Heritability in the Rhesus Macaque (Macaca mulatta) Vertebral Column.

allometry axial skeleton genotype pedigree phenotype postcranial skeleton

Journal

American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949

Informations de publication

Date de publication:
20 Oct 2024
Historique:
revised: 19 09 2024
received: 06 02 2024
accepted: 28 09 2024
medline: 21 10 2024
pubmed: 21 10 2024
entrez: 21 10 2024
Statut: aheadofprint

Résumé

The vertebral column plays a central role in primate locomotion and positional behavior. Understanding its evolution, therefore, has the potential to clarify evolutionary processes that have occurred in the primate lineage as well as the specific behaviors of extinct primates. However, to understand primate vertebral anatomy, it is important to determine how much of this anatomy is heritable and how much develops as a response to environmental factors during life. We estimated heritability for vertebral counts as well as typical cervical, thoracic, and lumbar elements from 210 individuals from the pedigreed Cayo Santiago Macaca mulatta skeletal collection. We found moderate heritability of vertebral counts (h La columna vertebral tiene un rol central en la locomoción y postura de los primates. Por ende, entender su evolución podría clarificar tanto los procesos evolutivos en los primates como los comportamientos específicos de los primates extintos. Sin embargo, para poder entender la evolución de la anatomía vertebral es importante determinar cuál es la contribución genética y cuál es la contribución del comportamiento en vida a la anatomía. Estimamos heritabilidad para el número de vertebras y para vertebras típicas cervicales, torácicas y lumbares de 210 individuos de la colección esquelética de Macaca mulatta de Cayo Santiago, la cual tiene información genealógica. Encontramos estimados moderados de heritabilidad para el número de vértebras (h

Autres résumés

Type: Publisher (spa)
La columna vertebral tiene un rol central en la locomoción y postura de los primates. Por ende, entender su evolución podría clarificar tanto los procesos evolutivos en los primates como los comportamientos específicos de los primates extintos. Sin embargo, para poder entender la evolución de la anatomía vertebral es importante determinar cuál es la contribución genética y cuál es la contribución del comportamiento en vida a la anatomía. Estimamos heritabilidad para el número de vertebras y para vertebras típicas cervicales, torácicas y lumbares de 210 individuos de la colección esquelética de Macaca mulatta de Cayo Santiago, la cual tiene información genealógica. Encontramos estimados moderados de heritabilidad para el número de vértebras (h

Identifiants

pubmed: 39428679
doi: 10.1002/ajp.23686
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e23686

Subventions

Organisme : This project was funded by a Catalyzer Grant from the Puerto Rico Science, Technology, and Research Trust. The Caribbean Primate Research Center is funded by NIH ORIP #2-P40-OD012217.

Informations de copyright

© 2024 Wiley Periodicals LLC.

