Articles

Print Email

Deciduous dentition and dental eruption of Hyainailouroidea (Hyaenodonta, “Creodonta,” Placentalia, Mammalia)

Matthew R. Borths and Nancy J. Stevens

Plain Language Abstract

Although many vertebrate animals replace their teeth multiple times throughout a lifetime, mammals are typically restricted to two sets of teeth: the deciduous teeth that erupt first and the adult dentition that eventually replaces them. Most paleontological studies of meat-eating mammals focus on the adult dentition, hence less information exists on the importance of the deciduous teeth for many mammal groups. In this paper, we describe the deciduous teeth for six species from a group of African meat-eating mammals, the hyainailouroids, which lived from at least 62 to 15 million years ago. We discovered these animals retained their deciduous teeth relatively late in life, and the deciduous teeth actually preserve features that are helpful in understanding the evolutionary history of the group. We also examined the order in which the deciduous teeth were eventually replaced, and explored how these teeth may hold important information for understanding why this group went extinct and were replaced by true carnivores like dogs, cats, and hyenas.

Resumen en Español

Dentición decidua y erupción dental de Hyainailouroidea (Hyaenodonta, "Creodonta", Placentalia, Mammalia)

La morfología dental decidua y la secuencia de la erupción dental permanente ofrecen perspectivas evolutivas y filogenéticas sobre la evolución de los mamíferos. La historia evolutiva temprana de Hyaenodonta, un clado morfológicamente diverso y biogeográficamente extendido de mamíferos carnívoros conocidos del Paleógeno y el Neógeno temprano, solo ha sido examinada de cerca para un género: Hyaenodon. Aquí describimos la morfología dental decidua para seis Hyainailouroidea, un clado lejanamente relacionado con Hyaenodon que dominó los primeros nichos Afro-arábicos del Cenozoico durante casi 20 millones de años. Los resultados sugieren una variación significativa entre Hyainailouroidea en la expresión de los protoconos, paraconos y metaconos de dP3 y dP4, y en la expresión del paracónido, metacónido y talónido de dP3 y dP4. Los caracteres dentales deciduos se incorporaron en un análisis filogenético bayesiano. La topología fue congruente con los análisis sistemáticos anteriores de la evolución de Hyaenodontidae, lo que sugiere que las características dentales deciduas pueden ser filogenéticamente informativas y que los taxones conocidos solo a partir de dientes deciduos se pueden incorporar en los estudios sobre la sistemática de mamíferos. A partir de los ejemplares descritos aquí, se reconstruye la secuencia de erupción dental de Hyainailouroidea. P4 y P3 entran en erupción después de M3, evidencia de que el complejo carnoso deciduo formado entre dP3 y dP4 se retuvo hasta el final del desarrollo, lo que permitió a los Hyaenodontidae desgastar fuertemente las áreas de corte en estos dientes antes del reemplazo. Esto difiere de Carnivora, un grupo que tiende a reemplazar la dentición decidua más temprano en el desarrollo, limitando a los carnívoros de forma notoria a un solo grupo de carniceras durante la mayor parte de su vida. Esta diferencia de desarrollo entre carnívoros y Hyaenodontidae ahora puede examinarse en un contexto sistemático y ecológico más amplio.

Palabras clave: Ontogenia; Dieta carnívora; Egipto; África; Paleógeno.

Traducción: Enrique Peñalver (Sociedad Española de Paleontología) 

Résumé en Français

in progress

Translator: Antoine Souron

Deutsche Zusammenfassung

Milchbezahnung und Zahneruption bei Hyainailouroidea (Hyaenodonta, “Creodonta,” Placentalia, Mammalia)

