fossil species showed that Morganucodon closely resembled extant placental mammals in having rapid juvenile growth followed by truncated, determinate adult growth. Oligokyphus showed intermediate growth patterns, with more extended adult growth patterns than Morganucodon and slightly slower juvenile growth. This suggests a gradual evolution of mammalian growth patterns across the cynodont to mammaliaform transition, possibly with the origin of rapid juvenile growth preceding that of truncated, determinate adult growth. In turn, acquisition of both these aspects of mammalian growth was likely necessary for the evolution of diphyodont tooth replacement in the mammaliaform lineage. Rachel N. O’Meara and Robert J. Asher. University Museum of Zoology, Downing Street, Cambridge, CB2 3EJ, United Kingdom. E-mail: [email protected] Accepted: 12 November 2015 Published online: 28 April 2016 Supplemental material deposited at Dryad: doi: 10.5061/dryad.8rv01 Introduction determinate (or “truncated” in contrast to Once erupted, teeth cannot increase in size “extended”) skull growth in mammals may (although some species, including rodents, limit the requirement for continuous tooth have open-rooted dentitions and show contin- replacement (Crompton and Jenkins 1973; uous eruption). Therefore, continuous growth Zhang et al. 1998; Luo et al. 2004). This is of the jaw requires that teeth are succeeded by supported by observations in mammals that larger replacement teeth or that additional most postnatal cranial growth (up to 80%) teeth are added to the tooth row to maintain a occurs before deciduous eruption is complete functional dentition (Edmund 1960; Osborn (Crompton and Parker 1978) and that after the 1974). Hence, in many amniotes with “indeter- deciduous dentition has erupted relatively minate” growth patterns in which growth little further growth of the jaw is required to continues for most of the animal’s life span accommodate the replacement permanent den- (here referred to as “extended” adult growth) tition and new permanent molars (Pond 1977; such as crocodilians, some dinosaurs, and Crompton and Parker 1978). Rapid juvenile some nonmammalian cynodonts, polyphyo- growth, particularly of the skull, in mammals dont replacement of larger teeth has been limits the time during which teeth of inter- linked with continuous jaw growth (Edmund mediate size are required and hence also 1960; Hopson 1971; Osborn 1971; Osborn and permits the reduction of tooth replacement Crompton 1973; Westergaard and Ferguson (Pond 1977; Zhang et al. 1998). Therefore, both 1986, 1987; Butler 1995). In contrast, determinate, truncated adult growth and rapid © 2016 The Paleontological Society. All rights reserved. 0094-8373/16 Downloaded from https://www.cambridge.org/core. Pendlebury Library of Music, on 14 Sep 2017 at 12:50:04, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2015.51 440 RACHEL N. O’MEARA AND ROBERT J. ASHER juvenile growth are correlated with, and may et al. 2002; Kielan-Jaworowska et al. 2004). have permitted the evolution of, diphyodonty. Antemolars in Morganucodon were replaced Maternal provisioning by lactation may also only once, and molars were probably unre- be linked with the evolution of diphyodonty placed in both M. watsoni and M. oehleri (Mills (Ewer 1963; Hopson 1971, 1973; Zhang et al. 1971; Parrington 1971, 1973, 1978; Kermack and 1998; Kielan-Jaworowska et al. 2004) since Kermack 1984; Luo 1994; Crompton and Luo (1) maternal provisioning results in rapid 1993), although further evidence is required to juvenile growth, particularly of the skull show that the ultimate molar was unreplaced relative to the postcranium (Pond 1977), and (Luo et al. 2004). Similarly, molar replacement (2) functional teeth are not required until a has not been observed in the morganucodontan neonate mammal is weaned, so eruption of the Dinnetherium (Crompton and Luo 1993; Luo first generation of teeth is delayed in mammals 1994), leading Luo et al. (2004) to suggest that relative to diapsids (Ewer 1963; Hopson 1971; mammal-like diphyodont