Skip to main content
Log in

Comparative Quantitative Genetics of the Pelvis in Four-Species of Rodents and the Conservation of Genetic Covariance and Correlation Structure

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

Abstract

Quantitative genetics is a powerful tool for predicting phenotypic evolution on a microevolutionary scale. This predictive power primarily comes from the Lande equation (Δ = ), a multivariate expansion of the breeder’s equation, where phenotypic change (Δ) is predicted from the genetic covariances (G) and selection (β). Typically restricted to generational change, evolutionary biologists have proposed that quantitative genetics could bridge micro- and macroevolutionary patterns if predictions were expanded to longer timescales. While mathematically possible, making quantitative genetic predictions across generations or species is contentiously debated, principally in assuming long-term stability of the G-matrix. Here we tested stability at a macroevolutionary timescale by conducting full- and half-sib breeding programs in two species of sigmodontine rodents from South America, the leaf-eared mice Phyllotis vaccarum and P. darwini and estimated the G-matrices for eight pelvic traits. To expand our phylogenetic breadth, we incorporated two additional G-matrices measured for the same traits from Kohn & Atchley’s 1988 study of the murine rodents Mus musculus and Rattus norvegicus. Using a phylogenetic comparative framework and four separate metrics of matrix divergence or similarity, we found no significant association between evolutionary divergence among species G-matrices and time, supporting the assumption of stability for at least some structures. However, the phylogenetic sample size is necessarily small. We suggest that small fluctuations in covariance structure can occur rapidly, but underlying developmental regulation prevents significant divergence at macroevolutionary scales, analogous to an Ornstein–Uhlenbeck pattern. Expanded taxonomic sampling will be needed to test this suggestion.

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.

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

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

Code Availability

Statistical code available by request.

References

  • Agrawal, A. F., & Stinchcombe, J. R. (2009). How much do genetic covariances alter the rate of adaptation? Proceedings of the Royal Society of London B: Biological Sciences, 276(1659), 1183–1191.

    Google Scholar 

  • Aguirre, J., Hine, E., McGuigan, K., & Blows, M. (2014). Comparing G: Multivariate analysis of genetic variation in multiple populations. Heredity, 112(1), 21.

    CAS  PubMed  Google Scholar 

  • Arnold, S. J., Bürger, R., Hohenlohe, P. A., Ajie, B. C., & Jones, A. G. (2008). Understanding the evolution and stability of the G-matrix. Evolution, 62(10), 2451–2461.

    PubMed  PubMed Central  Google Scholar 

  • Atchley, W. R., & Rutledge, J. J. (1980). Genetic components of size and shape. I. Dynamics of components of phenotypic variability and covariability during ontogeny in the laboratory rat. Evolution, 34, 1161–1173.

    PubMed  Google Scholar 

  • Atchley, W. R., Rutledge, J. J., & Cowley, D. E. (1981). Genetic components of size and shape. II. Multivariate covariance patterns in the rat and mouse skull. Evolution, 35(6), 1037–1055.

    PubMed  Google Scholar 

  • Baker, R. H., & Wilkinson, G. S. (2003). Phylogenetic analysis of correlation structure in stalk-eyed flies (Diasemopsis diopsidae). Evolution, 57(1), 87–103.

    PubMed  Google Scholar 

  • Baker, R. L., Chapman, A. B., & Wardell, R. T. (1975). Direct response to selection for postweaning gain in the rat. Genetics, 80(1), 171–189. https://doi.org/10.1093/genetics/80.1.171

    Article  PubMed  PubMed Central  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.

    PubMed  PubMed Central  Google Scholar 

  • Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57(4), 717–745.

    PubMed  Google Scholar 

  • Bolstad, G. H., Hansen, T. F., Pélabon, C., Falahati-Anbaran, M., Pérez-Barrales, R., & Armbruster, W. S. (2014). Genetic constraints predict evolutionary divergence in Dalechampia blossoms. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1649), 20130255.

    Google Scholar 

  • Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36(3), 499–516.

    PubMed  Google Scholar 

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

    Google Scholar 

  • 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(1), 5–42.

    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(2), 461–469.

    Google Scholar 

  • Cheverud, J. M., Leamy, L. J., Atchley, W. R., & Rutledge, J. (1983a). Quantitative genetics and the evolution of ontogeny: I. Ontogenetic changes in quantitative genetic variance components in random bred mice. Genetics Research, 42(1), 65–75.

