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Integration and Evolvability in Primate Hands and Feet

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Abstract

Morphological integration theory predicts that sets of phenotypic traits that covary strongly due to developmental and/or functional connections between them eventually co-evolve because of a coordinated response to selection, and accordingly become less independently evolvable. This process is not irreversible, however, and phenotypic traits can become less integrated, and hence more independently evolvable, in the context of selection for divergent functions and morphologies. This study examines the reciprocal relationship between shared function, integration and evolvability by comparing integration patterns among serially homologous skeletal elements in the hands and feet of a functionally diverse sample of catarrhine primates. Two hypotheses are tested: (1) species in which the autopods are functionally more similar (e.g. quadrupedal monkeys) have more strongly integrated autopods than species in which the autopods are functionally divergent (e.g. gibbons, humans) and (2) the latter have autopods that are more evolvable, collectively and independently. Morphometric data from selected hand and foot digital rays were used to derive phenotypic variance/covariance matrices. The strength of integration among autopods was quantified using eigenanalysis and a measure of trait variational autonomy. Evolvability was estimated by subjecting phenotypic variance/covariance matrices to simulated random selection gradients, and comparing evolutionary responses among species. Results indicate that integration decreases as hands and feet become functionally divergent, and that the strongly integrated hand and foot skeletons of quadrupedal monkeys respond to selection in a highly collinear manner, even when simulated selective pressures acting on each autopod are in opposite directions in phenotypic space. Results confirm that the evolvability of morphological traits depends largely on how strongly they covary with other traits, but also with body size. The role of pleiotropy as a developmental mechanism underlying integration and evolvability is also discussed.

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References

  • Ackermann, R. R., & Cheverud, J. M. (2000). Phenotypic covariance structure in tamarins (genus Saguinus): A comparison of variation patterns using matrix correlation and common principal component analysis. American Journal of Physical Anthropology, 111, 489–501. doi:10.1002/(SICI)1096-8644(200004)111:4<489::AID-AJPA5>3.0.CO;2-U.

    Article  PubMed  CAS  Google Scholar 

  • Ackermann, R. R., & Cheverud, J. M. (2004). Detecting genetic drift versus selection in human evolution. Proceedings of the National Academy of Sciences of the United States of America, 101, 17946–17951. doi:10.1073/pnas.0405919102.

    Article  PubMed  CAS  Google Scholar 

  • Cannon, C. H., & Leighton, M. (1994). Comparative locomotor ecology of gibbons and macaques—selection of canopy elements for crossing gaps. American Journal of Physical Anthropology, 93, 505–524. doi:10.1002/ajpa.1330930409.

    Article  PubMed  CAS  Google Scholar 

  • Cant, J. G. H. (1987). Positional behavior of female Bornean orangutans (Pongo pygmaeus). American Journal of Primatology, 12, 71–90. doi:10.1002/ajp.1350120104.

    Article  Google Scholar 

  • Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution: International Journal of Organic Evolution, 36, 499–516. doi:10.2307/2408096.

    Google Scholar 

  • Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution: International Journal of Organic Evolution, 42, 958–968. doi:10.2307/2408911.

    Google Scholar 

  • Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145, 63–89. doi:10.1086/285728.

    Article  Google Scholar 

  • Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44–50.

    Google Scholar 

  • Cheverud, J. M., & Marroig, G. (2007). Comparing covariance matrices: Random skewers method compared to the common principal components model. Genetics and Molecular Biology, 30, 461–469. doi:10.1590/S1415-47572007000300027.

    Article  Google Scholar 

  • Darwin, C. (1859). On the origin of species by means of natural selection. London: J. Murray.

    Google Scholar 

  • Darwin, C. (1871). The descent of man and selection in relation to sex. New York: D. Appleton and company.

    Google Scholar 

  • Doran, D. (1997). Ontogeny of locomotion in mountain gorillas and chimpanzees. Journal of Human Evolution, 32, 323–344.

    Google Scholar 

  • Fleagle, J. G. (1999). Primate adaptation and evolution. San Diego: Academic Press.

    Google Scholar 

  • Gebo, D. L., & Chapman, C. A. (1995). Positional behavior in 5 sympatric old-world monkeys. American Journal of Physical Anthropology, 97, 49–76. doi:10.1002/ajpa.1330970105.

    Article  PubMed  CAS  Google Scholar 

  • Gebo, D. L., & Sargis, E. J. (1994). Terrestrial adaptations in the postcranial skeletons of guenons. American Journal of Physical Anthropology, 93, 341–371. doi:10.1002/ajpa.1330930306.

