Skip to main content
Log in

Quantitative Genetics and Modularity in Cranial and Mandibular Morphology of Calomys expulsus

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Patterns of genetic covariance between characters (represented by the covariance matrix \({\varvec{G}}\)) play an important role in morphological evolution, since they interact with the evolutionary forces acting over populations. They are also expected to influence the patterns expressed in their phenotypic counterparts \(({\varvec{P}})\), because of limits imposed by multiple developmental and functional restrictions on the genotype/phenotype map. We have investigated genetic covariances in the skull and mandible of the vesper mouse (Calomys expulsus) in order to estimate the degree of similarity between genetic and phenotypic covariances and its potential roots on developmental and functional factors shaping those integration patterns. We use a classic ad hoc analysis of morphological integration based on current state of art of developmental/functional factors during mammalian ontogeny and also applied a novel methodology that makes use of simulated evolutionary responses. We have obtained \({\varvec{P}}\) and \({\varvec{G}}\) that are strongly similar, for both skull and mandible; their similarity is achieved through the spatial and temporal organization of developmental and functional interactions, which are consistently recognized as hypothesis of trait associations in both matrices.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams, D. C., Cardini, A., Monteiro, L. R., O’Higgins, P., & Rohlf, F. J. (2011). Morphometrics and phylogenetics: Principal components of shape from cranial modules are neither appropriate nor effective cladistic characters. Journal of Human Evolution, 60(2), 240–243. doi:10.1016/j.jhevol.2010.02.003.

    Article  CAS  PubMed  Google Scholar 

  • Almeida, F. C., Bonvicino, C. R., & Cordeiro-Estrela, P. (2007). Phylogeny and temporal diversification of calomys (rodentia, sigmodontinae): Implications for the biogeography of an endemic genus of the open/dry biomes of South America. Molecular Phylogenetics and Evolution, 42(2), 449–466. doi:10.1016/j.ympev.2006.07.005.

    Article  CAS  PubMed  Google Scholar 

  • Atchley, W. R., & Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Reviews, 66, 101–157.

    Article  CAS  PubMed  Google Scholar 

  • Berner, D. (2012). How much can the orientation of g’s eigenvectors tell us about genetic constraints? Ecology and Evolution, 2(8), 1834–1842. doi:10.1002/ece3.306.

    Article  PubMed Central  PubMed  Google Scholar 

  • Berner, D., Kaeuffer, R., Grandchamp, A. C., Raeymaekers, J. A. M., Räsänen, K., & Hendry, A. P. (2011). Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: Implications for reproductive isolation. Journal of Evolutionary Biology, 1–9. doi:10.1111/j.1420-9101.2011.02330.x.

  • Bonvicino, C., Lima, J., & Almeida, F. (2003). A new species of calomys waterhouse (rodentia, Sigmodontinae) from the cerrado of central brazil. Revista Brasileira de Zoologia, 20(2), 301–307.

    Article  Google Scholar 

  • Bonvicino, C. R., & Almeida, F. C. (2000). Karyotype, morphology and taxonomic status of calomys expulsus (rodentia: Sigmodontinae). Mammalia, 64, 339–351.

    Article  Google Scholar 

  • Bookstein, F. L. (1991). Morphometric tools for landmark data: Geometry and biology. Cambridge: Cambridge University Press.

    Google Scholar 

  • Bookstein, F. L., Chernoff, B., Elder, R., & Strauss, R. (1985). Morphometrics in evolutionary biology. Philadelphia: The Academy of Natural Sciences of Philadelphia.

    Google Scholar 

  • Cheverud, J. M. (1984). Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155–172.

    Article  CAS  PubMed  Google Scholar 

  • Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution, 42(5), 958–968.

    Article  Google Scholar 

  • Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145(1), 63–89.

    Article  Google Scholar 

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

    Google Scholar 

  • Cheverud, J. M. (2006). Modular pleiotropic effects of quantitative trait loci on morphological traits. In G. Schlosser & G. P. Wagner (Eds.), Modularity in development and evolution (1st ed., pp. 132–153). Chicago: The University of Chicago Press.

    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 

  • Cheverud, J. M., Routman, E. J., & Irschick, D. J. (1997). Pleiotropic effects of individual gene loci on mandibular morphology. Evolution, 51(6), 2006–2016.

    Article  Google Scholar 

  • Cheverud, J. M., Wagner, G. P., & Dow, M. M. (1989). Methods for the comparative analysis of variation patterns. Evolution, 38(3), 201–213.

