Loyola University Chicago

Department of Biology

Primate Systematics and Morphological Integration

We have been exploring the evolutionary bases for craniofacial morphological variation among primate species using phylogenetically-informed tests of the roles of genetic drift and natural selection as sources of interspecific morphological differentiation. This work
uses microevolutionary models of response to selection and genetic drift to interpret interspecific differences in craniofacial morphology. A key feature of these models relates to the patterns of morphological variation within species and the stability of these patterns over evolutionary time and taxonomic range. We have found that, in general, patterns of craniofacial morphological variation reflect patterns of functional and developmental relationships between traits and that these general patterns are consistent across primates. When possible, we have studied the heritable basis of morphological variation in these taxa. We have applied these evolutionary concepts to the differentiation of cranial morphology in the New World Monkeys among genera across the whole group and across species within genera. We discovered strong evidence for ecologically-driven size selection in the differentiation of New World Monkey genera and various combinations of genetic drift and selection for differences among taxa within genera. We are also applying these approaches to paleontological samples and to differentiation among the Old World Monkeys.

Collaborators

Dr. Becky Ackermann, University of Cape Town

Dr. Gabriel Marroig, University of Sao Paolo

Dr. Charles Roseman, University of Illinois

Grant Funding

Supported by NSF grant BCS-0725068

Publications on the Topic

Porto, A, H. Sebastião, S. E. Pavan, J. L. VandeBerg, G. Marroig and J. M.Cheverud. 2015. Rate of evolutionary change in cranial morphology of the marsupial genus Monodelphis is constrained by the availability of additive genetic variation. Journal of Evolutionary Biology 28:973-985.

Pavličev, M. and J. M. Cheverud. 2015. Constraints evolve: context-dependency of gene effects allows evolution of pleiotropy. Annual Review of Evolution, Ecology, and Systematics 46: (in press).

Schroeder, L., C.C. Roseman, J. M. Cheverud, R. R. Ackermann. 2014. Characterizing the evolutionary path(s) to early Homo. PLoS ONE 9(12): e114307. doi:10.1371/journal.pone.0114307

Ackermann, R. R., L. Schroeder, J. Rogers, and J. M. Cheverud. 2014. Further evidence for phenotypic signatures of hybridization in descendent baboon populations. Journal of Human Evolution 76: 54-62.

Atkinson, E. G., J. Rogers, M. C. Mahaney, L. A. Cox, and J. M. Cheverud. 2015. Cortical folding of the primate brain: An interdisciplinary examination of the genetic architecture, modularity, and evolvability of a significant neurological trait in pedigreed baboons (genus Papio). Genetics 200: 651-665.

Pelabon, C., G. H. Bolstad, C. K. Egset, J. M. Cheverud, M. Pavlicev and G. Rosenqvist. 2013. On the relationship between ontogenetic and static allometry. American Naturalist 181: 195-212.

Pavlicev, M., J. M. Cheverud, and G. P. Wagner. 2011. Evolution of adaptive phenotypic variation patterns by direct selection for evolvability. Proceedings of the Royal Society, B 278: 1903-1912, doi: 10.1098/rspb.2010.2113.

Marroig, G. and J. M. Cheverud. 2010. Size as a line of least resistance II: Direct selection on size or correlated response due to constraints? Evolution 64:1470-1488.

Pavlicev, M., G. P. Wagner and J. M. Cheverud. 2009. Measuring evolutionary constraints through the dimensionality of the phenotype: Adjusted bootstrap method to estimate rank of phenotypic covariance matrices. Evolutionary Biology, 36: 339-353.

Pavlicev, M., J. M. Cheverud and G. P Wagner. 2009. Measuring morphological integration using eigenvalue variance. Evolutionary Biology 36:157-170.