Références

Bastir, M., D. Sanz‐Prieto, J. M. López‐Rey, et al. 2022. “The Evolution, Form and Function of the Human Respiratory System.” Journal of Anthropological Sciences = Rivista di antropologia: JASS 100: 141–172. https://doi.org/10.4436/JASS.10014.
Belting, H.‐G., C. S. Shashikant, and F. H. Ruddle. 1998. “Modification of Expression and Cis ‐Regulation of Hoxc8 in the Evolution of Diverged Axial Morphology.” Proceedings of the National Academy of Sciences of the United States of America 95, no. 5: 2355–2360. https://doi.org/10.1073/pnas.95.5.2355.
Bénazéraf, B., and O. Pourquié. 2013. “Formation and Segmentation of the Vertebrate Body Axis.” Annual Review of Cell and Developmental Biology 29, no. 1: 1–26. https://doi.org/10.1146/annurev-cellbio-101011-155703.
Benton, R. S. 1976. “Structural Patterns in the Pongidae and Cercopithecidae.” Yearbook of Physical Anthropology 18: 65–88.
Benton, R. S. 1965. “Morphological Evidence for Adaptations Within the Epaxial Region of the Primates.” In The Baboon in Medical Research, edited by H. Vaghtborg, 10–20. University of Texas Press.
Blomquist, G. E. 2012. “Female Age of First Reproduction at Cayo Santiago: Heritability and Shared Environments.” In Bones, Genetics, and Behavior of Rhesus Macaques, edited by Q. Wang, 195–208. New York, NY: Springer. https://doi.org/10.1007/978-1-4614-1046-1_9.
Böhmer, C., E. Amson, P. Arnold, A. H. van Heteren, and J. A. Nyakatura. 2018. “Homeotic Transformations Reflect Departure From the Mammalian ‘Rule of Seven’ Cervical Vertebrae in Sloths: Inferences on the Hox Code and Morphological Modularity of the Mammalian Neck.” BMC Evolutionary Biology 18, no. 1: 84. https://doi.org/10.1186/s12862-018-1202-5.
Borchers, N., N. Reinsch, and E. Kalm. 2004. “The Number of Ribs and Vertebrae in a Piétrain Cross: Variation, Heritability and Effects on Performance Traits.” Journal of Animal Breeding and Genetics 121, no. 6: 392–403.
Boszczyk, B. M., A. A. Boszczyk, and R. Putz. 2001. “Comparative and Functional Anatomy of the Mammalian Lumbar Spine.” Anatomical Record 264, no. 2: 157–168. https://doi.org/10.1002/ar.1156.
ten Broek, C. M. A., A. J. Bakker, I. Varela‐Lasheras, M. Bugiani, S. Van Dongen, and F. Galis. 2012. “Evo‐Devo of the Human Vertebral Column: On Homeotic Transformations, Pathologies and Prenatal Selection.” Evolutionary Biology 39, no. 4: 456–471. https://doi.org/10.1007/s11692-012-9196-1.
Buchholtz, E. A., H. G. Bailin, S. A. Laves, J. T. Yang, M.‐Y. Chan, and L. E. Drozd. 2012. “Fixed Cervical Count and the Origin of the Mammalian Diaphragm.” Evolution & Development 14, no. 5: 399–411. https://doi.org/10.1111/j.1525-142X.2012.00560.x.
Bull, J. J. 1987. “Evolution of Phenotypic Variance.” Evolution 41, no. 2: 303–315. https://doi.org/10.1111/j.1558-5646.1987.tb05799.x.
Burgos, J., C. Barrios, G. Mariscal, A. Lorente, and R. Lorente. 2021. “Non‐Uniform Segmental Range of Motion of the Thoracic Spine During Maximal Inspiration and Exhalation in Healthy Subjects.” Frontiers in Medicine 8: 699357. https://doi.org/10.3389/fmed.2021.699357.
Cheverud, J. M. 1982. “Phenotypic, Genetic, and Environmental Morphological Integration in the Cranium.” Evolution 36, no. 3: 499–516. https://doi.org/10.1111/j.1558-5646.1982.tb05070.x.
Cheverud, J. M. 1995. “Morphological Integration in the Saddle‐Back Tamarin (Saguinus fuscicollis) Cranium.” The American Naturalist 145, no. 1: 63–89. https://doi.org/10.1086/285728.
Cheverud, J. M. 1996. “Quantitative Genetic Analysis of Cranial Morphology in the Cotton‐Top (Saguinus oedipus) and Saddle‐Back (S. fuscicollis) Tamarins.” Journal of Evolutionary Biology 9: 5–42.
Cheverud, J. M., and J. E. Buikstra. 1981. “Quantitative Genetics of Skeletal Nonmetric Traits in the Rhesus Macaques on Cayo Santiago. II. Phenotypic, Genetic, and Environmental Correlations Between Traits.” American Journal of Physical Anthropology 54, no. 1: 51–58. https://doi.org/10.1002/ajpa.1330540107.