    Google Scholar 

  • Dochtermann, N. A. (2011). Testing cheverud’s conjecture for behavioral correlations and behavioral syndromes. Evolution, 65(6), 1814–1820. doi:10.1111/j.1558-5646.2011.01264.x.

    Article  PubMed  Google Scholar 

  • Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis. New York: Wiley.

    Google Scholar 

  • Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics (4th ed.). Harlow, Essex: Addison Wesley Longman.

    Google Scholar 

  • Franz-Odendaal, T. A. (2011). Epigenetics in bone and cartilage development. In B. Hallgrímsson & B. K. Hall (Eds.), Epigenetics: Linking genotype and phenotype in development and evolution (1st ed., pp. 195–220). Oakland, CA: University of California Press.

    Google Scholar 

  • Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., et al. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36(4), 355–376. doi:10.1007/s11692-009-9076-5.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hallgrímsson, B., & Lieberman, D. E. (2008). Mouse models and the evolutionary developmental biology of the skull. Integrative and Comparative Biology, 48(3), 373–384. doi:10.1093/icb/icn076.

    Article  PubMed  Google Scholar 

  • Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21(5), 1201–1219. doi:10.1111/j.1420-9101.2008.01573.x.

    Article  CAS  PubMed  Google Scholar 

  • Herring, S. W. (2011). Muscle-bone interactions and the development of skeletal phenotype. In B. Hallgrímsson & B. K. Hall (Eds.), Epigenetics: Linking genotype and phenotype in development and evolution (1st ed., pp. 221–237). Oakland, CA: University of California Press.

    Google Scholar 

  • Hershkovitz, P. (1962). Evolution of neotropical cricetine rodents (muridae) with special reference to the phyllotine group. Fieldiana: Zoology, 46, 1–524.

    Google Scholar 

  • Hill, W. G., & Thompson, R. (1978). Probabilities of non-positive definite between-group or genetic covariance matrices. Biometrics, 34(3), 429–439.

    Article  Google Scholar 

  • Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology, Evolution, and Systematics, 39(1), 115–132. doi:10.1146/annurev.ecolsys.37.091305.110054.

    Article  Google Scholar 

  • Klingenberg, C. P., & Leamy, L. J. (2001). Quantitative genetics of geometric shape in the mouse mandible. Evolution, 55, 2342–2352.

    Article  CAS  PubMed  Google Scholar 

  • Klingenberg, C. P., Leamy, L. J., & Cheverud, J. M. (2004). Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics, 166, 1909–1921.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krupinski, P., Chickarmane, V., & Peterson, C. (2011). Simulating the mammalian blastocyst-molecular and mechanical interactions pattern the embryo. PLoS Computational Biology, 7(5), e1001,128. doi:10.1371/journal.pcbi.1001128.

    Article  CAS  Google Scholar 

  • Lande, R. (1979). Quantitative genetic analysis of multivariate evolution applied to brain: body size allometry. Evolution, 33(1), 402–416.

    Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leamy, L. J., Routman, E. J., & Cheverud, J. M. (1999). Quantitative trait loci for early and late developing skull characters in mice: A test of the genetic independence model of morphological integration. The American Naturalist, 153, 201–214. doi:10.1086/303165.

    Article  Google Scholar 

  • Lessels, C. M., & Boag, P. T. (1987). Unrepeatable repeatabilities: A common mistake. The Auk, 2, 116–121.

    Article  Google Scholar 

  • Linde, Kvd, & Houle, D. (2009). Inferring the nature of allometry from geometric data. Evolutionary Biology, 36(3), 311–322. doi:10.1007/s11692-009-9061-z.

    Article  Google Scholar 

  • Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits. Sunderland: Sinauer Associates.

    Google Scholar 

  • Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.

    CAS  PubMed  Google Scholar 

  • Marroig, G., & Cheverud, J. M. (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, 55(12), 2576–2600.

    Article  CAS  PubMed  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, 59(5), 1128–1142.

    Article  PubMed  Google Scholar 

  • Marroig, G., de Vivo, M., & Cheverud, J. M. (2004). Cranial evolution in sakis (Pithecia, Platyrrhini) II: Evolutionary processes and morphological integration. Journal of Evolutionary Biology, 17(1), 144–155. doi:10.1046/j.1420-9101.2003.00653.x.

    Article  CAS  PubMed  Google Scholar 

  • Marroig, G., Melo, D. A. R., & Garcia, G. (2012). Modularity, noise and natural selection. Evolution, 66(5), 1506–1524. doi:10.1111/j.1558-5646.2011.01555.x.

