Biomechanical correlates of zygomaxillary-surface shape in papionin primates and the effects of hard-object feeding on mangabey facial form

Michelle Singleton; Daniel E. Ehrlich; Justin W. Adams

doi:10.1016/j.jhevol.2021.103121

Biomechanical correlates of zygomaxillary-surface shape in papionin primates and the effects of hard-object feeding on mangabey facial form

Michelle Singleton, Daniel E. Ehrlich, Justin W. Adams

Institute for Social Research & Data Innovation

Research output: Contribution to journal › Article › peer-review

Abstract

Extant African papioninans are distinguished from macaques by the presence of excavated facial fossae; however, facial excavation differs among taxa. Mangabeys (Cercocebus, Rungwecebus, and Lophocebus) exhibit fossae that invade the zygomatic forming pronounced suborbital fossae (SOFs). Larger-bodied Papio, Mandrillus, and Theropithecus have lateral rostral fossae with minimal/absent suborbital fossae. Because prior studies have shown that mangabeys exhibit adaptations to anterior dental loading (e.g., palatal retraction), it is plausible that mangabey SOFs represent structural accommodation to masticatory-system shape rather than facial allometry, as commonly hypothesized. We analyzed covariation between zygomaxillary-surface shape, masticatory-system shape, and facial size in 141 adult crania of Macaca fascicularis, Papio kindae, Cercocebus, and Lophocebus. These taxa represent the range of papionin SOF expression while minimizing size variation (narrow allometry). Masticatory-system landmarks (39) registered palate shape, bite points, masticatory muscle attachments, and the temporomandibular joint. Semilandmarks (450) captured zygomaxillary-surface shape. Following Procrustes superimposition with semilandmark sliding and principal components analyses, multivariate regression was used to explore allometry, and two-block partial least-squares analyses (within-configuration and separate-blocks) were used to examine covariation patterns. Scores on principal components 1–2 and the first partial least-square (PLS1) separate mangabeys from Macaca and Papio. Both zygomaxillary-surface shape and masticatory-system shape are correlated with size within taxa and facial morphotypes; however, regression distributions indicate morphotype shape differences are non-allometric. PLS1 accounts for ∼95% of shape covariance (p < 0.0001) and shows strong linear correlations (r-PLS = ∼0.95, p < 0.0001) between blocks. Negative PLS1 scores in mangabeys reflect deep excavation of the suborbital malar surface, palatal retraction, and anterior displacement of jaw adductor muscles and the temporomandibular joint. Neither PC1 nor PLS1 scores ordinate specimens by facial size. Taken together, these results fail to support the allometric hypothesis but suggest that mangabey zygomaxillary morphology is closely linked with adaptations to hard-object feeding.

Original language	English (US)
Article number	103121
Journal	Journal of Human Evolution
Volume	163
DOIs	https://doi.org/10.1016/j.jhevol.2021.103121
State	Published - Feb 2022

Bibliographical note

Funding Information:
This study is dedicated to the memory of Dennis E. Slice, whose contributions to the discipline of geometric morphometrics were matched only by his generosity and collegiality. For specimen access and curatorial assistance, we thank L. Heaney, A. Ferguson, W. Stanley, and R. Banasiak (Field Museum of Natural History); D. Lundey and E. Langan (National Museum of Natural History—Smithsonian Institution); K. McNulty, M. Tappan, and J. Soderbergh (Department of Anthropology, University of Minnesota—Twin Cities); W.S. McGraw (Department of Anthropology, The Ohio State University); R. Portela Miquez and P. Jenkins (Natural History Museum—London); B. Mahala and S. van der Merwe (Amathole Museum—Qonce); and T. Rae (University of Roehampton). Logistical support was provided by NYCEP, the Field Museum of Natural History, and the Department of Anthropology, University of Illinois–Urbana-Champaign. For data collection and technical assistance, we thank past Midwestern University staff members A. Martiny, B. Seitelman, and J. Krecioch and student researchers A. Schraber, C. Malzenski, and D. Polito. Clément Zanolli and four anonymous reviewers provided constructive comments that improved this manuscript. This study is NYCEP Morphometrics Contribution #115. This research was supported by the Australian Research Council ( DP170100056 ), The Leakey Foundation , and Midwestern University 's Office of Research and Sponsored Programs, Core Facility, and Department of Anatomy. Funding sources played no role in the design or execution of this study or in the writing or submission of this article.