tooth replacement Pond 1977). Thus, the jaw usually reaches a may be common to all morganucodontans. greater proportion of adult size at the time of The docodont Haldanodon is also diphyodont eruption of the first generation of teeth in and lacks molar replacement (Martin and mammals compared with diapsids, further Nowotny 2000; Nowotny et al. 2001). The limiting the requirement for polyphyodonty diphyodont condition is widely considered an in the former (Ewer 1963; Pond 1977). Varia- apomorphy of the clade comprising the last bility may of course occur, but usually entails common ancestor of morganucodontans and growth preceding eruption (Asher and crown Mammalia and its descendants (Luo Lehmann 2008; Asher and Olbricht 2009; 1994; Kielan-Jaworowska et al. 2004; Luo et al. Ciancio et al. 2012), rather than eruption 2004), although some gobiconodontids do show preceding growth, for obvious mechanical replacement of at least anterior molariforms requirements of having space in the jaw into (Jenkins and Schaff 1988; Kielan-Jaworowska which teeth may erupt (although in some and Dashzeveg 1998), which may complicate species the relationship between size and this interpretation. eruption is not straightforward; cf. Godfrey Given the theoretical links between diphyo- et al. 2005). Lactation, diphyodonty, rapid donty and mammalian growth patterns, Luo juvenile growth, and determinate growth et al. (2004) hypothesized that Morganucodon may in turn be linked with several other experienced determinate (truncated) growth important mammalian morphological and and rapid juvenile growth and, by implication, behavioral apomorphies. These include may have provisioned its young by lactation. increased precision of molar occlusion Evidence for determinate growth is based on (Crompton and Jenkins 1973; Pond 1977; the narrow range of skull lengths in M. oehleri Crompton 1995); the increased complexity of (Luo et al. 2001, 2004; Kielan-Jaworowska et al. enamel microstructure and evolution of 2004). This range is much more restricted than enamel prisms, which may prevent propaga- that of the basal mammaliaform Sinoconodon, tion of cracks and hence reduce wear (Grine which did not have diphyodont tooth replace- and Vrba 1980; Crompton et al. 1994); ment (Zhang et al. 1998). Hence, M. oehleri was mammalian jaw-closing mechanisms (Cromp- inferred to have had a more mammal-like ton and Jenkins 1973; Pond 1977; Crompton growth pattern than Sinoconodon, and perhaps and Parker 1978; Crompton 1995); and mutua- also nonmammalian cynodonts, although listic social behavior (Pond 1977). comparable studies have not been carried out Dating from the Late Triassic–Early Jurassic, in more basal cynodont species. Morganucodon is the geologically oldest mam- Rapid juvenile growth in Morganucodon has maliaform (defined following Rowe [1998] as also been inferred from the high proportion of the clade comprising the last common ancestor adult to juvenile specimens in M. watsoni of Sinoconodon and crown Mammalia, and its (Parrington 1971, 1978; Kermack et al. 1973, descendants) and the most cladistically basal to 1981; Gow 1985; Luo 1994), suggesting that the have had diphyodont tooth replacement (Luo juvenile stage was of short duration relative Downloaded from https://www.cambridge.org/core. Pendlebury Library of Music, on 14 Sep 2017 at 12:50:04, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2015.51 EVOLUTION OF MAMMALIAN GROWTH PATTERNS 441 to overall life span in this genus (Gow 1985; abruptly terminating growth of mammals and Luo et al. 2004). In addition, bone histology lepidosaurs as “determinate” or “truncated” supports the hypothesis of mammal-like adult growth and the less strongly plateaued growth patterns in Morganucodon; the high growth of testudines and crocodilians (Fig. 1) bone-deposition rates in early ontogeny, as “extended adult growth.” followed by a reduction in the rate of bone Evidence from tooth replacement studies formation in M. watsoni, are similar to those suggests that many
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