    Article  PubMed  Google Scholar 

  • Marroig, G., Shirai, L. T., Porto, A., de Oliveira, F., & de Conto, V. (2009). The evolution of modularity in the mammalian skull II: Evolutionary consequences. Evolutionary Biology, 36(1), 136–148. doi:10.1007/s11692-009-9051-1.

    Article  Google Scholar 

  • Marroig, G., Melo, D., Porto, A., Sebastião, H., & Garcia, G. (2011). Selection response decomposition (SRD): A new tool for dissecting differences and similarities between matrices. Evolutionary Biology, 38(2), 225–241. doi:10.1007/s11692-010-9107-2.

    Article  Google Scholar 

  • Martínez-Abadías, N., Esparza, M., Sjøvold, T., González-José, R., Hernández, M., & Klingenberg, C.P. (2011). Pervasive genetic integration directs the evolution of human skull shape. Evolution, 66(4), 1010–1023. doi:10.5061/dryad.12g3c7ht.

  • Márquez, E. J., Cabeen, R., Woods, R. P., & Houle, D. (2012). The measurement of local variation in shape. Evolutionary Biology, 39(3), 419–439. doi:10.1007/s11692-012-9159-6.

    Article  PubMed Central  PubMed  Google Scholar 

  • Meyer, K. (2007). WOMBAT: A tool for mixed model analyses in quantitative genetics by restricted maximum likelihood (REML). Journal of Zhejiang University Science B, 8(11), 815–821. doi:10.1631/jzus.2007.B0815.

    Article  PubMed Central  PubMed  Google Scholar 

  • Meyer, K., & Kirkpatrick, M. (2008). Perils of parsimony: Properties of reduced-rank estimates of genetic covariance matrices. Genetics, 180(2), 1153–1166. doi:10.1534/genetics.108.090159.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mezey, J. G., Cheverud, J. M., & Wagner, G. P. (2000). Is the genotype/phenotype map modular? A statistical approach using mouse quantitative trait loci data. Genetics, 156, 305–311.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mitteroecker, P. (2009). The developmental basis of variational modularity: Insights from quantitative genetics, morphometrics, and developmental biology. Evolutionary Biology, 36(4), 377–385. doi:10.1007/s11692-009-9075-6.

    Article  Google Scholar 

  • Mitteroecker, P., & Bookstein, F. L. (2007). The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology, 56(5), 818–836. doi:10.1080/10635150701648029.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Polly, P. D. (2008). Developmental dynamics and g-matrices: Can morphometric spaces be used to model phenotypic evolution? Evolutionary Biology, 35(2), 83–96. doi:10.1007/s11692-008-9020-0.

    Article  Google Scholar 

  • Porto, A., 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, 36(1), 118–135.

    Article  Google Scholar 

  • Porto, A., Shirai, L. T., de Oliveira, F. B., & Marroig, G. (2013). Size variation, growth strategies, and the evolution of modularity in the mammalian skull. Evolution, 67(11), 3305–3322. doi:10.1111/evo.12177.

    Article  PubMed  Google Scholar 

  • R Core Team (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

  • Ramaesh, T., & Bard, J. B. L. (2003). The growth and morphogenesis of the early mouse mandible: A quantitative analysis. Journal of Anatomy, 203, 213–222. doi:10.1046/j.1469-7580.2003.00210.x.

    Article  PubMed Central  PubMed  Google Scholar 

  • Reusch, T., & Blanckenhorn, W. U. (1998). Quantitative genetics of the dung fly sepsis cynipsea: Cheverud’s conjecture revisited. Heredity, 81, 111–119.

    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.

    Article  Google Scholar 

  • Roff, D. A. (1997). Evolutionary quantitative genetics. New York: Chapman & Hall.

    Book  Google Scholar 

  • Roff, D. A., & Fairbairn, D. J. (2011). Path analysis of the genetic integration of traits in the sand cricket: a novel use of BLUPs. Journal of Evolutionary Biology, 1–13. doi:10.1111/j.1420-9101.2011.02315.x.

  • Rohlf, F. J. (2006). tpsDig2, version 2.6. Department of Ecology and Evolution. Stony Brook, New York: SUNY.

    Google Scholar 

  • Roseman, C. C., Kenny-Hunt, J. P., & Cheverud, J. M. (2009). Phenotypic integration without modularity: Testing hypotheses about the distribution of pleiotropic quantitative trait loci in a continuous space. Evolutionary Biology, 36(3), 282–291. doi:10.1007/s11692-009-9067-6.

