Skip to main content
Log in

Low scaling of a life history variable: Analysing eutherian gestation periods with and without phylogeny-informed statistics

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Traditionally, biological times (gestation period, longevity) are proposed to scale to body mass M as M0.25. Although phylogeny-informed statistics have become widespread, it is still sometimes assumed that in datasets comprising a very large number of species, analyses that do not and that do account for phylogeny will yield similar results. Here we show, in a large dataset on gestation period length in eutherian mammals (1214 species from 20 orders), that the allometric scaling exponent is about twice as high using conventional statistics (ordinary least squares OLS, M0.18–020) as when using phylogenetic generalised least squares (PGLS, M007-010), indicating that among closely related taxa, the scaling of gestation is much lower than generally assumed. This matches the well-known absence of scaling among different-sized breeds of domestic animal species, and indicates that changes in M must be more related to changes in development speed rather than development time among closely related species, which has implications for interpreting life history-consequences of insular dwarfism and gigantism. Only when allowing just one species per order (simulated in 100 randomised datasets of n = 20 species across 20 orders) is 0.25 included in the scaling exponent confidence interval in both OLS and PGLS. Differences in scaling at different taxonomic levels in comparative datasets may indicate evolutionary trends where successive taxonomic groups compete by fundamental variation in organismal design not directly linked to changes in M. Allometries then do not necessarily represent universal scaling rules, but snapshots of evolutionary time that depend on diversification and extinction events before the picture was taken. It is either by analysing subsets separately, or by using PGLS in large datasets, that the underlying relationships with M can then be unveiled.

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.

Similar content being viewed by others

References

  • Amoah, EA, Gelaye, S., Guthrie, P., Rexroad, C.E., 1996. Breeding season and aspects of reproduction of female goats. J. Anim. Sci. 74, 723–728.

    Article  CAS  PubMed  Google Scholar 

  • Andersen, H., Plum, M., 1965. Gestation length and birth weight in cattle and buffaloes: a review. J. Dairy Sci. 48, 1224–1235.

    Article  CAS  PubMed  Google Scholar 

  • Baker, R.H., 2002. Comparative methods. In: DeSalle, R., Giribet, G., Wheeler, W. (Eds.), Techniques in Molecular Systematics and Evolution. Birkhäuser Verlag, Basel, pp. 146–161.

    Chapter  Google Scholar 

  • Benton, M.J., Csiki, Z., Grigorescu, D., Redelstorff, R., Sander, P.M., Stein, K., Weishampel, D.B., 2010. Dinosaurs and the island rule: the dwarfed dinosaurs from Hateg Island. Palaeogeogr. Palaeoclimatol. Palaeoecol. 293, 438–454.

    Article  Google Scholar 

  • Bernstein, R.M., 2010. The big and the small of it: how body size evolves. Yearb. Phys. Anthropol. 53, 46–62.

    Article  Google Scholar 

  • Bininda-Emonds, O.R.P., Cardillo, M., Jones, K.E., MacPhee, R.D.E., Beck, R.M.D., Grenyer, R., Price, S.A., Vos, R.A., Gittleman, J.L., Purvis, A., 2007. The delayed rise of present-day mammals. Nature 446, 507–512.

    Article  CAS  PubMed  Google Scholar 

  • Bininda-Emonds, O.R.P., Cardillo, M., Jones, K.E., MacPhee, R.D.E., Beck, R.M.D., Grenyer, R., Price, S.A., Vos, R.A., Gittleman, J.L, Purvis, A., 2008. Corrigendum: The delayed rise of present-day mammals. Nature 456, 274.

    Article  CAS  Google Scholar 

  • Bonner, J.T., 2006. Why Size Matters. Princeton University Press, Princeton.

    Google Scholar 

  • Bos, H., Van der Mey, G.J.W., 1980. Length of gestation periods of horses and ponies belonging to different breeds. Livest. Prod. Sci. 7, 181–187.

    Article  Google Scholar 

  • Bradford, G.E., Hart, R., Quirke, J.F., Land, R.B., 1972. Genetic control of the duration of gestation in sheep. J. Reprod. Fertil. 30, 459–463.

    Article  CAS  PubMed  Google Scholar 

  • Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M., West, G.B., 2004. Towards a metabolic theory of ecology. Ecology 85, 1771–1789.

