Energetic tradeoffs control the size distribution of aquatic mammals

Abstract

Four extant lineages of mammals have invaded and diversified in the water: Sirenia, Cetacea, Pinnipedia, and Lutrinae. Most of these aquatic clades are larger bodied, on average, than their closest land-dwelling relatives, but the extent to which potential ecological, biomechanical, and physiological controls contributed to this pattern remains untested quantitatively. Here, we use previously published data on the body masses of 3,859 living and 2,999 fossil mammal species to examine the evolutionary trajectories of body size in aquatic mammals through both comparative phylogenetic analysis and examination of the fossil record. Both methods indicate that the evolution of an aquatic lifestyle is driving three of the four extant aquatic mammal clades toward a size attractor at ∼500 kg. The existence of this body size attractor and the relatively rapid selection toward, and limited deviation from, this attractor rule out most hypothesized drivers of size increase. These three independent body size increases and a shared aquatic optimum size are consistent with control by differences in the scaling of energetic intake and cost functions with body size between the terrestrial and aquatic realms. Under this energetic model, thermoregulatory costs constrain minimum size, whereas limitations on feeding efficiency constrain maximum size. The optimum size occurs at an intermediate value where thermoregulatory costs are low but feeding efficiency remains high. Rather than being released from size pressures, water-dwelling mammals are driven and confined to larger body sizes by the strict energetic demands of the aquatic medium.

Physiological constraints on body size distributions in Crocodyliformes

“…The findings herein, coupled with related findings for marine mammals (Gearty et al. ), suggest that broad‐scale patterns of body size evolution and the shapes of body size distributions within higher taxa are often determined by physiological constraints more than by ecological interactions or environmental fluctuations. The model that we have developed provides a physiological basis for the factors that may drive differential extinction and origination dynamics as a function of body size.…”

“…The neutral buoyancy, habitat area, and protein availability hypotheses predict relaxation of constraints on maximum body size associated with transitions from terrestrial to aquatic habitats, and therefore increases in variance that would also be associated with increases in average body size (Gearty et al. ). Contrary to the expectations associated with these hypotheses, the increase in mean and optimum size in marine crocodyliforms is associated with an increase in the minimum body size but little or no change in the maximum body size, leading to a decrease in variance.…”

“…; Gearty et al. ). We calculated these transformations using the raw parameter estimates and model‐averaged these values as above to provide metrics for describing the rate of evolution relative to units of time and the variance relative to units of mass.…”

“…Similar aquatic invasions in mammals resulted in significant and convergent increases in size (Gearty et al. ). Furthermore, the response of body size evolution to these invasions suggest that, contrary to some hypotheses for aquatic gigantism in marine tetrapods, living in water imposes stronger selection on vertebrate body size than does living on land.…”

“…As in mammals, there are many reasons that one might expect secondarily aquatic crocodyliforms to be larger than their terrestrial counterparts (Gearty et al. ). Theories involving neutral buoyancy, increased habitat area, and greater protein availability in the aquatic realm all predict relaxation of selective pressures against increase in the upper end of the body size spectrum (Schmidt‐Nielsen , ; Reynolds and Karlotski ; Anderson et al.…”