Cheverud, J. M., and J. E. Buikstra. 1982. “Quantitative Genetics of Skeletal Nonmetric Traits in the Rhesus Macaques of Cayo Santiago. III. Relative Heritability of Skeletal Nonmetric and Metric Traits.” American Journal of Physical Anthropology 59, no. 2: 151–155. https://doi.org/10.1002/ajpa.1330590205.
Cheverud, J. M., and W. P. J. Dittus. 1992. “Primate Population Studies at Polonnaruwa. II. Heritability of Body Measurements in a Natural Population of Toque Macaques (Macaca sinica).” American Journal of Primatology 27, no. 2: 145–154.
Chi, P. B., A. E. Duncan, P. A. Kramer, and V. N. Minin. 2014. “Heritability Estimation of Osteoarthritis in the Pig‐Tailed Macaque (Macaca nemestrina) With a Look Toward Future Data Collection.” PeerJ 2: e373. https://doi.org/10.7717/peerj.373.
Conley, D., T. M. Laidley, J. D. Boardman, and B. W. Domingue. 2016. “Changing Polygenic Penetrance on Phenotypes in the 20th Century Among Adults in the US Population.” Scientific Reports 6, no. 1: 30348. https://doi.org/10.1038/srep30348.
Corruccini, R. S. 1987. “Shape in Morphometrics: Comparative Analyses.” American Journal of Physical Anthropology 73, no. 3: 289–303.
Diaz‐Cuadros, M., O. Pourquié, and E. El‐Sherif. 2021. “Patterning With Clocks and Genetic Cascades: Segmentation and Regionalization of Vertebrate Versus Insect Body Plans.” PLOS Genetics 17, no. 10: e1009812. https://doi.org/10.1371/journal.pgen.1009812.
Fierst, J. L. 2011. “A History of Phenotypic Plasticity Accelerates Adaptation to a New Environment: Phenotypic Plasticity Accelerates Adaptation.” Journal of Evolutionary Biology 24, no. 9: 1992–2001. https://doi.org/10.1111/j.1420-9101.2011.02333.x.
Fleagle, J. G. 1983. “Locomotor Adaptations of Oligocene and Miocene Hominoids and Their Phyletic Implications.” In New Interpretations of Ape and Human Ancestry, edited by R. L. Ciochon and R. S. Corruccini, 301–324. New York, NY: Springer.
Fleagle, J. G. 1985. “Size and Adaptation in Primates.” In Size and Scaling in Primate Biology, edited by W. L. Jungers, 1–19. New York, NY: Springer.
Fox, R. J., J. M. Donelson, C. Schunter, T. Ravasi, and J. D. Gaitán‐Espitia. 2019. “Beyond Buying Time: The Role of Plasticity in Phenotypic Adaptation to Rapid Environmental Change.” Philosophical Transactions of the Royal Society B: Biological Sciences 374, no. 1768: 20180174. https://doi.org/10.1098/rstb.2018.0174.
Galis, F. 1999. “Why Do Almost All Mammals Have Seven Cervical Vertebrae? Developmental Constraints, Hox Genes, and Cancer.” Journal of Experimental Zoology 285: 19–26.
Galis, F., D. R. Carrier, J. van Alphen, et al. 2014. “Fast Running Restricts Evolutionary Change of the Vertebral Column in Mammals.” Proceedings of the National Academy of Sciences of the United States of America 111, no. 31: 11401–11406. https://doi.org/10.1073/pnas.1401392111.
Galis, F., T. J. M. V. Dooren, J. D. Feuth, et al. 2006. “Extreme Selection in Humans Against Homeotic Transformations of Cervical Vertebrae.” Evolution 60, no. 12: 2643–2654. https://doi.org/10.1111/j.0014-3820.2006.tb01896.x.
Gebo, D. 1993. Postcranial Adaptation in Non‐Human Primates. DeKalb, IL: Northern Illinois University Press.
Gilbert, S. F. 2005. “Mechanisms for the Environmental Regulation of Gene Expression: Ecological Aspects of Animal Development.” Journal of Biosciences 30, no. 1: 65–74. https://doi.org/10.1007/BF02705151.
Gomez, C., and O. Pourquié. 2009. “Developmental Control of Segment Numbers in Vertebrates.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 312, no. 6: 533–544. https://doi.org/10.1002/jez.b.21305.
Gommery, D. 2006. “Evolution of the Vertebral Column in Miocene Hominoids and Plio‐Pleistocene Hominids.” In Human Origins and Environmental Backgrounds, edited by H. Ishida, R. Tuttle, M. Pickford, N. Ogihara, and M. Nakatsukasa, 31–43. Springer US. https://doi.org/10.1007/0-387-29798-7_3.
Graf, W., C. de Waele, P. P. Vidal, D. H. Wang, and C. Evinger. 1995. “The Orientation of the Cervical Vertebral Column in Unrestrained Awake Animals (Part 1 of 2).” Brain, Behavior and Evolution 45: 209–220.