    Article  Google Scholar 

  • Brown, J.H., Sibly, R.M., Kodric-Brown, A., 2012. Introduction: metabolism as the basis for a theoretical unification of ecology. In: Sibly, R.M., Brown, J.H., Kodric-Brown, A. (Eds.), Metabolic Ecology. A Scaling Approach. Wiley-Blackwell, Chichester, UK, pp. 1–6.

    Google Scholar 

  • Calder, W.A., 1984. Size, Function, and Life History. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Capellini, I., Venditi, C, Barton, R.A., 2010. Phylogenyand metabolic scaling in mammals. Ecology 91, 2783–2793.

    Article  PubMed  Google Scholar 

  • Carvalho, P., Diniz-Filho, J., Bini, L., 2006. Factors influencing changes in trait correlations across species after using phylogenetic independent contrasts. Evol. Ecol. 20, 591–602.

    Article  Google Scholar 

  • Crew, F.A.E., 1923. The significance of an achondroplasia-like condition met with in cattle. Proc. R. Soc. Lond. B 95, 228–255.

    Article  Google Scholar 

  • Dirks, W., Bromage, T.G., Agenbroad, L.D., 2012. The duration and rate of molar plate formation in Palaeoloxodon cypriotes and Mammuthus columbi from dental histology. Quatern. Int. 255, 79–85.

    Article  Google Scholar 

  • Dubman, E., Collard, M., Mooers, A.Ø., 2012. Evidence that gestation duration and lactation duration are coupled traits in primates. Biol. Lett. 8, 998–1001.

    Article  PubMed  PubMed Central  Google Scholar 

  • Egset, C.K., ansen, T.F., Le Rouzic, A., Bolstad, G.H., Rosenqvist, G., Pélabon, C, 2012. Artificial selection on allometry: change in elevation but not slope. J. Evol. Biol. 25, 938–948.

    Article  CAS  PubMed  Google Scholar 

  • Freckleton, R.P., Harvey, P.H., Pagel, M., 2002. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726.

    Article  CAS  PubMed  Google Scholar 

  • Fritz, J., Hummel, J., Kienzle, E., Arnold, C, Nunn, C, Clauss, M., 2009. Comparative chewing efficiency in mammalian herbivores. Oikos 118, 1623–1632.

    Article  Google Scholar 

  • Geist, V., 1966. The evolution of horn-like organs. Behaviour 27, 175–214.

    Article  Google Scholar 

  • Grange, S., Duncan, P., 2006. Bottom-up and top-down processes in African ungulate communities: resources and predation acting on the relative abundance of zebra and grazing bovids. Ecography 29, 899–907.

    Article  Google Scholar 

  • Grange, S., Duncan, P., Gaillard, J.-M., Sinclair, A.R.E., Gogan, P.J.P., Packer, C, Heribert, H., East, M., 2004. What limits the Serengeti zebra population? Oecologia 140, 523–532.

    Article  PubMed  Google Scholar 

  • Hamilton, M.J., Davidson, A.D., Sibly, R.M., Brown, J.H., 2011. Universal scaling of production rates across mammalian lineages. Proc. R. Soc. Lond. B 278, 560–566.

    Article  Google Scholar 

  • Harvey, P.H., Pagel, M.D., 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.

    Google Scholar 

  • Hennemann, W.W., 1984. Intrinsic rates of natural increase of altricial and precocial eutherian mammals: the potential price of precociality. Oikos 43, 363–368.

    Article  Google Scholar 

  • Jollans, J.L., 1960. A study of the West African dwarf sheep in the closed forest zone of Ashanti. West Afr. J. Biol. Chem. 3, 74–80.

    Google Scholar 

  • Jones, K.E., Purvis, A., 1997. An optimum body size for mammals? Comparative evidence from bats. Funct. Ecol. 11, 751–756.

    Article  Google Scholar 

  • Jones, K.E., Bielby, J., Cardillo, M., Fritz, S.A., O’Dell, J., Orme, CD., Safi, K., Sechrest, W., Boakes, E.H., Carbone, C, Connolly, C, Cutts, M.J., Foster, J.K., Grenyer, R., Habib, M., Plaster, C.A., Price, S.A., Rigby, E.A., Rist, J., Teacher, A., Bininda-Emonds, O.R.P., Gittleman, J.L., Mace, G.M., Purvis, A., 2009. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648 (Ecological Archives E2090–2184).