Die Morphologie der Milchzähne und die Zahneruptionssequenz bieten uns entwicklungsbezogene phylogenetische Einsichten in die Evolution der Säugetiere. Die frühe Entwicklungsgeschichte der Hyaenodonta, einer morphologisch diversen und biogeographisch weit verbreiteten Klade von karnivoren Säugetieren aus dem Paläogen und frühen Neogen wurde nur bei der Gattung Hyaenodon eingehend untersucht. Hier beschreiben wir die Morphologie der Milchzähne für sechs Hyainailouroiden, einer Klade von Hyaenodonten, die weitläufig mit Hyaenodon verwandt sind und die die frühkänozoischen Fleischfresser-Nischen von Afro-Arabien für beinahe 20 Millionen Jahre dominierten. Die Ergebnisse weisen auf signifikante Unterschiede zwischen den Hyainailouroiden hin, was die Ausprägung des dP3 und dP4 Protoconus, Paraconus und Metaconus angeht und die des dP3 and dP4 Paraconid, Metaconid und Talonids. Die Merkmale des Milchgebisses wurden in eine Bayesianische Phylogenetische Analyse eingegeben. Die Topologie stimmte mit früheren systematischen Untersuchungen über die hyaenodonte Evolution überein, was zeigt, dass Merkmale des Milchgebisses phylogenetisch aussagekräftig sein können und dass Taxa, die nur durch Milchzähne bekannt sind, durchaus in Untersuchungen über Saugetiersystematik miteinbezogen werden können. Basierend auf dem hier beschriebenen Stück wird die Eruptionssequenz der Hyainailouroidea rekonstruiert. P4 and P3 brechen nach M3 durch, was darauf hindeutet, dass die Reißzähne des Milchgebisses zwischen dP3 and dP4 bis spät in der Entwicklung erhalten blieben, was es den Hyaenodonten erlaubte vor dem Zahnwechsel starke Schneidekanten auf diesen Zähnen zu tragen. Dies unterscheidet sich von den Carnivora, einer Gruppe die dazu tendiert die Milchbezahnung früher in der Entwicklung zu wechseln, was die Karnivora effektiv auf ein einziges Paar Reißzähne in ihrem Leben einschränkt. Dieser Unterschied in der Entwicklung von Karnivora und Hyaenodonten kann nun in einem größeren systematischen und ökologischen Zusammenhang untersucht werden.

Schlüsselwörter: Ontogenie; Karnivorie; Ägypten; Afrika; Paläogen.

Translator: Eva Gebauer

Arabic

Translator: Ashraf M.T. Elewa

 

 

TABLE 1. Measurements of the upper dentition. Asterisk indicates the measurements are based on the alveoli of the tooth. Length is mesiodistal length. Width is buccolingual length. ~, indicates an approximate measurement based on fragmentary material. See methods for definitions of these measurements.

Taxon Specimen Tooth Length Width
Apterodon macrognathus DPC 4126 dP3* 10.8 4.9
    dP4 15.6 9.0
Leakitherium hiwegi KNM-RU 2949 dP3 15.4 10.8
    dP4 16.7 13.4
Leakitherium hiwegi KNM-RU 15182 dP3 15.2 14.0
    dP4 ~16.5 17.5
Anasinopa leakeyi KNM-RU 2385 dP2 9.0 3.7
    dP3 9.6 6.7
    dP4 10.2 9.2
Dissopsalis pyroclasticus KNM-FT 3357 dP3 15.4 9.2
    dP4 15.6 13.4
    M1* 15.5 16.0
Masrasector nananubis DPC 20882 dP3 4.8 ~3.0
    dP4 4.4 2.7
Masrasector nananubis DPC 13837 dP3 5.0 3.0
    dP4 5.0 3.4
    M1 5.7 4.5
Metasinopa sp. DPC 10199 dP3 10.5 5.1
    dP4 10.9 7.1
    M1 12.5 11.7

 

TABLE 2. Measurements of the lower dentition. Asterisk indicates the measurements are based on the alveoli of the tooth. Length is mesiodistal length. Width is buccolingual length. ~, indicates an approximate measurement based on fragmentary material. See methods for definitions of these measurements.

Taxon Specimen Tooth Length Width
Apterodon macrognathus DPC 8217 dP3 11.7 3.8
    dP4 15.7 4.9
    M1 14.0 6.5
Anasinopa libyca BMNH M82378 dP3 9.9 2.2
    dP4 11.7 3.6
Masrasector nananubis DPC 10358 dP3 5.2 1.6
    dP4 5.0 2.2
    M1 4.7 2.6
    M2 5.6 3.3
Masrasector nananubis DPC 18276 dP2 3.9 1.5
    dP3 5.1 1.6
    dP4 4.7 1.8
Metasinopa sp. DPC 4544 P2 9.2 2.4
    dP3* 12.0 2.6
    dP4* 10.4 3.0
    M1 10.6 4.7
    M2 12.6 5.2
    M3 ~13.82 4.3

 

TABLE 3. Dental eruption sequences of Hyaenodonta and Ferae. Upper and lower eruption sequences are separated for this study because no hyainailouroid specimen directly reveals the relationship between the timing of eruption in the upper and lower dentition. Sequence reads from left to right with m-dashes identifying subsequent events. Tooth positions contained in parentheses are unknown. Tooth positions with an asterisk are variable within the group. Note that taxa listed in “Group” are not all the same taxonomic level.