Hadfield, J. D. 2010. “MCMC Methods for Multi‐Response Generalized Linear Mixed Models: The MCMCglmm R Package.” Journal of Statistical Software 33, no. 2: 1–22.
Halenar, L. B., and A. L. Rosenberger. 2013. “A Closer Look at the Protopithecus Fossil Assemblages: New Genus and Species From Bahia, Brazil.” Journal of Human Evolution 65, no. 4: 374–390. https://doi.org/10.1016/j.jhevol.2013.07.008.
Hallgrímsson, B., K. Willmore, and B. K. Hall. 2002. “Canalization, Developmental Stability, and Morphological Integration in Primate Limbs.” American Journal of Physical Anthropology 119, no. S35: 131–158. https://doi.org/10.1002/ajpa.10182.
Havill, L. M., M. R. Allen, T. L. Bredbenner, et al. 2010. “Heritability of Lumbar Trabecular Bone Mechanical Properties in Baboons.” Bone 46, no. 3: 835–840. https://doi.org/10.1016/j.bone.2009.11.002.
Henderson, C. R. 1976. “A Simple Method for Computing the Inverse of a Numerator Relationship Matrix Used in Prediction of Breeding Values.” Biometrics 32, no. 1: 69–83. https://doi.org/10.2307/2529339.
Hill, W. G., M. E. Goddard, and P. M. Visscher. 2008. “Data and Theory Point to Mainly Additive Genetic Variance for Complex Traits.” PLoS Genetics 4, no. 2: e1000008. https://doi.org/10.1371/journal.pgen.1000008.
Hivert, V., J. Sidorenko, F. Rohart, et al. 2021. “Estimation of Non‐Additive Genetic Variance in Human Complex Traits From a Large Sample of Unrelated Individuals.” American Journal of Human Genetics 108, no. 5: 786–798. https://doi.org/10.1016/j.ajhg.2021.02.014.
Hodges, P. W., V. S. Gurfinkel, S. Brumagne, T. C. Smith, and P. C. Cordo. 2002. “Coexistence of Stability and Mobility in Postural Control: Evidence From Postural Compensation for Respiration.” Experimental Brain Research 144: 293–302.
Ishiguro, K., T. Kawashima, and F. Sato. 2020. “The Phenotypic Morphology of Human Lumbar Plexus Roots Associated With Changes in the Thoracolumbar Vertebral Count and Trade‐Off.” Scientific Reports 10, no. 1: 127. https://doi.org/10.1038/s41598-019-56709-z.
Jellema, L. M., B. Latimer, and A. Walker. 1993. “The Rib Cage.” In the Nariokotome Homo Erectus Skeleton, edited by A. Walker, and R. Leakey, 294–325. Cambridge, MA: Harvard University Press.
Joganic, J. L., K. E. Willmore, J. T. Richtsmeier, et al. 2018. “Additive Genetic Variation in the Craniofacial Skeleton of Baboons (Genus Papio) and Its Relationship to Body and Cranial Size.” American Journal of Physical Anthropology 165, no. 2: 269–285. https://doi.org/10.1002/ajpa.23349.
Johnson, D. R., and P. O'higgins. 1994. “The Inheritance of Patterns of Metameric Variation in the Mouse (Mus musculus) Vertebral Column.” Journal of Zoology 233, no. 3: 473–492. https://doi.org/10.1111/j.1469-7998.1994.tb05278.x.
Jungers, W. L., A. B. Falsetti, and C. E. Wall. 1995. “Shape, Relative Size, and Size‐Adjustments in Morphometrics.” American Journal of Physical Anthropology 38, no. S21: 137–161. https://doi.org/10.1002/ajpa.1330380608.
Kapandji, I. A. 1974. The Physiology of the Joints. Vol. 3, The Trunk and Vertebral Column. New York, NY: Churchill Livingstone.
Kessel, M., and P. Gruss. 1991. “Homeotic Transformations of Murine Vertebrae and Concomitant Alteration of Hox Codes Induced By Retinoic Acid.” Cell 67, no. 1: 89–104. https://doi.org/10.1016/0092-8674(91)90574-I.
Kida, M. Y., D. R. Johnson, T. J. McAndrew, and P. O'higgins. 1999. “Adaptation in the Vertebral Column: A Comparative Study of Patterns of Metameric Variation in Seven Species of Small Mammals.” Journal of Anatomy 194, no. 2: 207–214. https://doi.org/10.1046/j.1469-7580.1999.19420207.x.
Kikuchi, Y., and N. Ogihara. 2021. “Functional Anatomy and Adaptation of the Third to Sixth Thoracic Vertebrae in Primates Using Three‐Dimensional Geometric Morphometrics.” Primates 62: 845–855.