    Article  Google Scholar 

  • Jordana, X., Köhler, M., 2011. Enamel microstructure in the fossil bovid Myotragus balearicus (Majorca, Spain): implications for life-history evolution of dwarf mammals in insular ecosystems. Palaeogeogr. Palaeoclimatol. Palaeoecol. 300, 59–66.

    Article  Google Scholar 

  • Jordana, X., Marín-Moratalla, N., DeMiguel, D., Kaiser, T.M., Köhler, M., 2012. Evidence of correlated evolution of hypsodonty and exceptional longevity in endemic insular mammals. Proc. R. Soc. Lond. B 279, 3339–3346.

    Article  Google Scholar 

  • Kihlström, J.E., 1972. Period of gestation and body weight in some placental mammals. Comp. Biochem. Physiol. A 43, 673–679.

    Article  PubMed  Google Scholar 

  • King Wilson, W., Dudley, F.J., 1952. The duration of gestation in rabbit breeds and crosses. J. Genet. 50, 384–391.

    Article  Google Scholar 

  • Kirkwood, J.K., 1985. The influence of size on the biology of the dog. J. Small Anim. Pract. 26, 97–110.

    Article  Google Scholar 

  • Köhler, M., Moyà-Solà, S., 2009. Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proc. Natl. Acad. Sci. U. S. A. 106, 20354–20358.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kozlowski, J., Weiner, J., 1997. Interspecific allometries are by-products of body size optimization. Am. Nat. 149, 352–380.

    Article  Google Scholar 

  • Lindstedt, S.L, Calder, W.A.I., 1981. Body size, physiological time and longevity of homeothermic animals. Q. Rev. Biol. 56, 1–16.

    Article  Google Scholar 

  • Martin, R.D., MacLarnon, A.M., 1985. Gestation period, neonatal size and maternal investment in placental mammals. Nature 313, 220–223.

    Article  Google Scholar 

  • Martin, R.D., Genoud, M., Hemelrijk, C.K., 2005. Problems of allometric scaling analysis: examples from mammalian reproductive biology. J. Exp. Biol. 208, 1731–1747.

    Article  PubMed  Google Scholar 

  • Meiri, S., Raia, P., 2010. Reptilian all the way? Proc. Natl. Acad. Sci. U. S. A. 107, E27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller, D.W.H., Codron, D., Werner, J., Fritz, J., Hummel, J., Griebeler, E.M., Clauss, M., 2012. Dichotomy of eutherian reproduction and metabolism. Oikos 121, 102–115.

    Article  Google Scholar 

  • Müller, D.W.H., Codron, D., Meloro, C, Munn, A., Schwarm, A., Hummel, J., Clauss, M., 2013. Assessing the Jarman-Bell principle: scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores. Comp. Biochem. Physiol. A 164, 129–140.

    Article  CAS  Google Scholar 

  • Müller, D.W.H., Zerbe, P., Codron, D., Clauss, M., Hatt, J.-M., 2011. A long life among ruminants: giraffids and other special cases. Schweiz. Arch. Tierheilkd. 153, 515–519.

    Article  PubMed  Google Scholar 

  • Nunn, C.L., 2011. The Comparative Approach in Evolutionary Anthropology and Biology. University of Chicago Press, Chicago.

    Book  Google Scholar 

  • Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., 2010. Caper: comparative analyses of phylogenetics and evolution in R. R package version 04/r71. See http://wwwR-ForgeR-projectorg/projects/caper/

  • Pagel, M., 1999. Inferring the historical patterns of biological evolution. Nature 401, 877–884.

    Article  CAS  PubMed  Google Scholar 

  • Palombo, M.R., 2007. How can endemic proboscideans help us understand the “island rule”? A case study of Mediterranean islands. Quatern. Int. 169/170, 105–124.

    Google Scholar 

  • Paradis, E., Claude, J., Strimmer, K., 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.

    Article  CAS  PubMed  Google Scholar 

  • Peters, R.H., 1983. The Ecological Implications of Body Size. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., R Development Core Team, 2011. Nlme: linear and nonlinear mixed effects models. R package version 31–102. Available at http://cranrprojectorg/web/packages/nlme/citationhtml

  • Raia, P., Barbera, C, Conte, M., 2003. The fast life of a dwarfed giant. Evol. Ecol. 15, 293–312.