Wagner, G, Pavličev, M & Cheverud, J. (2007) 'The road to modularity', Nature Reviews Genetics, vol. 8, no. 12, pp. 921-931. doi:10.1038/nrg2267 [pdf]

Cheverud, J & Marroig, G. (2007) 'Comparing covariance matrices: Random Skewers method compared to the Common Principal Components model', Genetics and Molecular Biology, vol. 30, pp. 461-469. doi:10.1590/S1415-47572007000300027 [pdf]

Ackermann, R, Rogers, J & Cheverud, J. (2006) 'Identifying the morphological signatures of hybridization in primate and human evolution', Journal of Human Evolution, vol. 51, pp. 632-645. doi:10.1016/j.jhevol.2006.07.009 [pdf]

Marroig, G & Cheverud, J. (2005) 'Size as a line of least evolutionary resistance: Diet and adaptive morphological radiation in New World Monkeys', Evolution, vol. 59, pp. 1128-1142. doi:10.1111/j.0014-3820.2005.tb01049.x [pdf]

Harmon, L, Kolbe, J, Cheverud, J & Losos, J. (2005) 'Convergence and the multidimensional niche', Evolution, vol. 59, pp. 409-421. doi:10.1554/04-038 [pdf]

Ackermann, R & Cheverud, J. (2004) 'Detecting genetic drift versus selection in human evolution', Proceedings of the National Academy of Sciences, vol. 101, pp. 17946-17951. doi:10.1073/pnas.0405919102 [pdf]

Marroig, G & Cheverud, J. (2004) 'Cranial evolution in sakis (Pithecia, Platyrrhini) I: Interspecific differentiation and allometric patterns', American Journal of Physical Anthropology, vol. 125, pp. 266-278. doi:10.1002/ajpa.10421 [pdf]

Marroig, G & Cheverud, J. (2004) 'Did natural selection or genetic drift produce the cranial diversification of Neotropical monkeys?', American Naturalist, vol. 163, pp. 417-428. doi:10.1086/381693 [pdf]

Marroig, G, de Vivo, M & Cheverud, J. (2004) 'Cranial evolution in sakis (Pithecia, Platyrrhini) II: Evolutionary processes and morphological integration', Journal of Evolutionary Biology, vol. 17, pp. 144-155. doi:10.1046/j.1420-9101.2003.00653.x [pdf]

Marroig, G, Cropp, S & Cheverud, J. (2004) 'Systematics and evolution of the Jacchus group of marmosets', American Journal of Physical Anthropology, vol. 123, pp. 11-22. doi:10.1002/ajpa.10146 [pdf]

Cheverud, J. (2004) 'Darwinian evolution by the natural selection of heritable variation: Definition of parameters and application to social behaviors', In: The origins and nature of sociality, Sussman, R, Chapman, A (eds.), Aldine Publishing, New York, pp. 140-157.

Ackermann, R & Cheverud, J. (2004) 'Morphological integration in primate evolution', In: Phenotypic integration: Studying and ecology and evolution of complex phenotypes, Pigliucci, M & Preston, K (eds.), Oxford University Press, Oxford, pp. 302-319. [pdf]

Ackermann, R & Cheverud, J. (2002) 'Discerning evolutionary processes in patterns of tamarin (genus Saguinus) craniofacial variation', American Journal of Physical Anthropology, vol. 117, pp. 260-271. doi:10.1002/ajpa.10038 [pdf]

Smith, R & Cheverud, J. (2002) 'Scaling of sexual dimorphism in body mass: A phylogenetic analysis of Rensch's rule in Primates', International Journal of Primatology, vol. 23, pp. 1095-1135. doi:10.1023/A:1019654100876 [pdf]

Marroig, G & Cheverud, J. (2001) 'A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology and ontogeny during cranial evolution of New World Monkeys', Evolution, vol. 55, pp. 2576-2600. doi:10.1111/j.0014-3820.2001.tb00770.x [pdf]

Kohn, L, Langston, L & Cheverud, J. (2001) 'Subspecific genetic differences in the saddle-back tamarin (Saguinus fuscicollis) postcranial skeleton', American Journal of Primatology, vol. 54, pp. 41-56. doi:10.1002/ajp.1011 [pdf]

Ackermann, R & Cheverud, J. (2000) 'Phenotypic covariance structure in tamarins (genus Saguinus): A comparison of variation patterns using matrix correlations and common principal comoponent analysis', American Journal of Physical Anthropology, vol. 111, pp. 489-501. wiley:71001162 [pdf]

Cropp, S, Larson, A & Cheverud, J. (1999) 'Historical biogeography of the tamarins, Genus Saguinus: The molecular phylogenetic evidence', American Journal of Physical Anthropology, vol. 108, pp. 65-89. wiley:30001800 [pdf]

