Effects of body size and lifestyle on evolution of mammal life histories

Abstract

It has recently been proposed that life-history evolution is subject to a fundamental size-dependent constraint. This constraint limits the rate at which biomass can be produced so that production per unit of body mass is inevitably slower in larger organisms than in smaller ones. Here we derive predictions for how changes in body size and production rates evolve in different lifestyles subject to this constraint. Predictions are tested by using data on the mass of neonate tissue produced per adult per year in 637 placental mammal species and are generally supported. Compared with terrestrial insectivores with generalized primitive traits, mammals that have evolved more specialized lifestyles have divergent mass-specific production rates: (i) increased in groups that specialize on abundant and reliable foods: grazing and browsing herbivores (artiodactyls, lagomorphs, perissodactyls, and folivorous rodents) and flesh-eating marine mammals (pinnipeds, cetaceans); and (ii) decreased in groups that have lifestyles with reduced death rates: bats, primates, arboreal, fossorial, and desert rodents, bears, elephants, and rhinos. Convergent evolution of groups with similar lifestyles is common, so patterns of productivity across mammalian taxa reflect both ecology and phylogeny. The overall result is that groups with different lifestyles have parallel but offset relationships between production rate and body size. These results shed light on the evolution of the fast-slow life-history continuum, suggesting that variation occurs along two axes corresponding to body size and lifestyle.

Fig. 1.

Specific production rates of 637 mammal species as a function of body mass. (A) The whole data set, showing the different orders. (B) Plot for the species in orders with ≥10 data values. Symbols as in A, except that the Carnivora have been split into suborders Fissipedia (red triangles) and Pinnipedia (blue triangles) (compare Fig. 3B). The lines are fitted by GLM so as to have the same slopes, and they are color-coded according to taxon. (C) Plot for the species in the orders not shown in B. Symbols are as in A. The pink line, shown for purposes of comparison, is for Insectivora (see text).

Fig. 2.

Normalization constants for the major taxonomic and lifestyle groupings [mean, SE (thick bars) and SD (thin bars)], obtained by using GLM to fit lines of common slope to the data in Fig. 1B. Normalization constants measure the vertical displacement of the regression lines (i.e., y intercepts) (see Table 1). SDs are presented to show the variation within each grouping (see text). The dashed horizontal line, shown for purposes of comparison, is the normalization constant for Insectivora. Symbols on shaded backgrounds depict subgroups of carnivores and rodents based on lifestyle. “Rodentia nonfolivorous” refers to rodents that are arboreal, fossorial, or desert dwelling (see SI Table 2 for classification).

Fig. 3.

Specific production rate as a function of body mass for species grouped by lifestyle. Grazers and browsers (A); baleen and toothed whales and pinnipeds (B); terrestrial (fissiped) and marine (pinniped) carnivores (C); rodents (D); frugivorous and nectarivorous (green symbols) and insectivorous (black symbols) bats in the families containing more than five species (E). The Phyllostomidae, which include carnivorous, insectivorous, and fruit-eating species (http://animaldiversity.ummz.umich.edu), are not shown. The pink line shown in each image, for purposes of comparison, is for Insectivores. Some exceptional cases are highlighted: 1, crab-eating fox (C. thous); 2, African civet (Civettictis civetta); 3, sea otter (E. lutris); 4, African wild dog (L. pictus); 5, bears of the family Ursidae; 6, naked mole rat (H. glaber). See text for discussion.

Fig. 4.

The two major axes of the slow–fast life-history continuum, body mass, and lifestyle. To the well known axis of allometric variation due to body size, we have added a second orthogonal axis based on ecological lifestyle. Here the solid line represents an unspecialized ancestral condition, the dashed line depicts a more productive “live fast die young” lifestyle, and the dotted line shows a lifestyle with a lower death rate, slower life history, and consequently lower production.