    Google Scholar 

  • Cheverud, J. M., Rutledge, J., & Atchley, W. R. (1983b). Quantitative genetics of development: Genetic correlations among age-specific trait values and the evolution of ontogeny. Evolution, 37(5), 895–905.

    PubMed  Google Scholar 

  • Coutinho, L. C., de Oliveira, J. A., & Pessôa, L. M. (2013). Morphological variation in the appendicular skeleton of Atlantic forest sigmodontine rodents. Journal of Morphology, 274(7), 779–792. https://doi.org/10.1002/jmor.20134

    Article  PubMed  Google Scholar 

  • De Oliveira, F. B., Porto, A., & Marroig, G. (2009). Covariance structure in the skull of Catarrhini: A case of pattern stasis and magnitude evolution. Journal of Human Evolution, 56(4), 417–430.

    PubMed  Google Scholar 

  • Dietz, E. J. (1983). Permutation tests for association between two distance matrices. Sytematic Zoology, 32, 21–26.

    Google Scholar 

  • Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125(1), 1–15.

    Google Scholar 

  • Garcia, C. (2012). A simple procedure for the comparison of covariance matrices. BM Evolutionary Biology, 12(1), 222.

    Google Scholar 

  • Haber, A. (2016). Phenotypic covariation and morphological diversification in the ruminant skull. The American Naturalist, 187(5), 576–591.

    PubMed  Google Scholar 

  • Hansen, T. F. (1997). Stabilizing selection and the comparative analysis of adaptation. Evolution, 51(5), 1341–1351.

    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.

    CAS  PubMed  Google Scholar 

  • Houle, D., Mezey, J., & Galpern, P. (2002). Interpretation of the results of common principal components analyses. Evolution; International Journal of Organic Evolution, 56(3), 433–440.

    PubMed  Google Scholar 

  • Jayat, P. J., Teta, P., Ojeda, A. A., Ortiz, P. E., Novillo, A., Lanzone, C., Osland, J. M., Steppan, S. J., & Ojeda, R. A. (2021). Systematics of the Phyllotis xanthopygus species complex (Rodentia, Cricetidae) in the central Andes, with the description of a new species from central-western Argentina. Zoologica Scripta, 50(6), 689–706.

    Google Scholar 

  • Jones, A. G., Arnold, S. J., & Bürger, R. (2003). Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution, 57(8), 1747–1760.

    PubMed  Google Scholar 

  • Kingsolver, J. G., Hoekstra, H. E., Hoekstra, J. M., Berrigan, D., Vignieri, S. N., Hill, C., Hoang, A., Gibert, P., & Beerli, P. (2001). The strength of phenotypic selection in natural populations. The American Naturalist, 157(3), 245–261.

    CAS  PubMed  Google Scholar 

  • Kohn, L. A. P., & Atchley, W. R. (1988). How similar are genetic correlation structures? Data from mice and rats. Evolution, 42(3), 467–481.

    PubMed  Google Scholar 

  • Kruuk, L. E., Clutton-Brock, T. H., Slate, J., Pemberton, J. M., Brotherstone, S., & Guinness, F. E. (2000). Heritability of fitness in a wild mammal population. Proceedings of the National Academy of Sciences of the United States of America, 97(2), 698–703.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: Body size allometry. Evolution, 33(1Part2), 402–416.

    PubMed  Google Scholar 

  • Legendre, P., & Fortin, M.-J. (2010). Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Molecular Ecology Resources, 10(5), 831–844.

    PubMed  Google Scholar 

  • Lofsvold, D. (1986). Quantitative genetics of morphological differentiation in Peromyscus. I. Tests of the homogeneity of genetic covariance structure among species and subspecies. Evolution, 40, 559–573.

    PubMed  Google Scholar 

  • Matta, B., & Bitner-Mathé, B. (2004). Genetic architecture of wing morphology in Drosophila simulans and an analysis of temperature effects on genetic parameter estimates. Heredity, 93(4), 330.

    CAS  PubMed  Google Scholar 

  • McGlothlin, J. W., Kobiela, M. E., Wright, H. V., Mahler, D. L., Kolbe, J. J., Losos, J. B., & Brodie, E. D., III. (2018). Adaptive radiation along a deeply conserved genetic line of least resistance in Anolis lizards. Evolution Letters, 2(4), 310–322.