Kim, T., D. R. Seol, S. C. Hahm, et al. 2015. “Analgesic Effect of Intra‐Articular Injection of Temperature‐Responsive Hydrogel Containing Bupivacaine on Osteoarthritic Pain in Rats.” BioMed Research International 2015: 1–9. https://doi.org/10.1155/2015/671349.
Kimock, C. M., C. Dubuc, L. J. N. Brent, and J. P. Higham. 2019. “Male Morphological Traits Are Heritable But Do Not Predict Reproductive Success in a Sexually‐Dimorphic Primate.” Scientific Reports 9, no. 1: 19794. https://doi.org/10.1038/s41598-019-52633-4.
Klein, T. W. 1974. “Heritability and Genetic Correlation: Statistical Power, Population Comparisons, and Sample Size.” Behavior Genetics 4, no. 2: 171–189. https://doi.org/10.1007/BF01065758.
Klein, T. W., J. C. DeFries, and C. T. Finkbeiner. 1973. “Heritability and Genetic Correlation: Standard Errors of Estimates and Sample Size.” Behavior Genetics 3, no. 4: 355–364. https://doi.org/10.1007/BF01070218.
Lande, R., and S. J. Arnold. 1983. “The Measurement of Selection on Correlated Characters.” Evolution 37, no. 6: 1210. https://doi.org/10.2307/2408842.
Larson, S. G. 2018. “Nonhuman Primate Locomotion.” American Journal of Physical Anthropology 165, no. 4: 705–725. https://doi.org/10.1002/ajpa.23368.
Latimer, B., and C. V. Ward. 1993. “The Thoracic and Lumbar Vertebrae.” In the Nariokotome Homo Erectus Skeleton skeleton, edited by A. Walker and R. Leakey, 266–293. Cambridge, MA: Harvard University Press.
Leigh, S. R. 1992. “Patterns of Variation in the Ontogeny of Primate Body Size Dimorphism.” Journal of Human Evolution 23, no. 1: 27–50. https://doi.org/10.1016/0047-2484(92)90042-8.
Lovejoy, C. O. 2005. “The Natural History of Human Gait and Posture Part 1. Spine and Pelvis.” Gait & Posture 21, no. 1: 95–112. https://doi.org/10.1016/S0966-6362(04)00014-1.
MacLarnon, A. 1987. Size Relationships of the Spinal Cord and Associated Skeleton in Primates [Doctoral Dissertation]. University College London.
MacLarnon, A. 1993. “The Vertebral Canal.” In the Nariokotome Homo Erectus Skeleton, edited by In. A. Walker, and R. Leakey, 359–390. Cambridge, MA: Harvard University Press.
MacLarnon, A. 1996. “The Evolution of the Spinal Cord in Primates: Evidence From the Foramen Magnum and the Vertebral Canal.” Journal of Human Evolution 30, no. 2: 121–138. https://doi.org/10.1006/jhev.1996.0009.
Maestripieri, D. 2009. “Maternal Influences on Offspring Growth, Reproduction, and Behavior in Primates.” In Maternal Effects in Mammals, edited by In. D. Maestripieri, and J. M. Mateo, 256–291. Chicago, IL: University of Chicago Press.
Mäki‐Tanila, A., and W. G. Hill. 2014. “Influence of Gene Interaction on Complex Trait Variation With Multilocus Models.” Genetics 198, no. 1: 355–367. https://doi.org/10.1534/genetics.114.165282.
Mallo, M. 2018. “Reassessing the Role of Hox Genes During Vertebrate Development and Evolution.” Trends in Genetics 34, no. 3: 209–217. https://doi.org/10.1016/j.tig.2017.11.007.
Mallo, M., T. Vinagre, and M. Carapuo. 2009. “The Road to the Vertebral Formula.” International Journal of Developmental Biology 53, no. 8‐9–10: 1469–1481. https://doi.org/10.1387/ijdb.072276mm.
Mallo, M., D. M. Wellik, and J. Deschamps. 2010. “Hox Genes and Regional Patterning of the Vertebrate Body Plan.” Developmental Biology 344, no. 1: 7–15. https://doi.org/10.1016/j.ydbio.2010.04.024.
Martínez‐Abadías, N., M. Esparza, T. Sjøvold, R. González‐José, M. Santos, and M. Hernández. 2009. “Heritability of Human Cranial Dimensions: Comparing the Evolvability of Different Cranial Regions.” Journal of Anatomy 214, no. 1: 19–35. https://doi.org/10.1111/j.1469-7580.2008.01015.x.
McAdam, A. G., S. Boutin, D. Réale, and D. Berteaux. 2002. “Maternal Effects and the Potential for Evolution in a Natural Population of Animals.” Evolution; International Journal of Organic Evolution 56, no. 4: 846–851. https://doi.org/10.1111/j.0014-3820.2002.tb01396.x.
McCollum, M. A., B. A. Rosenman, G. Suwa, R. S. Meindl, and C. O. Lovejoy. 2010. “The Vertebral Formula of the Last Common Ancestor of African Apes and Humans.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 314B, no. 2: 123–134. https://doi.org/10.1002/jez.b.21316.
