Skip to main content
SpringerLink
Log in

The evolution of placental mammal body sizes: evolutionary history, form, and function

  • Ecophysiology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The unimodal, right-skewed distribution, most frequently identified in contemporary descriptions of placental mammal body size distributions, masks an underlying multidistribution structure; a long-term evolutionary process that has generated a concatenation of two or three frequency distributions specific to locomotory modes (plantigrade, digitigrade and unguligrade). The Afrotropical assemblages are bimodal, with a tendency towards trimodality, whereas the Nearctic assemblage is unimodal. However, mixtures of two and three normal distributions fitted the Nearctic data well, suggesting a multidistribution structure masked by disproportionate species numbers within locomotory modes. Differences in proportional species numbers within modes between assemblages may reflect the evolutionary history of form and function. However, common interassemblage predictions of such proportions in contemporary distributions may be disguised by the relative severity of the Pleistocene megafaunal extinction (patterns supported by the fossil record), geographical scale, and taxonomic composition. A species gap occurs at body sizes around 1 kg at the interface between the largest plantigrade mammals and the smallest digitigrade mammals, coincident with the minimum interspecific variance of basal metabolic rate. In terms of the evolution of the optimal body size in the trade-off between mortality and production, there may be good historical and evolutionary reasons why we should not expect optimization to produce the same results in different zoogeographical assemblages. Moreover, the evolution of diverse mammalian forms and functions, especially with respect to predator-prey interactions and diet, render a single body size optimum untenable in the search for an energetic definition of fitness.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–C
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adkins RM, Gelke EL, Rowe D, Honeycutt RL (2001) Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Mol Biol Evol 18:777–791

    CAS  PubMed  Google Scholar 

  • Alroy J (1998) Cope’s Rule and the dynamics of body mass evolution in North American fossil mammals. Science 280:731–734

    Article  CAS  PubMed  Google Scholar 

  • Benton MJ (2000) Vertebrate palaeontology. Blackwell, London

  • Bininda-Emonds ORP, Gittleman JL, Purvis A (1999) Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev 74:143–175

    CAS  Google Scholar 

  • Blackburn TM, Gaston KJ (1994) Animal body size distributions: patterns, mechanisms and implications. Trends Ecol Evol 9:471–474

    Google Scholar 

  • Blackburn TM, Gaston KJ (1996) On being the right size: different definitions of ‘right’. Oikos 75:551–557

    Google Scholar 

  • Blackburn TM, Gaston KJ (1998) The distribution of mammal body masses. Divers Distrib 4:121–133

    Google Scholar 

  • Bokma F (2001) Evolution of body size: limitations of an energetic definition of fitness. Funct Ecol 15:696–699

    Article  Google Scholar 

  • Bowman AW, Azzalini A (1997) Applied smoothing techniques for data analysis. Clarendon, Oxford

  • Brown JH, Maurer BA (1986) Body size, ecological dominance and Cope’s rule. Nature 324:248–250

    Google Scholar 

  • Brown JH, Nicoletto PF (1991) Spatial scaling of species composition: body masses of North American land mammals. Am Nat 138:1478–1512

    Article  Google Scholar 

  • Brown JH, Marquet PA, Taper ML (1993) Evolution of body size: consequences of an energetic definition of fitness. Am Nat 142:573–584

    Article  Google Scholar 

  • Burt WH, Grossenheider RP (1976) A field guide to the mammals of America north of Mexico. Houghton Mifflin, Boston

  • Calow P (1977) Ecology, evolution and energetics: a study in metabolic adaptation. Adv Ecol Res 10:1–62

    Google Scholar 

  • Choquenot D, Bowman DMJS (1998) Marsupial megafauna, aborigines and the overhill hypothesis: application of predator-prey models to the question of Pleistocene extinction in Australia. Global Ecol Biog 7:167–180

    Article  Google Scholar 

  • Chown SL, Gaston KJ (1997) The species-body size distribution: energy, fitness and optimality. Funct Ecol 11:365–375

    Google Scholar 

  • Damuth J (1981) Population density and body size in mammals. Nature 290:699–700

    Google Scholar 

  • Demment MW, Van Soest PJ (1985) A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat 125:641–672