    PubMed  PubMed Central  Google Scholar 

  • Melo, D., Garcia, G., Hubbe, A., Assis, A. P., & Marroig, G. (2015). Evolqg: An R package for evolutionary quantitative genetics [version 3]. F1000Research, 4, 925.

    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. https://doi.org/10.1631/jzus.2007.B0815

    Article  PubMed  PubMed Central  Google Scholar 

  • Mezey, J. G., & Houle, D. (2003). Comparing G matrices: Are common principal components informative? Genetics, 165(1), 411–425.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Münkemüller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K., & Thuiller, W. (2012). How to measure and test phylogenetic signal. Methods in Ecology and Evolution, 3(4), 743–756.

    Google Scholar 

  • Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H., Wagner, H., & Oksanen, M. J. (2013). Package ‘vegan.’ Community Ecology Package, Version, 2(9), 1–295.

    Google Scholar 

  • Park, Y., Hansen, C., Chung, C., & Chapman, A. B. (1966). Influence of feeding regime on the effects of selection for postweaning gain in the rat. Genetics, 54(6), 1315–1327.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips, P. C., & Arnold, S. J. (1999). Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution, 53, 1506–1515.

    PubMed  Google Scholar 

  • Pigliucci, M. (2006). Genetic variance-covariance matrices: A critique of the evolutionary quantitative genetics research program. Biology and Philosophy, 21(1), 1–23.

    Google Scholar 

  • Pomikal, C., & Streicher, J. (2009). 4D-analysis of early pelvic girdle development in the mouse (Mus musculus). Journal of Morphology, 271(1), 116–126. https://doi.org/10.1002/jmor.10785

    Article  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, 36(1), 118–135.

    Google Scholar 

  • Porto, A., Schmelter, R., VandeBerg, J. L., Marroig, G., & Cheverud, J. M. (2016). Evolution of the genotype-to-phenotype map and the cost of pleiotropy in mammals. Genetics, 204(4), 1601–1612.

    PubMed  PubMed Central  Google Scholar 

  • Revell, L. J. (2007). The G matrix under fluctuating correlational mutation and selection. Evolution, 61(8), 1857–1872.

    PubMed  Google Scholar 

  • Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecology and Evolution, 3, 217–223.

    Google Scholar 

  • Revell, L. J., Harmon, L. J., & Collar, D. C. (2008). Phylogenetic signal, evolutionary process, and rate. Systematic Biology, 57(4), 591–601.

    PubMed  Google Scholar 

  • Riska, B., Atchley, W. R., & Rutledge, J. J. (1984). A genetic analysis of targeted growth in mice. Genetics, 107(1), 79–101.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roff, D. A. (1995). The estimation of genetic correlations from phenotypic correlations: A test of Cheverud’s conjecture. Heredity, 74(5), 481.

    Google Scholar 

  • Roff, D. A., & Fairbairn, D. J. (2012). A test of the hypothesis that correlational selection generates genetic correlations. Evolution, 66(9), 2953–2960.

    PubMed  Google Scholar 

  • Roff, D. A., & Mousseau, T. (2005). The evolution of the phenotypic covariance matrix: Evidence for selection and drift in Melanoplus. Journal of Evolutionary Biology, 18(4), 1104–1114.

    CAS  PubMed  Google Scholar 

  • Roff, D. A., Prokkola, J., Krams, I., & Rantala, M. (2012). There is more than one way to skin a G matrix. Journal of Evolutionary Biology, 25(6), 1113–1126.

    CAS  PubMed  Google Scholar 

  • Rossoni, D. M., Assis, A. P. A., Giannini, N. P., & Marroig, G. (2017). Intense natural selection preceded the invasion of new adaptive zones during the radiation of New World leaf-nosed bats. Scientific Reports, 7(1), 11076.

    PubMed  PubMed Central  Google Scholar 

  • Rutledge, J. J., & Chapman, A. B. (1975). Systematic cross-fostering within control lines. Journal of Animal Science, 40, 70–74.