Moyà‐Solà, S., M. Köhler, D. M. Alba, I. Casanovas‐Vilar, and J. Galindo. 2004. “Pierolapithecus catalaunicus, A New Middle Miocene Great Ape From Spain.” Science 306, no. 5700: 1339–1344. https://doi.org/10.1126/science.1103094.
Müller, J., T. M. Scheyer, J. J. Head, et al. 2010. “Homeotic Effects, Somitogenesis and the Evolution of Vertebral Numbers in Recent and Fossil Amniotes.” Proceedings of the National Academy of Sciences of the United States of America 107, no. 5: 2118–2123. https://doi.org/10.1073/pnas.0912622107.
Munds, R. A., E. B. Cooper, M. C. Janiak, et al. 2022. “Variation and Heritability of Retinal Cone Ratios in a Free‐Ranging Population of Rhesus Macaques.” Evolution 76, no. 8: 1776–1789. https://doi.org/10.1111/evo.14552.
Nakatsukasa, M. 2008. “Comparative Study of Moroto Vertebral Specimens.” Journal of Human Evolution 55, no. 4: 581–588. https://doi.org/10.1016/j.jhevol.2008.04.009.
Nakatsukasa, M. 2019. “Miocene Ape Spinal Morphology: The Evolution of Orthogrady.” In Spinal Evolution, edited by E. Been, A. Gómez‐Olivencia, and P. A. Kramer, 73–96. Springer.
Nakatsukasa, M., Y. Kunimatsu, Y. Nakano, and H. Ishida. 2007. “Vertebral Morphology of Nacholapithecus kerioi Based on KNM‐BG 35250.” Journal of Human Evolution 52, no. 4: 347–369. https://doi.org/10.1016/j.jhevol.2006.08.008.
Nalley, T. K., and N. Grider‐Potter. 2015. “Functional Morphology of the Primate Head and Neck.” American Journal of Physical Anthropology 156, no. 4: 531–542. https://doi.org/10.1002/ajpa.22729.
Narita, Y., and S. Kuratani. 2005. “Evolution of the Vertebral Formulae in Mammals: A Perspective on Developmental Constraints.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 304B, no. 2: 91–106. https://doi.org/10.1002/jez.b.21029.
O'Higgins, P., N. Milne, D. R. Johnson, C. K. Runnion, and C. E. Oxnard. 1997. “Adaptation in the Vertebral Column: A Comparative Study of Patterns of Metameric Variation in Mice and Men.” Journal of Anatomy 190, no. 1: 105–113. https://doi.org/10.1046/j.1469-7580.1997.19010105.x.
Pal, G. P., and R. V. Routal. 1986. “A Study of Weight Transmission Through the Cervical and Upper Thoracic Regions of the Vertebral Column in Man.” Journal of Anatomy 148: 245–261.
Pal, G. P., and R. V. Routal. 1987. “Transmission of Weight Through the Lower Thoracic and Lumbar Regions of the Vertebral Column in Man.” Journal of Anatomy 152: 93–105.
Patel, B. A., C. C. Gilbert, and K. E. Ericson. 2007. “Cercopithecoid Cervical Vertebral Morphology and Implications for the Presence of Theropithecus in Early Pleistocene Europe.” Journal of Human Evolution 52, no. 2: 113–129. https://doi.org/10.1016/j.jhevol.2006.07.014.
Pilbeam, D. 2004. “The Anthropoid Postcranial Axial Skeleton: Comments on Development, Variation, and Evolution.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 302B, no. 3: 241–267. https://doi.org/10.1002/jez.b.22.
Polderman, T. J. C., B. Benyamin, C. A. De Leeuw, et al. 2015. “Meta‐Analysis of the Heritability of Human Traits Based on Fifty Years of Twin Studies.” Nature Genetics 47, no. 7: 702–709. https://doi.org/10.1038/ng.3285.
Ponzi, E., L. F. Keller, T. Bonnet, and S. Muff. 2018. “Heritability, Selection, and the Response to Selection in the Presence of Phenotypic Measurement Error: Effects, Cures, and the Role of Repeated Measurements.” Evolution 72, no. 10: 1992–2004. https://doi.org/10.1111/evo.13573.
Preuschoft, H., S. Hayama, and M. M. Günther. 1988. “Curvature of the Lumbar Spine as a Consequence of Mechanical Necessities in Japanese Macaques Trained for Bipedalism.” Folia Primatologica 50, no. 1–2: 42–58. https://doi.org/10.1159/000156333.
R Core Team2023. R: A Language and Environment for Statistical Computing. (Version 4.3.1) [Computer Software]. R Foundation for Statistical Computing. https://www.R-project.org.