    Article  PubMed  CAS  Google Scholar 

  • Hall, B. K. (1995). Homology and embryonic development. In “Evolutionary Biology Vol 28”, 28, 1–37.

    CAS  Google Scholar 

  • Hallgrimsson, B., & Maiorana, V. (2000). Variability and size in mammals and birds. Biological Journal of the Linnean Society. Linnean Society of London, 70, 571–595. doi:10.1111/j.1095-8312.2000.tb00218.x.

    Article  Google Scholar 

  • Hallgrimsson, B., Willmore, K., & Hall, B. (2002). Canalization, developmental stability, and morphological integration in primate limbs. Yearbook of Physical Anthropology, 45, 131–158. doi:10.1002/ajpa.10182.

    Article  Google Scholar 

  • Hansen, T. F. (2003). Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Bio Systems, 69, 83–94. doi:10.1016/S0303-2647(02)00132-6.

    PubMed  Google Scholar 

  • Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201–1219. doi:10.1111/j.1420-9101.2008.01573.x.

    Article  PubMed  CAS  Google Scholar 

  • Hunt, K. D., Cant, J. G. H., Gebo, D. L., Rose, M. D., Walker, S. E., & Youlatos, D. (1996). Standardized descriptions of primate locomotor and postural modes. Primates, 37, 363–387. doi:10.1007/BF02381373.

    Article  Google Scholar 

  • Isbell, L. A., Pruetz, J. D., Lewis, M., & Young, T. P. (1998). Locomotor activity differences between sympatric patas monkeys (Erythrocebus patas) and vervet monkeys (Cercopithecus aethiops): Implications for the evolution of long hindlimb length in Homo. American Journal of Physical Anthropology, 105, 199–207. doi:10.1002/(SICI)1096-8644(199802)105:2<199::AID-AJPA7>3.0.CO;2-Q.

    Article  PubMed  CAS  Google Scholar 

  • Jouffroy, F. K., Godinot, M., & Nakano, Y. (1991). Biometrical characteristics of primate hands. Human Evolution, 6, 269–306. doi:10.1007/BF02437254.

    Article  Google Scholar 

  • Jungers, W. L., Falsetti, A. B., & Wall, C. E. (1995). Shape, relative size, and size adjustments in morphometrics. Yearbook of Physical Anthropology, 38, 137–161. doi:10.1002/ajpa.1330380608.

    Article  Google Scholar 

  • Khan, P., Linkhart, B., & Simon, H. (2002). Different regulation of T-box genes Tbx4 and Tbx5 during limb development and limb regeneration. Developmental Biology, 250, 383–392.

    PubMed  CAS  Google Scholar 

  • Lande, R. (1979). Quantitative genetic-analysis of multivariate evolution, applied to brain—body size allometry. Evolution: International Journal of Organic Evolution, 33, 402–416. doi:10.2307/2407630.

    Google Scholar 

  • Lande, R. (1980). The genetic covariance between characters maintained by pleiotropic mutations. Genetics, 94, 203–215.

    PubMed  Google Scholar 

  • Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution: International Journal of Organic Evolution, 37, 1210–1226. doi:10.2307/2408842.

    Google Scholar 

  • Lleonart, J., Salat, J., & Torres, G. J. (2000). Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205, 85–93. doi:10.1006/jtbi.2000.2043.

    Article  PubMed  CAS  Google Scholar 

  • Magwene, P., & Chernoff, B. (1999). Morphological integration: Forty years later. In E. Olson & R. Miller (Eds.), Morphological integration (pp. 319–353). Chicago: University of Chicago Press.

    Google Scholar 

  • Manly, B. F. J. (1991). Randomization and Monte Carlo methods in biology. London: Chapman and Hall.

    Google Scholar 

  • Margulies, E. H., Kardia, S. L. R., & Innis, J. W. (2001). A comparative molecular analysis of developing mouse forelimbs and hindlimbs using Serial Analysis of Gene Expression (SAGE). Genome Research, 11, 1686–1698. doi:10.1101/gr.192601.

    Article  PubMed  CAS  Google Scholar 

  • Marroig, G., & Cheverud, J. M. (2004). Cranial evolution in sakis (Pithecia, Platyrrhini) I: Interspecific differentiation and allometric patterns. American Journal of Physical Anthropology, 125, 266–278.

    Google Scholar 

  • Marroig, G., & Cheverud, J. M. (2005). Size as a line of least evolutionary resistance: Diet and adaptive morphological radiation in New World monkeys. Evolution: International Journal of Organic Evolution, 59, 1128–1142.