    Article  Google Scholar 

  • Runcie, D. E., & Mukherjee, S. (2013). Dissecting high-dimensional phenotypes with bayesian sparse factor analysis of genetic covariance matrices. Genetics, 194(3), 753–767. doi:10.1534/genetics.113.151217.

    Article  PubMed Central  PubMed  Google Scholar 

  • Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50(5), 1766–1774.

    Article  Google Scholar 

  • Shaw, R. G. (1987). Maximum-likelihood approaches applied to quantitative genetics of natural populations. Evolution, 41, 812–826.

    Article  Google Scholar 

  • Shirai, L. T., & Marroig, G. (2010). Skull modularity in neotropical marsupials and monkeys: Size variation and evolutionary constraint and flexibility. Journal of experimental zoology Part B, Molecular and developmental evolution, 314B(June), 663–683. doi:10.1002/jez.b.21367.

    Article  Google Scholar 

  • Steppan, S. J., Adkins, R., & Anderson, J. (2004). Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology, 53, 533–553.

    Article  PubMed  Google Scholar 

  • Steppan, S. J., Phillips, P. C., & Houle, D. (2002). Comparative quantitative genetics: Evolution of the g matrix. Trends in Ecology and Evolution, 17, 320–327.

    Article  Google Scholar 

  • Theobald, D. L., & Wuttke, D. S. (2006). Empirical bayes hierarchical models for regularizing maximum likelihood estimation in the matrix gaussian procrustes problem. Proceedings of the National Academy of Sciences, 103(49), 18,521–18,527. doi:10.1073/pnas.0508445103.

    Article  CAS  Google Scholar 

  • Tiedemann, H. B., Schneltzer, E., Zeiser, S., Hoesel, B., Beckers, J., Przemeck, G. K. H., et al. (2012). From dynamic expression patterns to boundary formation in the presomitic mesoderm. PLoS Computational Biology, 8(6), e1002,586. doi:10.1371/journal.pcbi.1002586.

    Article  CAS  Google Scholar 

  • Turing, A. M. (1952). The chemical basis of morphogenesis. Philosophical Transactions of the Royal Society of London, 237(641), 37–72.

    Article  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.

    Article  Google Scholar 

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

    Google Scholar 

  • Wagner, G. P., & Altenberg, L. (1996). Perspective: Complex adaptations and the evolution of evolvability. Evolution, 50, 967–976.

    Article  Google Scholar 

  • Watson, R. A., Wagner, G. P., Pavlicev, M., Weinreich, D. M., & Mills, R. (2013). The evolution of phenotypic correlations and ‘developmental memory’. Evolution, 67(4), 1124–1138. doi:10.1111/evo.12337.

    Google Scholar 

  • Willmore, K. E., Roseman, C. C., Rogers, J., Cheverud, J. M., & Richtsmeier, J. T. (2009). Comparison of mandibular phenotypic and genetic integration between baboon and mouse. Evolutionary Biology, 36(1), 19–36. doi:10.1007/s11692-009-9056-9.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wolf, J. B., Frankino, W. A., Agrawal, A. F., Iii, E. D. B., & Moore, A. J. (2001). Developmental interactions and the constituents of quantitative variation. Evolution, 55(2), 232–245. doi:10.1111/j.0014-3820.2001.tb01289.x.

    Article  CAS  PubMed  Google Scholar 

  • Zelditch, M. L., & Carmichael, A. C. (1989). Ontogenetic variation in patterns of developmental and functional integration in skulls of sigmodon fulviventer. Evolution, 43, 814–824.

    Article  Google Scholar 

  • Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer (1st ed.). San Diego: Elsevier.

    Google Scholar 

Download references

Acknowledgments

We would like to thank N. P. Barros, A. M. Marcondes, F. Almeida, L. Araripe, J. M. Freschi for help with lab work; F. A. Machado, D. Melo, and two anonymous reviewers for comments on early drafts. We also thank D. Runcie and S. Murkherjee for help with their BSFG model codes. This work has been supported by grants from CNPq (Conselho Nacional de Pesquisa e Desenvolvimento), FAPERJ (Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro), FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo), MMA (Ministério do Meio Ambiente) and MCT (Ministério de Ciência e Tecnologia).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guilherme Garcia.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (pdf 572 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garcia, G., Hingst-Zaher, E., Cerqueira, R. et al. Quantitative Genetics and Modularity in Cranial and Mandibular Morphology of Calomys expulsus . Evol Biol 41, 619–636 (2014). https://doi.org/10.1007/s11692-014-9293-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-014-9293-4

Keywords

Navigation