    Article  Google Scholar 

  • Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman & Hall, New York

  • Eizirik E, Murphy WJ, Obrien SJ (2001) Molecular dating and biogeography of the early placental mammal radiation. J Hered 92:212–219

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Flannery T (1994) The future eaters. Braziller, New York

  • Flannery TF, Gott B (1985) The Spring Creek locality: a late Pleistocene megafaunal site from southwestern Victoria. Aust Zool 21:385–422

    Google Scholar 

  • Garland T (1983a) Scaling the ecological cost of transport to body mass in terrestrial mammals. Am Nat 121:571–587

    Article  Google Scholar 

  • Garland T (1983b) The relation between maximal running speed and body mass in terrestrial mammals. J Zool (Lond) 199:157–170

    Google Scholar 

  • Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

  • Harvey PH, Pagel MD, Rees JA (1991) Mammalian metabolism and life histories. Am Nat 137:556–566

    Article  Google Scholar 

  • Hildebrand M (1974) Analysis of vertebrate structure. Wiley, New York

  • Holling CS (1992) Cross-scale morphology, geometry, and dynamics of ecosystems. Ecol Monogr 62:447–502

    Google Scholar 

  • Huchon D, Douzery EJP (2001) From the old world to the new world: a molecular chronicle of the phylogeny and biogeography of Hystricognath rodents. Mol Phylogenet Evol 20:238–251

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Kindlmann P, Dixon AFG, Dostalkova I (1999) Does body size optimization result in skewed body size distribution on a logarithmic scale? Am Nat 153:445–447

    Article  Google Scholar 

  • Kingdon J (1997) The Kingdon field guide to African mammals. Academic, London

  • Klein RG (1984) Southern African prehistory and paleoenvironments. Balkema, Boston

  • Kozłowski J (1996a) Optimal initial size and adult size of animals: consequences for macroevolution and community structure. Am Nat 147:101–114

    Article  Google Scholar 

  • Kozłowski J (1996b) Energetic definition of fitness? Yes, but not that one. Am Nat 147:1087–1091

    Article  Google Scholar 

  • Kozłowski J, Gawelczyk AT (2002) Why are species’ body size distributions usually skewed to the right? Funct Ecol 16:419–432

    Article  Google Scholar 

  • Kozłowski J, Weiner J (1997) Interspecific allometries are the by-products of body size optimization. Am Nat 149:352–380

    Article  Google Scholar 

  • Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nat 392:917–920

    CAS  PubMed  Google Scholar 

  • Kurtén B (1971) The age of mammals. Trinity, London

  • Loder N, Blackburn TM, Gaston KJ (1997) The slippery slope: towards an understanding of the body size frequency distribution. Oikos 78:195–201

    Google Scholar 

  • Lomolino MV (1985) Body size of animals on islands: the island rule reexamined. Am Nat 125:310–316

    Article  Google Scholar 

  • Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156:201–219

    PubMed  Google Scholar 

  • Lovegrove BG (2001) The evolution of body armor in mammals: plantigrade constraints of large body size. Evolution 55:1464–1473

    CAS  PubMed  Google Scholar 

  • Maglio VJ, Cooke HBS (1978) Evolution of African mammals. Harvard University Press, Massachusetts

  • Manly BFJ (1996) Are there clumps in body size distributions? Ecology 77:81–86

    Google Scholar 

  • Maree S (2002) Phylogenetic relationships and mitochondrial DNA sequence evolution in the African rodent subfamily Otomyinae (Muridae). University of Pretoria, Pretoria, South Africa

  • Mares MA (1985) Mammal faunas of xeric habitats and the Great American Interchange. In: Stehli F, Webb D (eds) The great American biotic interchange. Plenum, New York, pp 489–520

  • Mares MA (1992) Neotropical mammals and the myth of Amazonian biodiversity. Science 255:976–979

    Google Scholar 

  • Marquet PA, Taper ML (1998) On size and area: patterns of mammalian body size extremes across landmasses. Evol Ecol 12:127–139

    Article  Google Scholar 

  • Marquet PA, Navarrete SA, Castilla JC (1995) Body size, population density, and the energetic equivalence rule. J Anim Ecol 64:325–332