    Google Scholar 

  • McFadden, D., & Bracht, M. S. (2003). The relative lengths and weights of metacarpals and metatarsals in baboons (Papio hamadryas). Hormones and Behavior, 43, 347–355. doi:10.1016/S0018-506X(02)00048-X.

    Article  PubMed  Google Scholar 

  • McFadden, D., & Bracht, M. S. (2005). Sex differences in the relative lengths of metacarpals and metatarsals in gorillas and chimpanzees. Hormones and Behavior, 47, 99–111. doi:10.1016/j.yhbeh.2004.08.013.

    Article  PubMed  Google Scholar 

  • Menke, D. B., Guenther, C., & Kingsley, D. M. (2008). Dual hindlimb control elements in the Tbx4 gene and region-specific control of bone size in vertebrate limbs. Development, 135, 2543–2553. doi:10.1242/dev.017384.

    Article  PubMed  CAS  Google Scholar 

  • Olson, E. C., & Miller, R. L. (1951). A mathematical model applied to a study of the evolution of species. Evolution: International Journal of Organic Evolution, 5, 325–338. doi:10.2307/2405677.

    Google Scholar 

  • Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.

    Google Scholar 

  • Page, S. L., & Goodman, M. (2001). Catarrhine phylogeny: Noncoding DNA evidence for a diphyletic origin of the mangabeys and for a human-chimpanzee clade. Molecular Phylogenetics and Evolution, 18, 14–25. doi:10.1006/mpev.2000.0895.

    Article  PubMed  CAS  Google Scholar 

  • Pavlicev, M., Kenney-Hunt, J. P., Norgard, E. A., Roseman, C. C., Wolf, J. B., & Cheverud, J. M. (2008). Genetic variation in pleiotropy: Differential epistasis as a source of variation in the allometric relationship between long bone lengths and body weight. Evolution: International Journal of Organic Evolution, 62, 199–213.

    Google Scholar 

  • Porto, A., de Oliveira, F. B., Shirai, L. T., De Conto, V., & Marroig, G. (2009). The evolution of modularity in the mammalian skull I: Morphological integration patterns and magnitudes. Evolutionary Biology. doi:10.1007/s11692-008-9038-3.

  • Rallis, C., Bruneau, B. G., Del Buono, J., Seidman, C. E., Seidman, J. G., Nissim, S., et al. (2003). Tbx5 is required for forelimb bud formation and continued outgrowth. Development, 130, 2741–2751. doi:10.1242/dev.00473.

    Article  PubMed  CAS  Google Scholar 

  • Remis, M. (1995). Effects of body-size and social-context on the arboreal activities of lowland gorillas in the Central-African-Republic. American Journal of Physical Anthropology, 97, 413–433. doi:10.1002/ajpa.1330970408.

    Article  PubMed  CAS  Google Scholar 

  • Ripley, S. (1967). Leaping of Langurs—a problem in study of locomotor adaptation. American Journal of Physical Anthropology, 26, 149. doi:10.1002/ajpa.1330260206.

    Article  Google Scholar 

  • Roff, D. A. (1995). The estimation of genetic correlations from phenotypic correlations—a test of Cheverud’s conjecture. Heredity, 74, 481–490. doi:10.1038/hdy.1995.68.

    Article  Google Scholar 

  • Roff, D. A. (1996). The evolution of genetic correlations: An analysis of patterns. Evolution: International Journal of Organic Evolution, 50, 1392–1403. doi:10.2307/2410877.

    Google Scholar 

  • Rohlf, F. J. (2005). TPSDig2. Stony Brook: State University of New York.

    Google Scholar 

  • Rose, M. D. (1988). Functional anatomy of the cheiridia. In J. H. Schwartz (Ed.), Orangutan biology (pp. 299–310). Oxford: Oxford University Press.

    Google Scholar 

  • Rudel, D., & Sommer, R. J. (2003). The evolution of developmental mechanisms. Developmental Biology, 264, 15–37. doi:10.1016/S0012-1606(03)00353-1.

    Article  PubMed  CAS  Google Scholar 

  • Ruvinsky, I., & Gibson-Brown, J. J. (2000). Genetic and developmental bases of serial homology in vertebrate limb evolution. Development, 127, 5233–5244.

    PubMed  CAS  Google Scholar 

  • Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution: International Journal of Organic Evolution, 50, 1766–1774. doi:10.2307/2410734.

    Google Scholar 

  • Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jonsson, B., et al. (2004). Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature, 428, 717–723. doi:10.1038/nature02415.