Romero, A. N., E. Dickinson, C. M. Turcotte, and C. E. Terhune. 2023. “Skeletal Age During Hurricane Impacts Fluctuating Asymmetry in Cayo Santiago Rhesus Macaques.” Ecology and Evolution 13, no. 8: e10425. https://doi.org/10.1002/ece3.10425.
Rook, L., B. Martínez‐Navarro, and F. Clark Howell. 2004. “Occurrence of Theropithecus sp. in the Late Villafranchian of Southern Italy and Implication for Early Pleistocene “Out of Africa” Dispersals.” Journal of Human Evolution 47, no. 4: 267–277. https://doi.org/10.1016/j.jhevol.2004.08.001.
Russo, G. A., and L. J. Shapiro. 2013. “Reevaluation of the Lumbosacral Region of Oreopithecus bambolii.” Journal of Human Evolution 65, no. 3: 253–265. https://doi.org/10.1016/j.jhevol.2013.05.004.
Sanders, W. J., and B. E. Bodenbender. 1994. “Morphometric Analysis of Lumbar Vertebra UMP 67‐28: Implications for Spinal Function and Phylogeny of the Miocene Moroto Hominoid.” Journal of Human Evolution 26: 203–237.
Šešelj, M., D. L. Duren, and R. J. Sherwood. 2015. “Heritability of the Human Craniofacial Complex.” Anatomical Record 298, no. 9: 1535–1547. https://doi.org/10.1002/ar.23186.
Schlensker, E., and O. Distl. 2016. “Heritability of Hemivertebrae in the French Bulldog Using an Animal Threshold Model.” The Veterinary Journal 207: 188–189.
Schultz, A. H. 1938. “The Relative Length of the Regions of the Spinal Column in Old World Primates.” American Journal of Physical Anthropology 24: 1–22.
Schultz, A. H. 1960. “Einige Beobachtungen und Maße am Skelett von Oreopithecus im Vergleich mit anderen catarrhinen Primaten.” Zeitschrift Für Morphologie Und Anthropologie 50: 136–149.
Schultz, A. H., and W. L. Straus Jr. 1945. “The Numbers of Vertebrae in Primates.” Proceedings of the American Philosophical Society 89: 601–626.
Shapiro, L. J. 1993. “Functional Morphology of the Vertebral Column in Primates.” In Postcranial Adaptation in Nonhuman Primates, edited by D. Gebo, 121–149. DeKalb, IL: Northern Illinois University Press.
Shapiro, L. J., and A. D. Kemp. 2019. “Functional and Developmental Influences on Intraspecific Variation in Catarrhine Vertebrae.” American Journal of Physical Anthropology 168, no. 1: 131–144. https://doi.org/10.1002/ajpa.23730.
Shapiro, L. J., C. V. M. Seiffert, L. R. Godfrey, W. L. Godfrey, E. L. Jungers, and G. F. N. Simons. 2005. “Morphometric Analysis of Lumbar Vertebrae in Extinct Malagasy Strepsirrhines.” American Journal of Physical Anthropology 128, no. 4: 823–839.
Slijper, E. J. 1946. “Comparative Biologic‐Anatomical Investigations on the Vertebral Column and Spinal Musculature of Mammals.” Verhandelingen Der Koninklijke Nederlandsche Akademie van Wetenschappen, Afd. Natuurkunde (Tweede Sectie) 42: 1–128.
Steinsaltz, D., A. Dahl, and K. W. Wachter. 2018. “Statistical Properties of Simple Random‐Effects Models for Genetic Heritability.” Electronic Journal of Statistics 12, no. 1: 321–358. https://doi.org/10.1214/17-EJS1386.
Stern, J. T., and C. E. Oxnard. 1973. “Primate Locomotion: Some Links With Evolution and Morphology.” In Primatologia, vol. 4, Basel, NY: S. Karger.
Susanna, I., D. M. Alba, S. Almécija, and S. Moyà‐Solà. 2014. “The Vertebral Remains of the Late Miocene Great Ape Hispanopithecus laietanus From Can Llobateres 2 (Vallès‐Penedès Basin, NE Iberian Peninsula).” Journal of Human Evolution 73: 15–34. https://doi.org/10.1016/j.jhevol.2014.05.009.
Tague, R. G. 2018. “Proximate Cause, Anatomical Correlates, and Obstetrical Implication of a Supernumerary Lumbar Vertebra in Humans.” American Journal of Physical Anthropology 165, no. 3: 444–456. https://doi.org/10.1002/ajpa.23361.
Turnquist, J. E., and M. J. Kessler. 1989. “Free‐Ranging Cayo Santiago Rhesus Monkeys (Macaca mulatta): I. Body Size, Proportion, and Allometry.” American Journal of Primatology 19, no. 1: 1–13. https://doi.org/10.1002/ajp.1350190102.
Vidal, P. P., W. Graf, and A. Berthoz. 1986. “The Orientation of the Cervical Vertebral Column in Unrestrained Awake Animals: I. Resting Position.” Experimental Brain Research 61, no. 3: 549–559. https://doi.org/10.1007/BF00237580.