    Article  Google Scholar 

  • Revell, L.J., 2010. Phylogenetic signal and linear regression on species data. Methods Ecol. Evol. 1, 319–329.

    Article  Google Scholar 

  • Revell, L.J., 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223.

    Article  Google Scholar 

  • Ricklefs, R.E., Starck, J.M., 1996. Applications of phylogenetically independent contrasts: a mixed progress report. Oikos 77, 167–172.

    Article  Google Scholar 

  • Roth, V.L., 1990. Island dwarf elephants: a case study in body mass estimatio and ecological inference. In: Damuth, J., MacFadden, J.B. (Eds.), Body Size in Mammalian Paleobiology. Cambridge University Press, New York, pp. 51–179.

    Google Scholar 

  • Roth, V.L, 1992. Inferences from allometry and fossils: dwarfing elephant on islands. In: Futuyma, D., Antonovics, J. (Eds.), Oxford Surveys in Evolutionary Biology, vol. 8. Oxford University Press, New York, pp. 259–288.

    Google Scholar 

  • Sander, P.M., Klein, N., Buffetaut, E.,Cuny, G., Suteethorn, V., Le Loeuff, J., 2004. Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration. Organ. Divers. Evol. 4, 165–173.

    Article  Google Scholar 

  • Sander, P.M., Mateus, O., Laven, T., Knötschke, N., 2006. Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature 441, 739–741.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt-Nielsen, K., 1984. Scaling: Why is Animal Size so Important? Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Sibly, R.M., 2012. Life history. In: Sibly, R.M., Brown, J.H., Kodric-Brown, A. (Eds.), Metabolic Ecology. A Scaling Approach. Wiley-Blackwell, Chichester, UK, pp. 57–66.

    Chapter  Google Scholar 

  • Sibly, R.M., Brown, J.H., Kodric-Brown, A. (Eds.), 2012. Metabolic Ecology. A Scaling Approach. Wiley-Blackwell, Chichester, UK.

    Google Scholar 

  • Sieg, A.E., O’Connor, M.P., McNair, J.N., Grant, B.W., Agosta, S.J., Dunham, A.E., 2009. Mammalian metabolic allometry: do intraspecific variation, phylogeny, and regression models matter? Am. Nat. 174, 720–733.

    Google Scholar 

  • Stein, K., Csiki, Z., Curry Rogers, K., Weishampel, D.B., Redelstorff, R., Carballido, J.L., Sander, P.M., 2010. Small body size and extreme cortical bone remodeling indicate phyletic dwarfism in Magyarosaurus dacus (Sauropoda: Titanosauria). Proc. Natl. Acad. Sci. U. S. A. 107, 9258–9263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Team RDC, 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0 http://wwwR-projectorg/

  • Western, D., 1979. Size, life history and ecology in mammals. Afr. J. Ecol. 17, 185–204.

    Article  Google Scholar 

  • White, C.R., Blackburn, T.M., Seymour, R.S., 2009. Phylogenetically informed analysis of the allometry of mammalian basal metabolic rate supports neither geometric nor quarter-power scaling. Evolution 63, 2658–2667.

    Article  PubMed  Google Scholar 

  • White, E.P., Xiao, X., Isaac, N.J.B., Sibly, R.M., 2012. Methodological tools. In: Sibly, R.M., Brown, J.H., Kodric-Brown, A. (Eds.), Metabolic Ecology. A Scaling Approach. Wiley-Blackwell, Chichester, UK, pp. 9–20.

    Google Scholar 

  • Zerbe, P., Clauss, M., Codron, D., Bingaman Lackey, L., Rensch, E., Streich, W.J., Hatt, J.M., Müller, D.H.W., 2012. Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation, photoperiodic control, and life history. Biol. Rev. 87, 965–990.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marcus Clauss.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clauss, M., Dittmann, M.T., Müller, D.W.H. et al. Low scaling of a life history variable: Analysing eutherian gestation periods with and without phylogeny-informed statistics. Mamm Biol 79, 9–16 (2014). https://doi.org/10.1016/j.mambio.2013.01.002

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2013.01.002

Keywords

Navigation