    Article  PubMed  CAS  Google Scholar 

  • Shou, S. M., Scott, V., Reed, C., Hitzemann, R., & Stadler, H. S. (2005). Transcriptome analysis of the murine forelimb and hindlimb autopod. Developmental Dynamics, 234, 74–89. doi:10.1002/dvdy.20514.

    Article  PubMed  CAS  Google Scholar 

  • Stern, J. T., & Oxnard, C. (1973). Primate locomotion: Some links with evolution and morphology. Primatologia, 4, 1–93.

    Google Scholar 

  • Strasser, E. (1994). Relative development of the hallux and pedal digit formulas in Cercopithecidae. Journal of Human Evolution, 26, 413–440. doi:10.1006/jhev.1994.1026.

    Article  Google Scholar 

  • Susman, R. L. (1979). Comparative and functional morphology of hominoid fingers. American Journal of Physical Anthropology, 50, 215–236. doi:10.1002/ajpa.1330500211.

    Article  PubMed  CAS  Google Scholar 

  • Tosi, A. J., Melnick, D. J., & Disotell, T. R. (2004). Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini). Journal of Human Evolution, 46, 223–237. doi:10.1016/j.jhevol.2003.11.006.

    Article  PubMed  Google Scholar 

  • Wagner, G. P. (1984). On the eigenvalue distribution of genetic and phenotypic dispersion matrices—evidence for a nonrandom organization of quantitative character variation. Journal of Mathematical Biology, 21, 77–95.

    Google Scholar 

  • Wagner, G. P. (1990). A comparative study of morphological integration in Apis mellifera (Insecta, Hymenoptera). Zeitschrift fur Zoologische Systematik und Evolutionsforschung, 28, 48–61.

    Google Scholar 

  • Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36–43.

    Google Scholar 

  • Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution: International Journal of Organic Evolution, 50, 967–976. doi:10.2307/2410639.

    Google Scholar 

  • Wells, J. P., & Turnquist, J. E. (2001). Ontogeny of locomotion in rhesus macaques (Macaca mulatta): II. Postural and locomotor behavior and habitat use in a free-ranging colony. American Journal of Physical Anthropology, 115, 80–94. doi:10.1002/ajpa.1059.

    Article  PubMed  CAS  Google Scholar 

  • Wilkins, A. S. (2002). The evolution of developmental pathways. Sunderland: Sinauer Associates.

    Google Scholar 

  • Willis, J. H., Coyne, J. A., & Kirkpatrick, M. (1991). Can one predict the evolution of quantitative characters without genetics? Evolution: International Journal of Organic Evolution, 45, 441–444. doi:10.2307/2409678.

    Google Scholar 

  • Young, N. M., & Hallgrimsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution: International Journal of Organic Evolution, 59, 2691–2704.

    Google Scholar 

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Acknowledgements

Thanks to my co-organizer Kat Willmore, who helped put together the AAPA symposium at which some of these results were presented. Thanks also to Benedikt Hallgrimsson, for the opportunity to publish proceedings from the symposium in a special issue of the journal Evolutionary Biology. This research was supported by a National Science Foundation Doctoral Dissertation Improvement Grant (BCS 0647624) and a Canadian Natural Sciences and Engineering Research Council Postgraduate Scholarship. I am grateful to J. Chupasko (Museum of Comparative Zoology), D. Dunbar and T. Kensler (Laboratory for Primate Morphology and Genetics, University of Puerto Rico), L. Jellema (Cleveland Museum of Natural History), L. Gordon and D. Hunt (National Museum of Natural History), E. Westwig (American Museum of Natural History), M. Tappen and J. Soderberg (University of Minnesota), S. Leigh and J. Polk (University of Illinois - Urbana-Champaign), M. Harman (Powell-Cotton Museum), D. Hills (Natural History Museum, London), M. Hiermeier (Bavarian Zoological State Collection) and L. Shapiro (University of Texas—Austin) for providing access to specimens in their care. Finally, thanks to my dissertation committee members, D. Lieberman, D. Pilbeam, G. Lauder and B. Hallgrimsson, for helping me through the design, implementation and analysis of this project, and for reading earlier incarnations of the manuscript.

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  1. Department of Cell Biology and Anatomy, University of Calgary, G503 - 3330 Hospital Drive NW, Calgary, AB, T2N4N1, Canada

    Campbell Rolian

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Rolian, C. Integration and Evolvability in Primate Hands and Feet. Evol Biol 36, 100–117 (2009). https://doi.org/10.1007/s11692-009-9049-8

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