Kohn, L, Olson, P & Cheverud, J. (1997) 'Age of epiphyseal closure in tamarins and marmosets', American Journal of Primatology, vol. 41, pp. 129-139. doi:10.1002/(SICI)1098-2345(1997)41:2<129::AID-AJP5>3.0.CO;2-Z [pdf]

Cheverud, J. (1996) 'Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins', Journal of Evolutionary Biology, vol. 9, pp. 5-42. doi:10.1046/j.1420-9101.1996.9010005.x [pdf]

Jacobs, S, Larson, A & Cheverud, J. (1995) 'Phylogenetic relationships and orthogenetic evolution of coat color among tamarins (genus Saguinus)', Systematic Biology, vol. 44, pp. 515-532. doi:10.2307/2413658 [pdf]

Hutchison, D & Cheverud, J. (1995) 'Fluctuating asymmetry in tamarin (Saguinus) cranial morphology: Intra- and interspecific comparisons between taxa with varying levels of genetic heterozygosity', Journal of Heredity, vol. 86, pp. 280-288. pmid:7657996 [pdf]

Cheverud, J. (1995) 'Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium', American Naturalist, vol. 145, pp. 63-89. doi:10.1086/285728 [pdf]

Cheverud, J, Routman, E, Jaquish, C, Tardif, S, Peterson, G, Belfiore, N & Forman, L. (1994) 'Quantitative and molecular genetic variation in captive cotton-top tamarins (Saguinus oedipus)', Conservation Biology, vol. 8, pp. 95-105. doi:10.1046/j.1523-1739.1994.08010095.x [pdf]

Richtsmeier, J, Corner, B, Grausz, H, Cheverud, J & Danahey, S. (1993) 'The role of postnatal growth pattern in the production of facial morphology', Systematic Biology, vol. 42, pp. 307-330. doi:10.2307/2992466 [pdf]

Cheverud, J, Jacobs, S & Moore, A. (1993) 'Genetic differences among subspecies of the Saddle-back Tamarin (Saguinus fuscicollis): Evidence from hybrids', American Journal of Primatology, vol. 31, pp. 23-39. doi:10.1002/ajp.1350310104

Richtsmeier, J, Cheverud, J, Dahaney, S, Corner, B & Lele, S. (1993) 'Sexual dimorphism of ontogeny in the crab-eating macaque (Macaca fascicularis)', Journal of Human Evolution, vol. 25, pp. 1-30.

Cheverud, J, Dittus, W & Wilson, P. (1992) 'Primate population studies at Polonnaruwa. III. Somatometric growth in a natural population of toque macaques (Macaca sinica)', Journal of Human Evolution, vol. 23, pp. 51-78. doi:10.1016/0047-2484(92)90043-9

Moore, A & Cheverud, J. (1992) 'Systematics of the Saguinus oedipus group of the bare-face tamarins: Evidence from facial morphology', American Journal of Physical Anthropology, vol. 89, pp. 73-84. doi:10.1002/ajpa.1330890107 [pdf]

Cheverud, J & Dittus, W. (1992) 'Primate population studies at Polonnaruwa. II. Heritability of body measurements in a natural population of toque macaques (Macaca sinica)', American Journal of Primatology, vol. 27, no. 2, pp. 145-154. doi:10.1002/ajp.1350270209

Konigsberg, L & Cheverud, J. (1992) 'Uncertain paternity in primate quantitative genetic studies', American Journal of Primatology, vol. 27, pp. 133-144. doi:10.1002/ajp.1350270208

Richtsmeier, J, Cheverud, J & Lele, S. (1992) 'Advances in anthropological morphometrics', Annual Reviews in Anthropology, vol. 21, pp. 283-305. doi:10.1146/annurev.an.21.100192.001435 [pdf]

Leigh, S & Cheverud, J. (1991) 'Sexual dimorphism in the baboon facial skeleton', American Journal of Physical Anthropology, vol. 84, pp. 193-208. pmid:2021194

Cheverud, J & Moore, A. (1990) 'Subspecific morphological variation in the saddle-back tamarin (Saguinus fuscicollis)', American Journal of Primatology, vol. 21, pp. 1-16. doi:10.1002/ajp.1350210102

Cheverud, J. (1990) 'The evolution of morphological variation patterns', In: Evolutionary innovations, Nitecki, M (ed.), University of Chicago Press, Chicago, IL, pp. 133-146.

