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Patterns and Constraints of Craniofacial Variation in Colobine Monkeys: Disentangling the Effects of Phylogeny, Allometry and Diet

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Abstract

Leaf-eating monkeys (colobines) are a highly diversified subfamily with 61 species in ten genera, in which patterns and constraints of morphological evolution are still poorly resolved. In the present study, we measured the skulls of 452 specimens collected from different museums worldwide. Using one of the most extensive samples ever employed, and geometric morphometric techniques, we aimed to elucidate the evolutionary processes that have led to the craniofacial diversification of colobines. Our comprehensive analyses of the colobine cranium demonstrated that phylogeny is the first order signal to emerge, with clear interspecific patterns of differentiation. Allometric trend constrains shape variation for most colobine taxa, but to a lesser degree than phylogeny. We also confirmed that diet is significantly associated with the variation in cranial shape among colobines. In particular, the mechanical advantage of the masseter for biting at the anterior dentition is linked to seed intake. We postulate that such ecomorphological patterns explain, in part, the non-phylogenetic and non-allometric variations in the colobine skull, and indicate the importance of diet in interspecific resource partitioning, allowing for species coexistence.

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Acknowledgements

Authors thank the museum staffs for access to specimens and Goro Hanya, Takeshi Nishimura, Gen Suwa, Daisuke Shimizu, and Masanaru Takai for discussions. This study was supported by KAKENHI (Grant Nos. 26711023, 18H02492, 18H04816, and 18K19359), by the Cooperation Research Program of Primate Research Institute, Kyoto University (Grant No. 2010-A-3) and by the LabEx Sciences Archéologiques de Bordeaux (Grant No. ANR-10-LABX-52).

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Authors and Affiliations

  1. UMR5199 PACEA, Université de Bordeaux, Allée Geoffroy Saint Hilaire, Bâtiment B8, 33615, Pessac, France

    Ronan Ledevin

  2. Department of Humanities and Sciences, Musashino Art University, 1-736 Ogawa-cho, Kodaira, Tokyo, 187-8505, Japan

    Daisuke Koyabu

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  1. Ronan Ledevin
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Correspondence to Daisuke Koyabu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11692_2019_9469_MOESM1_ESM.xlsx

Online Resource 1 List of the specimens analyzed in this study, with accession ID and institutes housing them: Natural History Museum (BMNH), Primate Research Institute of Kyoto University (KUPRI), Smithsonian National Museum of Natural History (USNM), and Zoological Reference Collection of Lee Kong Chian Natural History Museum at the National University of Singapore (ZRC)—Supplementary material 1 (XLSX 32 KB)

Online Resource 2 Measurements employed in the mechanical advantage analyses—Supplementary material 2 (PDF 393 KB)

11692_2019_9469_MOESM3_ESM.xlsx

Online Resource 3 Landmark definitions employed in the geometric morphometric analyses—Supplementary material 3 (XLSX 9 KB)

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Online Resource 4 Mean values of measured moment arms and calculated mechanical advantages of the masseter, temporalis, and medial pterygoid muscles for each species. Canine position measurement is not available for T. policephalus due to missing canine in the studied specimen—Supplementary material 4 (XLSX 23 KB)

11692_2019_9469_MOESM5_ESM.xlsx

Online Resource 5 Pearson’s correlation coefficients for comparsions between mechanical advantage and centroid size—Supplementary material 5 (XLSX 9 KB)

11692_2019_9469_MOESM6_ESM.xls

Online Resource 6 Inter-specific comparison of size using Kruskal-Wallis tests. Significant probabilities are either in bold (P < 0.001) or in italic (P < 0.05). Species for which the number of specimens available if lower than five are written in red—Supplementary material 6 (XLS 51 KB)

11692_2019_9469_MOESM7_ESM.xlsx

Online Resource 7 Basic measurements (n = 15) and centroid size (n = 2) for Simias concolor—Supplementary material 7 (XLSX 9 KB)

11692_2019_9469_MOESM8_ESM.pdf

Online Resource 8 Alternative representation of shape deformations associated to: 1) shape axes bgPC1, bgPC2 and bgPC3, 2) allometry, and 3) 2B-PLS. Here the red dots correspond to the reference configuration compared to the target configuration (in green). The line between each red dot and its homologous green dot represents the deformation—Supplementary material 8 (PDF 1894 KB)

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Ledevin, R., Koyabu, D. Patterns and Constraints of Craniofacial Variation in Colobine Monkeys: Disentangling the Effects of Phylogeny, Allometry and Diet. Evol Biol 46, 14–34 (2019). https://doi.org/10.1007/s11692-019-09469-7

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