Funding Information:
This study is dedicated to the memory of Dennis E. Slice, whose contributions to the discipline of geometric morphometrics were matched only by his generosity and collegiality. For specimen access and curatorial assistance, we thank L. Heaney, A. Ferguson, W. Stanley, and R. Banasiak (Field Museum of Natural History); D. Lundey and E. Langan (National Museum of Natural History—Smithsonian Institution); K. McNulty, M. Tappan, and J. Soderbergh (Department of Anthropology, University of Minnesota—Twin Cities); W.S. McGraw (Department of Anthropology, The Ohio State University); R. Portela Miquez and P. Jenkins (Natural History Museum—London); B. Mahala and S. van der Merwe (Amathole Museum—Qonce); and T. Rae (University of Roehampton). Logistical support was provided by NYCEP, the Field Museum of Natural History, and the Department of Anthropology, University of Illinois–Urbana-Champaign. For data collection and technical assistance, we thank past Midwestern University staff members A. Martiny, B. Seitelman, and J. Krecioch and student researchers A. Schraber, C. Malzenski, and D. Polito. Clément Zanolli and four anonymous reviewers provided constructive comments that improved this manuscript. This study is NYCEP Morphometrics Contribution #115. This research was supported by the Australian Research Council (DP170100056), The Leakey Foundation, and Midwestern University's Office of Research and Sponsored Programs, Core Facility, and Department of Anatomy. Funding sources played no role in the design or execution of this study or in the writing or submission of this article.

Publisher Copyright:
© 2021 Elsevier Ltd

Keywords

Anterior dental loading
Facial retraction
Hard-object feeding
Mangabey
Masticatory biomechanics
Suborbital fossa

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't

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10.1016/j.jhevol.2021.103121

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@article{35917d988d494fc9881745ea2e2620ad,

title = "Biomechanical correlates of zygomaxillary-surface shape in papionin primates and the effects of hard-object feeding on mangabey facial form",

abstract = "Extant African papioninans are distinguished from macaques by the presence of excavated facial fossae; however, facial excavation differs among taxa. Mangabeys (Cercocebus, Rungwecebus, and Lophocebus) exhibit fossae that invade the zygomatic forming pronounced suborbital fossae (SOFs). Larger-bodied Papio, Mandrillus, and Theropithecus have lateral rostral fossae with minimal/absent suborbital fossae. Because prior studies have shown that mangabeys exhibit adaptations to anterior dental loading (e.g., palatal retraction), it is plausible that mangabey SOFs represent structural accommodation to masticatory-system shape rather than facial allometry, as commonly hypothesized. We analyzed covariation between zygomaxillary-surface shape, masticatory-system shape, and facial size in 141 adult crania of Macaca fascicularis, Papio kindae, Cercocebus, and Lophocebus. These taxa represent the range of papionin SOF expression while minimizing size variation (narrow allometry). Masticatory-system landmarks (39) registered palate shape, bite points, masticatory muscle attachments, and the temporomandibular joint. Semilandmarks (450) captured zygomaxillary-surface shape. Following Procrustes superimposition with semilandmark sliding and principal components analyses, multivariate regression was used to explore allometry, and two-block partial least-squares analyses (within-configuration and separate-blocks) were used to examine covariation patterns. Scores on principal components 1–2 and the first partial least-square (PLS1) separate mangabeys from Macaca and Papio. Both zygomaxillary-surface shape and masticatory-system shape are correlated with size within taxa and facial morphotypes; however, regression distributions indicate morphotype shape differences are non-allometric. PLS1 accounts for ∼95% of shape covariance (p < 0.0001) and shows strong linear correlations (r-PLS = ∼0.95, p < 0.0001) between blocks. Negative PLS1 scores in mangabeys reflect deep excavation of the suborbital malar surface, palatal retraction, and anterior displacement of jaw adductor muscles and the temporomandibular joint. Neither PC1 nor PLS1 scores ordinate specimens by facial size. Taken together, these results fail to support the allometric hypothesis but suggest that mangabey zygomaxillary morphology is closely linked with adaptations to hard-object feeding.",