Cheverud, J, Wagner, G & Dow, M. (1989) 'Methods for the comparative analysis of variation patterns', Systematic Zoology, vol. 38, pp. 201-213. doi:10.2307/2992282 [pdf]

Cheverud, J. (1989) 'A comparative analysis of morphological variation patterns in the papionins', Evolution, vol. 43, pp. 1737-1747. doi:10.2307/2409389 [pdf]

Cheverud, J. (1989) 'Evolution of morphological integration', In: Trends in Vertebrate Morphology, Proceedings of the 2nd International Symposium on Vertebrate Morphology, Fortschritte der Zoologie, vol. 35, Gustav Fisher Verlag, New York, pp. 196-197.

Cheverud, J. (1988) 'The evolution of genetic correlation and developmental constraints', In: Population Genetics and Evolution, de Jong, G (ed.), Springer-Verlag, Berlin, pp. 94-101.

Cheverud, J. (1988) 'A comparison of genetic and phenotypic correlations', Evolution, vol. 42, pp. 958-968. doi:10.2307/2408911 [pdf]

Cheverud, J, Dow, M & Leutenegger, W. (1986) 'A phylogenetic autocorrelation analysis of sexual dimorphism in primates', American Anthropologist, vol. 88, pp. 916-922. doi:10.1525/aa.1986.88.4.02a00090 [pdf]

Cheverud, J, Dow, M & Leutenegger, W. (1985) 'The quantitative assessment of phylogenetic constraints in comparative analyses: Sexual dimorphism in body weight among primates', Evolution, vol. 39, pp. 1335-1351. doi:10.2307/2408790 [pdf]

Richtsmeier, J, Cheverud, J & Buikstra, J. (!984) 'The relationship between cranial metric and nonmetric traits in the rhesus macaques from Cayo Santiago', American Journal of Physical Anthropology, vol. 64, pp. 213-222. doi:10.1002/ajpa.1330640303 [pdf]

McGrath, J, Cheverud, J & Buikstra, J. (1984) 'Genetic correlations between sides and heritability of asymmetry for nonmetric traits in rhesus macaques on Cayo Santiago', American Journal of Physical Anthropology, vol. 64, pp. 401-412. doi:10.1002/ajpa.1330640405 [pdf]

Cheverud, J. (1984) 'Quantitative genetics and developmental constraints on evolution by selection', Journal of Theoretical Biology, vol. 110, pp. 155-172. doi:10.1016/S0022-5193(84)80050-8 [pdf]

Cheverud, J. (1982) 'Phenotypic, genetic, and environmental morphological integration in the cranium', Evolution, vol. 36, pp. 499-516. doi:10.2307/2408096 [pdf]

Leutenegger, W & Cheverud, J. (1982) 'Correlates of sexual dimorphism in primates', International Journal of Primatology, vol. 3, no. 4, pp. 387-402. doi:10.1007/BF02693740 [pdf]

Cheverud, J. (1982) 'Relationships among ontogenetic, static, and evolutionary allometry', American Journal of Physical Anthropology, vol. 59, pp. 139-149. doi:10.1002/ajpa.1330590204 [pdf]

Cheverud, J & Buikstra, J. (1982) 'Quantitative genetics of skeletal non-metric traits in the rhesus macaques on Cayo Santiago. III. Relative heritability of skeletal non-metric and metric traits', American Journal of Physical Anthropology, vol. 59, pp. 151-155. doi:10.1002/ajpa.1330590205 [pdf]

Cheverud, J & Buikstra, J. (1981) 'Quantitative genetics of skeletal non-metric traits in the rhesus macaques on Cayo Santiago. I. Single trait heritabilities', American Journal of Physical Anthropology, vol. 54, pp. 43-49. doi:10.1002/ajpa.1330540106 [pdf]

Cheverud, J & Buikstra, J. (1981) 'Quantitative genetics of skeletal non-metric traits in the rhesus macaques on Cayo Santiago. II. Phenotypic, genetic, and environmental correlations between traits', American Journal of Physical Anthropology, vol. 54, pp. 51-58. doi:10.1002/ajpa.1330540107 [pdf]

Cheverud, J. (1981) 'Variation in highly and lowly heritable morphological traits among social groups of rhesus macaques (Macaca mulatta) on Cayo Santiago', Evolution, vol. 35, pp. 75-83. doi:10.2307/2407943 [pdf]