    Google Scholar 

  • Marshall LG (1984) Who killed cock robin: an investigation of the extinction controversy. In: Martin PS, Klein RG (eds) Quaternary extinctions: a prehistoric revolution. University of Arizona Press, Tucson, Ariz., pp 785–806

  • Martin PS (1984) Prehistoric overkill: the global model. In: Martin PS, Klein RG (eds) Quaternary extinctions, a prehistoric revolution. University of Arizona Press, Tucson, Ariz., pp 354–403

  • Matthee CA, Robinson TJ (1999) Cytochrome b phylogeny of the family Bovidae: resolution within the Alcephini, Antilopini, Neotragini, and Tragelaphini. Mol Phylogenet Evol 12:31–46

    Article  CAS  PubMed  Google Scholar 

  • Maurer BA, Brown JH, Rusler RD (1992) The micro and macro in body size evolution. Evolution 46:939–953

    Google Scholar 

  • Michaux J, Reyes A, Catzeflis F (2001) Evolutionary history of the most speciose mammals: molecular phylogeny of muroid rodents. Mol Biol Evol 18:2017–2031

    CAS  PubMed  Google Scholar 

  • Montgelard C, Bentz S, Tirard C, Verneau O, Catzeflis FM (2002) Molecular systematics of Sciurognathi (Rodentia): the mitochondrial cytochrome b and 12S rRNA genes support the Anomaluroidea (Pedetidae and Anomaluridae). Mol Phylogenet Evol 22:220–233

    Article  CAS  PubMed  Google Scholar 

  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryderk OA, Obrien SJ (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409:614–618

    Article  CAS  PubMed  Google Scholar 

  • Nowak RM, Paradiso JL (1983) Walker’s mammals of the world. Johns Hopkins University Press, Baltimore

  • Owen-Smith N (1988) Megafaunal extinctions: the conservation message from 11,000 years B.P. Conserv Biol 3:405–412

    Google Scholar 

  • Pagel M (1992) A method for the analysis of comparative data. J Theor Biol 156:431–442

    Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge

  • Querouil S, Hutterer R, Barriere P, Colyn M, Peterhans JCK, Verheyen E (2001) Phylogeny and evolution of African shrews (Mammalia:Soricidae) inferred from 16 s rRNA sequences. Mol Phylogenet Evol 20:185–195

    Article  CAS  PubMed  Google Scholar 

  • Qumsiyeh MB (1986) Phylogenetic studies of the rodent family Gerbillidae: 1. Chromosomal evolution of the southern African complex. J Mamm 67:680–692

    Google Scholar 

  • Qumsiyeh MB, Hamilton MJ, Dempster ER, Baker RJ (1991) Cytogenetics and systematics of the rodent genus Gerbillurus. J Mamm 72:89–96

    Google Scholar 

  • Raman J, Perrin MR (1997) Allozyme and isozyme variation in seven southern African elephant–shrew species. Z Saeugetierkd 62:108–116

    Google Scholar 

  • Romer AS (1966) Vertebrate palaeontology. University of Chicago Press, Chicago

  • Siemann E, Brown JH (1999) Gaps in mammalian body size distributions reexamined. Ecology 80:2788–2792

    Google Scholar 

  • Silva M, Downing JA (1995) CRC handbook of mammalian body masses. CRC Press, Boca Raton

  • Silverman BW (1981) Using kernel density estimates to investigate multimodality. J R Stat Soc B 43:97–99

    Google Scholar 

  • Silverman BW (1986) Density estimation for statistics and data analysis. Chapman & Hall, New York

  • Simpson GG (1961) Horses. Anchor, New York

  • Simpson GG (1980) Splendid isolation: the curious history of South American mammals. Yale University Press, New Haven

    Google Scholar 

  • Skinner JD, Smithers RHN (1990) The mammals of the southern African subregion. University of Pretoria, Pretoria, South Africa

  • Springer MS, Cleven GC, Madsen O, de Jong WW, Waddell VG, Amrine HM, Stanhope MJ (1997) Endemic African mammals shake the phylogenetic tree. Nature 388:61–64

    CAS  PubMed  Google Scholar 

  • Stanley SM (1973) An explanation for Cope’s rule. Evolution 27:1–26

    Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

  • Valen L van(1973) Body size and numbers of plants and animals. Evolution 27:27–35

    Google Scholar 

  • Walton AH, Nedbal MA, Honeycutt RL (2000) Evidence from intron 1 of the nuclear transthyretin (Prealbumin) gene for the phylogeny of African mole-rats (Bathyergidae). Mol Phylogenet Evol 16:467–474

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Grants from the NRF and the University of Natal Research Fund to B.G.L. financed this research. The authors are very grateful to Steven Chown for comments on the draft manuscript.