keywords = "Anterior dental loading, Facial retraction, Hard-object feeding, Mangabey, Masticatory biomechanics, Suborbital fossa",

author = "Michelle Singleton and Ehrlich, {Daniel E.} and Adams, {Justin W.}",

note = "Funding Information: This study is dedicated to the memory of Dennis E. Slice, whose contributions to the discipline of geometric morphometrics were matched only by his generosity and collegiality. For specimen access and curatorial assistance, we thank L. Heaney, A. Ferguson, W. Stanley, and R. Banasiak (Field Museum of Natural History); D. Lundey and E. Langan (National Museum of Natural History—Smithsonian Institution); K. McNulty, M. Tappan, and J. Soderbergh (Department of Anthropology, University of Minnesota—Twin Cities); W.S. McGraw (Department of Anthropology, The Ohio State University); R. Portela Miquez and P. Jenkins (Natural History Museum—London); B. Mahala and S. van der Merwe (Amathole Museum—Qonce); and T. Rae (University of Roehampton). Logistical support was provided by NYCEP, the Field Museum of Natural History, and the Department of Anthropology, University of Illinois–Urbana-Champaign. For data collection and technical assistance, we thank past Midwestern University staff members A. Martiny, B. Seitelman, and J. Krecioch and student researchers A. Schraber, C. Malzenski, and D. Polito. Cl{\'e}ment Zanolli and four anonymous reviewers provided constructive comments that improved this manuscript. This study is NYCEP Morphometrics Contribution #115. This research was supported by the Australian Research Council ( DP170100056 ), The Leakey Foundation , and Midwestern University 's Office of Research and Sponsored Programs, Core Facility, and Department of Anatomy. Funding sources played no role in the design or execution of this study or in the writing or submission of this article. Funding Information: This study is dedicated to the memory of Dennis E. Slice, whose contributions to the discipline of geometric morphometrics were matched only by his generosity and collegiality. For specimen access and curatorial assistance, we thank L. Heaney, A. Ferguson, W. Stanley, and R. Banasiak (Field Museum of Natural History); D. Lundey and E. Langan (National Museum of Natural History—Smithsonian Institution); K. McNulty, M. Tappan, and J. Soderbergh (Department of Anthropology, University of Minnesota—Twin Cities); W.S. McGraw (Department of Anthropology, The Ohio State University); R. Portela Miquez and P. Jenkins (Natural History Museum—London); B. Mahala and S. van der Merwe (Amathole Museum—Qonce); and T. Rae (University of Roehampton). Logistical support was provided by NYCEP, the Field Museum of Natural History, and the Department of Anthropology, University of Illinois–Urbana-Champaign. For data collection and technical assistance, we thank past Midwestern University staff members A. Martiny, B. Seitelman, and J. Krecioch and student researchers A. Schraber, C. Malzenski, and D. Polito. Cl{\'e}ment Zanolli and four anonymous reviewers provided constructive comments that improved this manuscript. This study is NYCEP Morphometrics Contribution #115. This research was supported by the Australian Research Council (DP170100056), The Leakey Foundation, and Midwestern University's Office of Research and Sponsored Programs, Core Facility, and Department of Anatomy. Funding sources played no role in the design or execution of this study or in the writing or submission of this article. Publisher Copyright: {\textcopyright} 2021 Elsevier Ltd",

year = "2022",

month = feb,

doi = "10.1016/j.jhevol.2021.103121",

language = "English (US)",

volume = "163",

journal = "Journal of Human Evolution",

issn = "0047-2484",

publisher = "Academic Press Inc.",

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TY - JOUR

T1 - Biomechanical correlates of zygomaxillary-surface shape in papionin primates and the effects of hard-object feeding on mangabey facial form

AU - Singleton, Michelle

AU - Ehrlich, Daniel E.