Group Eruption of Upper dentition Eruption of lower dentition Reference
Hyainailouroidea synthesis M1-M2- M3-P4 or P3 (P2, C) M1-M2-P-P3-M3-P4-C This study
Apterodon macrognathus   M1-M2 This study
Masrasector nananubis M1-?-?-P3-P4 M1-M2-P2-P3-M3-P4-C This study
Metasinopa   M1-M2-P2-P3-M3-P4-C This study
Brychotherium ephalmos M1-M2-M3-P4   This study
Leakitherium hiwegi ?P4-P3   This study
North American Hyaenodon M1-I- P2-P4-M 2-P3-C M1-M2-I-P2-P4-M3-P3-C Bastl and Nagel, 2013
European Hyaenodon M 1-P1-I- P2-P 4-M2-P3-C M1-P1-M2-I-P2-C, P3, M3-P4 Bastl and Nagel, 2013
Lesmesodon I-P1-M1-M2-C- P 2 I-P1-M1-M2-C-P2 Morlo and Habersetzer, 1999
Oxyaena woutersi   M1-P4-P2-P 3 (M2) Solé et al., 2011
Didymictis protenus M1-P2 /P3 /P4 P2 /M1 /M2-P3 /P4 Zack, 2012
Viverridae M1-P4-P2 *- P3-M2* M1-M2-P2 *-P3-P4 Slaughter et al., 1974
Felidae P2 / M1-P4-P3 M 1-P 4-P 3 Slaughter et al., 1974
Mustelidae M1-P4-P2-P3 M1-M2-P2*-P3-P4 Slaughter et al., 1974
Canidae M1-M2-P4-P2-P3 M1 /M 2-M3*-P2*-P4-P3 Slaughter et al., 1974

 

 

FIGURE 1. Apterodon macrognathus left maxilla fragment with dP4 and alveoli of dP3 (DPC 4126) from Quarry M (early Oligocene) in the Fayum Depression, Egypt in 1) occlusal view; 2) buccal view; and 3) lingual view. Scale bar is 10 mm.

figure 1jpg 

FIGURE 2. Apterodon macrognathus left dentary with dP3, dP4, M1 and M2 in crypt (DPC 8217) from Quarry M (early Oligocene) in the Fayum Depression, Egypt. Original specimen figured with digital model based on µ-CT scans reconstructed in Avizo. Mandibular corpus rendered transparent to reveal developing dentition. Grey, deciduous dentition. Yellow, permanent dentition. 1) Specimen occlusal view; 2) model occlusal view; 3) specimen lingual view; 4) model lingual view; 5) specimen buccal view; 6) model buccal view. Scale bar is 10 mm.

figure 2 

FIGURE 3. Leakitherium hiwegi maxilla fragments from Rusinga Island (early Miocene), Kenya. KNM-RU 2949 (CMF 4025 in Savage, 1965) is a left maxilla fragment dP3 and dP4 shown in 1) occlusal view; 2) buccal view; and 3) lingual view. KNM-RU 15182 is a right maxilla fragment with dP3 and dP4 and the germ of P4 shown in 4) occlusal view; 5) buccal view; 6) lingual view; 7) dorsal view; 8) and distal view. The well-developed germ of P4 is best viewed in dorsal and distal view. Specimens are to scale and scale bar is 10 mm.

 figure 3

FIGURE 4. Anasinopa leakeyi left maxilla cast with dP2, dP3 and dP4 (KNM-RU 2385) from Rusinga Island (early Miocene), Kenya in 1) occlusal view; 2) buccal view; and 3) lingual view. Scale bar is 10 mm.

figure 4 

FIGURE 5. Anasinopa libyca left dentary with dP3 and dP4 from Gebel Zelten (middle Miocene), Libya (BMNH M82378) in 1) occlusal view; 2) lingual view; 3) buccal view. Scale bar is 10 mm.

 figure 5

FIGURE 6. Dissopsalis pyroclasticus left maxilla with dP3 and dP4 (KNM-FT 3357) from Fort Ternan (early Miocene), Kenya in 1) occlusal view; 2) buccal view; and 3) lingual view. Scale bar is 10 mm.

figure 6 

FIGURE 7. Masrasector nananubis left maxillae from Locality 41 (latest Eocene), Fayum Depression, Egypt. Original specimens figured with digital models based on µ-CT scans reconstructed in Avizo. Maxilla rendered transparent to reveal developing dentition. Grey, deciduous dentition. Yellow, permanent dentition. DPC 20882 is a left maxilla fragment that preserves dP3 and dP4 and no indication of developing permanent dentition. 1) specimen occlusal view; 2) model occlusal view; 3) specimen buccal view; 4) model buccal view; 5) specimen lingual view; 6) model lingual view. DPC 13837 is a left maxilla fragment that preserves erupted dP3, dP4, and M1 and P3 and P4 developing in crypts. 7) specimen occlusal view; 8) model occlusal view; 9) specimen buccal view; 10) model buccal view; 11) specimen lingual view; 12) model lingual view. Scale bar is 10 mm.