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Schluter, D., Price, T., Mooers, A. Ø., & Ludwig, D. (1997). Likelihood of ancestor states in adaptive radiation. Evolution, 51(6), 1699–1711. https://doi.org/10.1111/j.1558-5646.1997.tb05095.x

    Article  PubMed  Google Scholar 

  • Selz, O. M., Lucek, K., Young, K. A., & Seehausen, O. (2014). Relaxed trait covariance in interspecific cichlid hybrids predicts morphological diversity in adaptive radiations. Journal of Evolutionary Biology, 27(1), 11–24. https://doi.org/10.1111/jeb.12283

    Article  CAS  PubMed  Google Scholar 

  • Steppan, S. J. (1997a). Phylogenetic analysis of phenotypic covariance structure. I. Contrasting results from matrix correlation and common principal component analyses. Evolution, 51(2), 571–586.

    PubMed  Google Scholar 

  • Steppan, S. J. (1997b). Phylogenetic analysis of phenotypic covariance structure. II. Reconstructing matrix evolution. Evolution, 51(2), 587–594.

    PubMed  Google Scholar 

  • Steppan, S. J. (2004). Phylogenetic comparative analysis of multivariate data. In M. Piggliuci & K. A. Preston (Eds.), Phenotypic integration (pp. 325–344). Oxford University Press.

    Google Scholar 

  • Steppan, S. J., & Schenk, J. J. (2017). Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS ONE, 12(8), e0183070.

    PubMed  PubMed Central  Google Scholar 

  • Steppan, S. J., Phillips, P. C., & Houle, D. (2002). Comparative quantitative genetics: Evolution of the G matrix. Trends in Ecology & Evolution, 17(7), 320–327.

    Google Scholar 

  • Turelli, M. (1988). Phenotypic evolution, constant covariances, and the maintenance of additive variance. Evolution, 42(6), 1342–1347.

    PubMed  Google Scholar 

  • Uhlenbeck, G., & Ornstein, L. (1930). On the theory of the Brownian motion. Physical Review, 36, 823–841.

    CAS  Google Scholar 

  • Walter, G. M., Aguirre, J. D., Blows, M. W., & Ortiz-Barrientos, D. (2018). Evolution of genetic variance during adaptive radiation. The American Naturalist, 191(4), 108–128.

    Google Scholar 

  • Leiva, D., Solanas, A., de Vries, H., & Kenny, D. A. (2010). DyaDA: An R package for dyadic data analysis. In Proceedings of measuring behavior 2010 (pp. 162–165).

  • Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits (Vol. 1). Sinauer Sunderland.

  • Maddison, W. P., & Maddison, D. R. (2017). Mesquite: A modular system for evolutionary analysis. Version 3.31. http://mesquiteproject.org

  • R Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria. https://www.R-project.org/

  • Roff, D. A. (2012). Evolutionary quantitative genetics. Springer Science & Business Media.

Download references

Acknowledgements

This research was supported by US National Science Foundation Grants DEB-0108422 and DEB-1754748 to SJS. We are deeply grateful to the staff of the Mammal Division at the Field Museum of Natural History, especially Bill Stanley and Bruce Patterson for the preparation of the voucher specimens used in this study, and to Juan Oyarce, for his technical assistance in capturing and caring for the animals. To David Houle for the time spent providing invaluable advice throughout this study, particularly in G-matrix estimation and statistical comparisons. Chris Klingenberg, Mihaela Pavlicev, and two anonymous reviewers provided helpful feedback on the manuscript.

Funding

US National Science Foundation Grants DEB 0108422 and DEB-1754748 to Scott Steppan.

Author information

Authors and Affiliations

Authors

Contributions

LIW, AES and SJS conceived the study. SJS acquired funding. LIW and AES managed the breeding colonies. LEC-W and CJS collected data. CJS and BMC performed analyses. CJS wrote the manuscript. LIW, BMC, and SJS edited and contributed revisions.

Corresponding author

Correspondence to Carl J. Saltzberg.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Ethical Approval

Not applicable.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saltzberg, C.J., Walker, L.I., Chipps-Walton, L.E. et al. Comparative Quantitative Genetics of the Pelvis in Four-Species of Rodents and the Conservation of Genetic Covariance and Correlation Structure. Evol Biol 49, 71–83 (2022). https://doi.org/10.1007/s11692-022-09559-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-022-09559-z

Keywords

Navigation