AU - Adams, Justin W.

N1 - Funding Information: This study is dedicated to the memory of Dennis E. Slice, whose contributions to the discipline of geometric morphometrics were matched only by his generosity and collegiality. For specimen access and curatorial assistance, we thank L. Heaney, A. Ferguson, W. Stanley, and R. Banasiak (Field Museum of Natural History); D. Lundey and E. Langan (National Museum of Natural History—Smithsonian Institution); K. McNulty, M. Tappan, and J. Soderbergh (Department of Anthropology, University of Minnesota—Twin Cities); W.S. McGraw (Department of Anthropology, The Ohio State University); R. Portela Miquez and P. Jenkins (Natural History Museum—London); B. Mahala and S. van der Merwe (Amathole Museum—Qonce); and T. Rae (University of Roehampton). Logistical support was provided by NYCEP, the Field Museum of Natural History, and the Department of Anthropology, University of Illinois–Urbana-Champaign. For data collection and technical assistance, we thank past Midwestern University staff members A. Martiny, B. Seitelman, and J. Krecioch and student researchers A. Schraber, C. Malzenski, and D. Polito. Clément Zanolli and four anonymous reviewers provided constructive comments that improved this manuscript. This study is NYCEP Morphometrics Contribution #115. This research was supported by the Australian Research Council ( DP170100056 ), The Leakey Foundation , and Midwestern University 's Office of Research and Sponsored Programs, Core Facility, and Department of Anatomy. Funding sources played no role in the design or execution of this study or in the writing or submission of this article. Funding Information: This study is dedicated to the memory of Dennis E. Slice, whose contributions to the discipline of geometric morphometrics were matched only by his generosity and collegiality. For specimen access and curatorial assistance, we thank L. Heaney, A. Ferguson, W. Stanley, and R. Banasiak (Field Museum of Natural History); D. Lundey and E. Langan (National Museum of Natural History—Smithsonian Institution); K. McNulty, M. Tappan, and J. Soderbergh (Department of Anthropology, University of Minnesota—Twin Cities); W.S. McGraw (Department of Anthropology, The Ohio State University); R. Portela Miquez and P. Jenkins (Natural History Museum—London); B. Mahala and S. van der Merwe (Amathole Museum—Qonce); and T. Rae (University of Roehampton). Logistical support was provided by NYCEP, the Field Museum of Natural History, and the Department of Anthropology, University of Illinois–Urbana-Champaign. For data collection and technical assistance, we thank past Midwestern University staff members A. Martiny, B. Seitelman, and J. Krecioch and student researchers A. Schraber, C. Malzenski, and D. Polito. Clément Zanolli and four anonymous reviewers provided constructive comments that improved this manuscript. This study is NYCEP Morphometrics Contribution #115. This research was supported by the Australian Research Council (DP170100056), The Leakey Foundation, and Midwestern University's Office of Research and Sponsored Programs, Core Facility, and Department of Anatomy. Funding sources played no role in the design or execution of this study or in the writing or submission of this article. Publisher Copyright: © 2021 Elsevier Ltd