 figure 7

FIGURE 8. Masrasector nananubis right dentary with erupted dC, dP2, dP3, and dP4, M1 alveoli and P2, P3, and M2 in crypts (DPC 18276) from Locality 41 (latest Eocene), Fayum Depression, Egypt. Original specimen figured with digital model based on µ-CT scans reconstructed in Avizo. Dentary rendered transparent to reveal developing dentition. Grey, deciduous dentition. Yellow, permanent dentition. 1) specimen occlusal view; 2) model occlusal view; 3) specimen lingual view; 4) model lingual view; 5) specimen buccal view; 6) model buccal view. Scale bar is 10 mm.

 figure 8

FIGURE 9. Masrasector nananubis left dentary with erupted dP3, dP4, M1 and M2 and P2, P3, and M3 in crypts (DPC 10358) from Locality 41 (latest Eocene), Fayum Depression, Egypt. Original specimen figured with digital model based on µ-CT scans reconstructed in Avizo. Dentary rendered transparent to reveal developing dentition. Grey, deciduous dentition. Yellow, permanent dentition. 1) specimen occlusal view; 2) model occlusal view; 3) specimen lingual view; 4) model lingual view; 5) specimen buccal view; 6) model buccal view. Scale bar is 10 mm.

 figure 9

FIGURE 10. Metasinopa sp. left maxilla fragments with dP3, dP4, and M1 (DPC 10199) from Quarry V (early Oligocene), Fayum Depression, Egypt in 1) occlusal view; 2) buccal view; and 3) lingual view. Note that there is matrix around the roots of the specimens that has been cropped to make the dentition easier to view. Scale bar is 10 mm.

figure 10 

FIGURE 11. Metasinopa sp. right dentary with dC, dP4, M1, M2 and I, C, P2, P3, P4 M3 in crypts (DPC 4544) from Quarry V (early Oligocene), Fayum Depression, Egypt. Original specimen figured with digital model based on µ-CT scans reconstructed in Avizo. Dentary rendered transparent to reveal developing dentition. Grey, deciduous dentition. Yellow, permanent dentition. 1) specimen occlusal view; 2) model occlusal view; 3) specimen lingual view; 4) model lingual view; 5) specimen buccal view; and 6) model buccal view. Scale bar is 10 mm.

figure 11 

FIGURE 12. Results of the phylogenetic analysis of Hyaenodonta character-taxon matrix including deciduous dental characters. Results are visualized as an “allcompat” (majority rule plus compatible groups) consensus tree. Posterior probabilities (PP) are placed over each node. Bold taxa are scored for deciduous dental characters. Major, named clades recovered or discussed in this analysis and recovered in other analyses are illustrated.

 figure 12

 

APPENDIX 1.

Character-taxon matrix used in this study, formatted for the program Mesquite (mesquiteproject.org). (For zipped file of all Appendix PDFs, click here.)

APPENDIX 2.

Descriptions of the characters used in this analysis with the source of the character or comparable characters from other analyses. (For zipped file of all Appendix PDFs, click here.)

APPENDIX 3.

List of all the taxa and specimens used in this analysis, along with information on age and locality data. (For zipped file of all Appendix PDFs, click here.)

APPENDIX 4.

Input file for the Bayesian phylogenetic analysis, formatted for MrBayes (mrbayes.sourceforge.net). (For zipped file of all Appendix PDFs, click here.)

APPENDIX 5.

Consensus “allcompat” (majority-rule plus compatible groups) tree from Bayesian phylogenetic analysis. (For zipped file of all Appendix PDFs, click here.)

 

borthsMatthew R. Borths. Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, Athens, Ohio 45701, USA; Center for Ecology and Evolutionary Studies, Ohio University, Athens, Ohio 45701, USA. This email address is being protected from spambots. You need JavaScript enabled to view it.

Mathew Borths is a paleontologist whose research focuses on the evolution of carnivorous mammals, particularly hyaenodonts and carnivorans in Africa. Currently he is a U.S. National Science Foundation Postdoctoral Research Fellow in Biology at Ohio University in the Department of Biomedical Sciences. He is the co-creator of Past Time , a project that uses a podcast, blog, social media, and virtual classroom visits to to teach non-specialists about the scientific process.

divider

stevensNancy J. Stevens. Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, Athens, Ohio 45701, USA; Center for Ecology and Evolutionary Studies, Ohio University, Athens, Ohio 45701, USA. This email address is being protected from spambots. You need JavaScript enabled to view it.

Nancy Stevens is an integrative biologist exploring interactions between organisms and environments through time. She has conducted field research in over a dozen countries, documenting several discoveries new to science, including the oldest fossil evidence of the split between Old World monkeys and apes. Stevens investigates impacts of environmental change through deep time by exploring patterns of biogeography and extinction in the Cenozoic fossil record, particularly in the East African Rift, and she co-leads the Rukwa Rift Basin Project. Stevens also conducts field studies to explore links between form, function and extinction dynamics in modern animals in habitats that are rapidly changing due to anthropogenic and natural environmental change.