Author information

Authors and Affiliations

  1. School of Botany and Zoology, University of Natal, P/Bag X01, 3209, Scottsville, South Africa

    Barry G. Lovegrove

  2. School of Mathematics, Statistics and Information Technology, University of Natal, P/Bag X01, 3209, Scottsville, South Africa

    Linda Haines

Authors
  1. Barry G. Lovegrove
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Linda Haines
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Barry G. Lovegrove.

Appendix

Appendix

Clade I

Topology

Orders (Eizirik et al. 2001), Afrosoricidae (Chrysochloridae)(G. Bronner, personal communication), Macroscelidea (Raman and Perrin 1997) (Fig. 7).

Fig. 7
figure a

Clade I

Full size image

Divergence dates

Node A, 102.1 mya (Eizirik et al. 2001); node B, 85 mya; node C, 79.9 mya; node D, 54.8 mya (Springer et al. 1997); node E, 24.3 mya (Eizirik et al. 2001); node G, 23 mya (Benton 2000). Node F was placed arbitrarily equidistant between nodes C and E. All tip branch lengths were arbitrarily set to 2 mya. All remaining branch lengths were chosen arbitrarily . The outgroup (marsupial) branch lengths are not to scale.

Clade III

Topology

Hystricognaths and Sciurognaths (Montgelard et al. 2002), Muridae (Michaux et al. 2001), Otomyinae (Maree 2002), Bathyergidae (Walton et al. 2000), Gerbillidae (Qumsiyeh 1986; Qumsiyeh et al. 1991) (Fig. 8).

Fig. 8
figure b

Clade III

Full size image

Divergence dates

Node A, 75.1 mya (Adkins et al. 2001); node B, 45.7 mya; node C, 51.2 mya; node D, 28.9 mya (Montgelard et al. 2002); node E, 18.8 mya; node F, 9 mya; node G, 13.3 mya; node H, 9 mya; node I, 10.5 mya (Michaux et al. 2001); node J, 5 mya (Maree 2002); node K, 28 mya; node L, 48 mya; node M, 63 mya; node N, 11 mya (Huchon and Douzery 2001). Nodes O, P, Q and R were placed arbitrarily 2, 4, 6 and 8 mya earlier than node A, respectively. All tip branch lengths were arbitrarily set to 2 mya and all remaining branches of unknown length were chosen arbitrarily.

Clade IV

Topology

Bovidae (Matthee and Robinson 1999), Carnivora (Bininda-Emonds et al. 1999), Eulipotyphla (Querouil et al. 2001) (Fig. 9).

Fig. 9
figure c

Clade IV

Full size image

Divergence dates

Node A, 93.2 mya (mean estimate Eizirik et al. 2001); node G, 93.9 mya, and node I, 94.6 mya, were placed equidistant between the maximum estimate of the primate-clade IV divergence (Node F, 95.3 mya in Fig. 2) and node A. Node B, 64.7 mya (Kumar and Hedges 1998); node C, 55 mya; node J, 38 mya (Benton 2000); node D, 22.3 mya (Matthee and Robinson 1999); node H, 53.8 mya (Bininda-Emonds et al. 1999); node I, 96.3 mya (see clade 1); node K, 19.1 mya (Querouil et al. 2001). Nodes E and F were placed arbitrarily equidistant between nodes B and D.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lovegrove, B.G., Haines, L. The evolution of placental mammal body sizes: evolutionary history, form, and function. Oecologia 138, 13–27 (2004). https://doi.org/10.1007/s00442-003-1376-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-003-1376-3

Keywords

Search

Navigation