PY - 2022/2

Y1 - 2022/2

N2 - Extant African papioninans are distinguished from macaques by the presence of excavated facial fossae; however, facial excavation differs among taxa. Mangabeys (Cercocebus, Rungwecebus, and Lophocebus) exhibit fossae that invade the zygomatic forming pronounced suborbital fossae (SOFs). Larger-bodied Papio, Mandrillus, and Theropithecus have lateral rostral fossae with minimal/absent suborbital fossae. Because prior studies have shown that mangabeys exhibit adaptations to anterior dental loading (e.g., palatal retraction), it is plausible that mangabey SOFs represent structural accommodation to masticatory-system shape rather than facial allometry, as commonly hypothesized. We analyzed covariation between zygomaxillary-surface shape, masticatory-system shape, and facial size in 141 adult crania of Macaca fascicularis, Papio kindae, Cercocebus, and Lophocebus. These taxa represent the range of papionin SOF expression while minimizing size variation (narrow allometry). Masticatory-system landmarks (39) registered palate shape, bite points, masticatory muscle attachments, and the temporomandibular joint. Semilandmarks (450) captured zygomaxillary-surface shape. Following Procrustes superimposition with semilandmark sliding and principal components analyses, multivariate regression was used to explore allometry, and two-block partial least-squares analyses (within-configuration and separate-blocks) were used to examine covariation patterns. Scores on principal components 1–2 and the first partial least-square (PLS1) separate mangabeys from Macaca and Papio. Both zygomaxillary-surface shape and masticatory-system shape are correlated with size within taxa and facial morphotypes; however, regression distributions indicate morphotype shape differences are non-allometric. PLS1 accounts for ∼95% of shape covariance (p < 0.0001) and shows strong linear correlations (r-PLS = ∼0.95, p < 0.0001) between blocks. Negative PLS1 scores in mangabeys reflect deep excavation of the suborbital malar surface, palatal retraction, and anterior displacement of jaw adductor muscles and the temporomandibular joint. Neither PC1 nor PLS1 scores ordinate specimens by facial size. Taken together, these results fail to support the allometric hypothesis but suggest that mangabey zygomaxillary morphology is closely linked with adaptations to hard-object feeding.

AB - Extant African papioninans are distinguished from macaques by the presence of excavated facial fossae; however, facial excavation differs among taxa. Mangabeys (Cercocebus, Rungwecebus, and Lophocebus) exhibit fossae that invade the zygomatic forming pronounced suborbital fossae (SOFs). Larger-bodied Papio, Mandrillus, and Theropithecus have lateral rostral fossae with minimal/absent suborbital fossae. Because prior studies have shown that mangabeys exhibit adaptations to anterior dental loading (e.g., palatal retraction), it is plausible that mangabey SOFs represent structural accommodation to masticatory-system shape rather than facial allometry, as commonly hypothesized. We analyzed covariation between zygomaxillary-surface shape, masticatory-system shape, and facial size in 141 adult crania of Macaca fascicularis, Papio kindae, Cercocebus, and Lophocebus. These taxa represent the range of papionin SOF expression while minimizing size variation (narrow allometry). Masticatory-system landmarks (39) registered palate shape, bite points, masticatory muscle attachments, and the temporomandibular joint. Semilandmarks (450) captured zygomaxillary-surface shape. Following Procrustes superimposition with semilandmark sliding and principal components analyses, multivariate regression was used to explore allometry, and two-block partial least-squares analyses (within-configuration and separate-blocks) were used to examine covariation patterns. Scores on principal components 1–2 and the first partial least-square (PLS1) separate mangabeys from Macaca and Papio. Both zygomaxillary-surface shape and masticatory-system shape are correlated with size within taxa and facial morphotypes; however, regression distributions indicate morphotype shape differences are non-allometric. PLS1 accounts for ∼95% of shape covariance (p < 0.0001) and shows strong linear correlations (r-PLS = ∼0.95, p < 0.0001) between blocks. Negative PLS1 scores in mangabeys reflect deep excavation of the suborbital malar surface, palatal retraction, and anterior displacement of jaw adductor muscles and the temporomandibular joint. Neither PC1 nor PLS1 scores ordinate specimens by facial size. Taken together, these results fail to support the allometric hypothesis but suggest that mangabey zygomaxillary morphology is closely linked with adaptations to hard-object feeding.

KW - Anterior dental loading

KW - Facial retraction

KW - Hard-object feeding

KW - Mangabey

KW - Masticatory biomechanics

KW - Suborbital fossa

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Biomechanical correlates of zygomaxillary-surface shape in papionin primates and the effects of hard-object feeding on mangabey facial form

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