Villamil, C. I., and E. R. Middleton. 2024. “Conserved Patterns and Locomotor‐Related Evolutionary Constraints in the Hominoid Vertebral Column.” Journal of Human Evolution 190: 103528. https://doi.org/10.1016/j.jhevol.2024.103528.
Visscher, P. M., W. G. Hill, and N. R. Wray. 2008. “Heritability in the Genomics Era—Concepts and Misconceptions.” Nature Reviews Genetics 9, no. 4: 255–266. https://doi.org/10.1038/nrg2322.
Wagner, G. P., and L. Altenberg. 1996. “Perspective: Complex Adaptations and the Evolution of Evolvability.” Evolution 50, no. 3: 967–976. https://doi.org/10.1111/j.1558-5646.1996.tb02339.x.
Ward, C. V. 1993. “Torso Morphology and Locomotion in Proconsul nyanzae.” American Journal of Physical Anthropology 92, no. 3: 291–328. https://doi.org/10.1002/ajpa.1330920306.
Ward, C. V., and B. Latimer. 2005. “Human Evolution and the Development of Spondylolysis.” Spine 30, no. 16: 1808–1814. https://doi.org/10.1097/01.brs.0000174273.85164.67.
Ward, C. V., A. Walker, and M. F. Teaford. 1991. “Proconsul Did Not Have a Tail.” Journal of Human Evolution 21: 215–220.
Welker, F., J. Ramos‐Madrigal, P. Gutenbrunner, et al. 2020. “The Dental Proteome of Homo antecessor.” Nature 580, no. 7802: 235–238. https://doi.org/10.1038/s41586-020-2153-8.
Wellik, D. M. 2009. “Chapter 9 Hox Genes and Vertebrate Axial Pattern.” In Current Topics in Developmental Biology. Vol.88, 257–278. Cambridge, MA: Academic Press. https://doi.org/10.1016/S0070-2153(09)88009-5.
West‐Eberhard, M. J. 1989. “Phenotypic Plasticity and the Origins of Diversity.” Annual Review of Ecology and Systematics 20: 249–278.
West‐Eberhard, M. J. 2003. Developmental Plasticity and Evolution. New York, NY: Oxford University Press.
Williams, S. A. 2012a. “Placement of the Diaphragmatic Vertebra in Catarrhines: Implications for the Evolution of Dorsostability in Hominoids and Bipedalism in Hominins.” American Journal of Physical Anthropology 148, no. 1: 111–122. https://doi.org/10.1002/ajpa.22049.
Williams, S. A. 2012b. “Variation in Anthropoid Vertebral Formulae: Implications for Homology and Homoplasy in Hominoid Evolution: VARIATION IN VERTEBRAL FORMULAE.” Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 318, no. 2: 134–147. https://doi.org/10.1002/jezb.21451.
Williams, S. A., E. R. Middleton, C. I. Villamil, and M. R. Shattuck. 2016. “Vertebral Numbers and Human Evolution.” American Journal of Physical Anthropology 159: 19–36. https://doi.org/10.1002/ajpa.22901.
Williams, S. A., and G. A. Russo. 2015. “Evolution of the Hominoid Vertebral Column: The Long and the Short of It.” Evolutionary Anthropology: Issues, News, and Reviews 24, no. 1: 15–32. https://doi.org/10.1002/evan.21437.
Williams, S. A., J. K. Spear, L. Petrullo, et al. 2019. “Increased Variation in Numbers of Presacral Vertebrae in Suspensory Mammals.” Nature Ecology & Evolution 3, no. 6: 949–956. Article 6. https://doi.org/10.1038/s41559-019-0894-2.
Willmore, K. E., C. C. Roseman, J. Rogers, J. M. Cheverud, and J. T. Richtsmeier. 2009. “Comparison of Mandibular Phenotypic and Genetic Integration Between Baboon and Mouse.” Evolutionary Biology 36, no. 1: 19–36. https://doi.org/10.1007/s11692-009-9056-9.
Zákány, J., M. Kmita, P. Alarcon, J.‐L. De La Pompa, and D. Duboule. 2001. “Localized and Transient Transcription of Hox Genes Suggests a Link Between Patterning and the Segmentation Clock.” Cell 106, no. 2: 207–217. https://doi.org/10.1016/S0092-8674(01)00436-6.

Auteurs

Catalina I Villamil (CI)

School of Chiropractic, Universidad Central del Caribe, Bayamón, Puerto Rico, USA.

Jeziel J Negrón (JJ)

School of Chiropractic, Universidad Central del Caribe, Bayamón, Puerto Rico, USA.
Department of Biology, University of Puerto Rico-Bayamón, Bayamón, Puerto Rico, USA.

Emily R Middleton (ER)

Department of Anthropology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin, USA.

Classifications MeSH